Hostname: page-component-54dcc4c588-tfzs5 Total loading time: 0 Render date: 2025-10-01T16:11:26.783Z Has data issue: false hasContentIssue false
  • English
  • Français

Visualizing transient dark states by NMR spectroscopy

Published online by Cambridge University Press:  20 January 2015

Nicholas J. Anthis  and
G. Marius Clore
Nicholas J. Anthis
Affiliation:
Laboratory of Chemical Physics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892-0520, USA
G. Marius Clore*
Affiliation:
Laboratory of Chemical Physics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892-0520, USA
*
*Author for correspondence: G. M. Clore, Laboratory of Chemical Physics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892-0520, USA. Tel.: 301 496 0782; Email: mariusc@intra.niddk.nih.gov
Get access Rights & Permissions [Opens in a new window]

Abstract

Myriad biological processes proceed through states that defy characterization by conventional atomic-resolution structural biological methods. The invisibility of these ‘dark’ states can arise from their transient nature, low equilibrium population, large molecular weight, and/or heterogeneity. Although they are invisible, these dark states underlie a range of processes, acting as encounter complexes between proteins and as intermediates in protein folding and aggregation. New methods have made these states accessible to high-resolution analysis by nuclear magnetic resonance (NMR) spectroscopy, as long as the dark state is in dynamic equilibrium with an NMR-visible species. These methods – paramagnetic NMR, relaxation dispersion, saturation transfer, lifetime line broadening, and hydrogen exchange – allow the exploration of otherwise invisible states in exchange with a visible species over a range of timescales, each taking advantage of some unique property of the dark state to amplify its effect on a particular NMR observable. In this review, we introduce these methods and explore two specific techniques – paramagnetic relaxation enhancement and dark state exchange saturation transfer – in greater detail.

Information

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 48 , Issue 1 , February 2015 , pp. 35 - 116
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

7. References

Altenbach, C., Kusnetzow, A. K., Ernst, O. P., Hofmann, K. P. & Hubbell, W. L. (2008). High-resolution distance mapping in rhodopsin reveals the pattern of helix movement due to activation. Proceedings of the National Academy of Sciences of the United States of America 105, 7439–7444.Google Scholar
Altenbach, C., Oh, K. J., Trabanino, R. J., Hideg, K. & Hubbell, W. L. (2001). Estimation of inter-residue distances in spin labeled proteins at physiological temperatures: experimental strategies and practical limitations. Biochemistry 40, 15471–15482.CrossRefGoogle ScholarPubMed
Anthis, N. J. & Clore, G. M. (2013). The length of the calmodulin linker determines the extent of transient interdomain association and target affinity. Journal of American Chemical Society 135, 9648–9651.CrossRefGoogle ScholarPubMed
Anthis, N. J., Doucleff, M. & Clore, G. M. (2011). Transient, sparsely populated compact states of apo and calcium-loaded calmodulin probed by paramagnetic relaxation enhancement: interplay of conformational selection and induced fit. Journal of American Chemical Society 133, 18966–18974.CrossRefGoogle ScholarPubMed
Babu, Y. S., Sack, J. S., Greenhough, T. J., Bugg, C. E., Means, A. R. & Cook, W. J. (1985). Three-dimensional structure of calmodulin. Nature 315, 37–40.Google Scholar
Bai, Y. & Englander, S. W. (1996). Future directions in folding: the multi-state nature of protein structure. Proteins 24, 145–151.3.0.CO;2-I>CrossRefGoogle ScholarPubMed
Bai, Y. W. (2006). Protein folding pathways studied by pulsed-and native-state hydrogen exchange. Chemical Reviews 106, 1757–1768.Google Scholar
Bai, Y. W., Sosnick, T. R., Mayne, L. & Englander, S. W. (1995). Protein-folding intermediates – native-state hydrogen-exchange. Science 269, 192–197.CrossRefGoogle ScholarPubMed
Baker, M. L., Hryc, C. F., Zhang, Q., Wu, W., Jakana, J., Haase-Pettingell, C., Afonine, P. V., Adams, P. D., King, J. A., Jiang, W. & Chiu, W. (2013). Validated near-atomic resolution structure of bacteriophage epsilon15 derived from cryo-EM and modeling. Proceedings of the National Academy of Sciences of the United States of America 110, 12301–12306.CrossRefGoogle ScholarPubMed
Balasubramaniam, D. & Komives, E. A. (2013). Hydrogen-exchange mass spectrometry for the study of intrinsic disorder in proteins. Biochimica et Biophysica Acta 1834, 1202–1209.CrossRefGoogle Scholar
Baldwin, A. J. & Kay, L. E. (2009). NMR spectroscopy brings invisible protein states into focus. Nature Chemical Biology 5, 808–814.CrossRefGoogle ScholarPubMed
Baldwin, A. J. & Kay, L. E. (2013). An R(1rho) expression for a spin in chemical exchange between two sites with unequal transverse relaxation rates. Journal of Biomolecular NMR 55, 211–218.CrossRefGoogle Scholar
Ban, D., Gossert, A. D., Giller, K., Becker, S., Griesinger, C. & Lee, D. (2012). Exceeding the limit of dynamics studies on biomolecules using high spin-lock field strengths with a cryogenically cooled probehead. Journal of Magnetic Resonance 221, 1–4.CrossRefGoogle ScholarPubMed
Ban, D., Mazur, A., Carneiro, M. G., Sabo, T. M., Giller, K., Koharudin, L. M., Becker, S., Gronenborn, A. M., Griesinger, C. & Lee, D. (2013). Enhanced accuracy of kinetic information from CT-CPMG experiments by transverse rotating-frame spectroscopy. Journal of Biomolecular NMR 57, 73–82.Google Scholar
Barbato, G., Ikura, M., Kay, L. E., Pastor, R. W. & Bax, A. (1992). Backbone dynamics of calmodulin studied by 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry 31, 5269–5278.CrossRefGoogle ScholarPubMed
Bartesaghi, A., Merk, A., Borgnia, M. J., Milne, J. L. & Subramaniam, S. (2013). Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nature Structural and Molecular Biology 20, 1352–1357.Google Scholar
Bashir, Q., Volkov, A. N., Ullmann, G. M. & Ubbink, M. (2009). Visualization of the encounter ensemble of the transient electron transfer complex of cytochrome c and cytochrome c peroxidase. Journal of American Chemical Society 132, 241–247.CrossRefGoogle Scholar
Battiste, J. L. & Wagner, G. (2000). Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data. Biochemistry 39, 5355–5365.Google Scholar
Baum, J., Dobson, C. M., Evans, P. A. & Hanley, C. (1989). Characterization of a partly folded protein by NMR methods: studies on the molten globule state of guinea pig alpha-lactalbumin. Biochemistry 28, 7–13.CrossRefGoogle ScholarPubMed
Benetis, N. & Kowalewski, J. (1985). Nuclear-spin relaxation in paramagnetic systems (S = 1) in the slow-motion regime for the electron-spin .4. Motional anisotropy andnNoncoinciding dipole-dipole and zero-field Splitting tensors. Journal of Magnetic Resonance 65, 13–33.Google Scholar
Berlin, K., Castaneda, C. A., Schneidman-Duhovny, D., Sali, A., Nava-Tudela, A. & Fushman, D. (2013). Recovering a representative conformational ensemble from underdetermined macromolecular structural data. Journal of American Chemical Society 135, 16595–16609.Google Scholar
Bermejo, G. A., Strub, M.-P., Ho, C. & Tjandra, N. (2009). Determination of the solution-bound conformation of an amino acid binding protein by NMR paramagnetic relaxation enhancement: use of a single flexible paramagnetic probe with improved estimation of its sampling space. Journal of American Chemical Society 131, 9532–9537.CrossRefGoogle ScholarPubMed
Bernado, P., Mylonas, E., Petoukhov, M. V., Blackledge, M. & Svergun, D. I. (2007). Structural characterization of flexible proteins using small-angle X-ray scattering. Journal of American Chemical Society 129, 5656–5664.Google Scholar
Bernini, A., Venditti, V., Spiga, O. & Niccolai, N. (2009). Probing protein surface accessibility with solvent and paramagnetic molecules. Progress in Nuclear Magnetic Resonance Spectroscopy 54, 278–289.CrossRefGoogle Scholar
Bertini, I., Ferella, L., Luchinat, C., Parigi, G., Petoukhov, M. V., Ravera, E., Rosato, A. & Svergun, D. I. (2012a). MaxOcc: a web portal for maximum occurrence analysis. Journal of Biomolecular NMR 53, 271–280.CrossRefGoogle ScholarPubMed
Bertini, I., Giachetti, A., Luchinat, C., Parigi, G., Petoukhov, M. V., Pierattelli, R., Ravera, E. & Svergun, D. I. (2010). Conformational space of flexible biological macromolecules from average data. Journal of American Chemical Society 132, 13553–13558.CrossRefGoogle ScholarPubMed
Bertini, I., Gupta, Y. K., Luchinat, C., Parigi, G., Peana, M., Sgheri, L. & Yuan, J. (2007). Paramagnetism-based NMR restraints provide maximum allowed probabilities for the different conformations of partially independent protein domains. Journal of the American Chemical Society 129, 12786–12794.CrossRefGoogle ScholarPubMed
Bertini, I., Luchinat, C., Nagulapalli, M., Parigi, G. & Ravera, E. (2012b). Paramagnetic relaxation enhancement for the characterization of the conformational heterogeneity in two-domain proteins. Physical Chemistry and Chemical Physics 14, 9149–9156.Google Scholar
Bertini, I., Luchinat, C. & Parigi, G. (2001a). Solution NMR of Paramagnetic Molecules: Applications to Metallobiomolecules and Models. Elsevier Science, Amsterdam.Google Scholar
Bertini, I., Luchinat, C. & Parigi, G. (2002). Magnetic susceptibility in paramagnetic NMR. Progress in Nuclear Magnetic Resonance Spectroscopy 40, 249–273.Google Scholar
Bertini, I., Luchinat, C., Parigi, G. & Pierattelli, R. (2005). NMR spectroscopy of paramagnetic metalloproteins. Chembiochem 6, 1536–1549.CrossRefGoogle ScholarPubMed
Bertini, I., Luchinat, C. & Piccioli, M. (2001b). Paramagnetic probes in metalloproteins. Methods in Enzymology 339, 314–340.Google Scholar
Bertoncini, C. W., Jung, Y. S., Fernandez, C. O., Hoyer, W., Griesinger, C., Jovin, T. M. & Zweckstetter, M. (2005). Release of long-range tertiary interactions potentiates aggregation of natively unstructured alpha-synuclein. Proceedings of the National Academy of Sciences of the United States of America 102, 1430–1435.CrossRefGoogle ScholarPubMed
Bloch, F. (1946). Nuclear induction. Physics Reviews 70, 460–474.Google Scholar
Bloembergen, N. (1957). Proton relaxation times in paramagnetic solutions. Journal of Chemical Physics 27, 572–573.Google Scholar
Bloembergen, N. & Morgan, L. O. (1961). Proton relaxation times in paramagnetic solutions effects of electron spin relaxation. Journal of Chemical Physics 34, 842–850.CrossRefGoogle Scholar
Bodner, C. R., Dobson, C. M. & Bax, A. (2009). Multiple tight phospholipid-binding modes of alpha-synuclein revealed by solution NMR spectroscopy. Journal of Molecular Biology 390, 775–790.Google Scholar
Bodner, C. R., Maltsev, A. S., Dobson, C. M. & Bax, A. (2010). Differential phospholipid binding of alpha-synuclein variants implicated in Parkinson's disease revealed by solution NMR spectroscopy. Biochemistry 49, 862–871.Google Scholar
Boehr, D. D., Dyson, H. J. & Wright, P. E. (2008). Conformational relaxation following hydride transfer plays a limiting role in dihydrofolate reductase catalysis. Biochemistry 47, 9227–9233.CrossRefGoogle Scholar
Boehr, D. D., Mcelheny, D., Dyson, H. J. & Wright, P. E. (2006). The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313, 1638–1642.Google Scholar
Boehr, D. D., Mcelheny, D., Dyson, H. J. & Wright, P. E. (2010). Millisecond timescale fluctuations in dihydrofolate reductase are exquisitely sensitive to the bound ligands. Proceedings of the National Academy of Sciences of the United States of America 107, 1373–1378.Google Scholar
Bouvignies, G. & Kay, L. E. (2012a). A 2D 13C-CEST experiment for studying slowly exchanging protein systems using methyl probes: an application to protein folding. Journal of Biomolecular NMR 53, 303–310.Google Scholar
Bouvignies, G. & Kay, L. E. (2012b). Measurement of proton chemical shifts in invisible states of slowly exchanging protein systems by chemical exchange saturation transfer. Journal of Physical Chemistry B 116, 14311–14317.Google Scholar
Bouvignies, G., Korzhnev, D. M., Neudecker, P., Hansen, D. F., Cordes, M. H. & Kay, L. E. (2010). A simple method for measuring signs of (1)H (N) chemical shift differences between ground and excited protein states. Journal of Biomolecular NMR 47, 135–141.Google Scholar
Bouvignies, G., Vallurupalli, P., Hansen, D. F., Correia, B. E., Lange, O., Bah, A., Vernon, R. M., Dahlquist, F. W., Baker, D. & Kay, L. E. (2011). Solution structure of a minor and transiently formed state of a T4 lysozyme mutant. Nature 477, 111–114.Google Scholar
Bouvignies, G., Vallurupalli, P. & Kay, L. E. (2014). Visualizing side chains of invisible protein conformers by solution NMR. Journal of Molecular Biology 426, 763–774.CrossRefGoogle ScholarPubMed
Bridges, M. D., Hideg, K. & Hubbell, W. L. (2010). Resolving conformational and rotameric exchange in spin-labeled proteins using saturation recovery EPR. Applied Magnetic Resonance 37, 363–390.Google Scholar
Bruschweiler, R., Roux, B., Blackledge, M., Griesinger, C., Karplus, M. & Ernst, R. R. (1992). Influence of rapid intramolecular motion on NMR cross-relaxation rates – a molecular-dynamics study of antamanide in solution. Journal of American Chemical Society 114, 2289–2302.Google Scholar
Bryngelson, J. D., Onuchic, J. N., Socci, N. D. & Wolynes, P. G. (1995). Funnels, pathways, and the energy landscape of protein-folding – a synthesis. Proteins 21, 167–195.CrossRefGoogle ScholarPubMed
Bryngelson, J. D. & Wolynes, P. G. (1987). Spin-glasses and the statistical-mechanics of protein folding. Proceedings of the National Academy of Sciences of the United States of America 84, 7524–7528.Google Scholar
Burnley, B. T., Afonine, P. V., Adams, P. D. & Gros, P. (2012). Modelling dynamics in protein crystal structures by ensemble refinement. eLife 1, e00311.Google Scholar
Caravan, P., Ellison, J. J., Mcmurry, T. J. & Lauffer, R. B. (1999). Gadolinium(III) chelates as MRI contrast agents: structure, dynamics, and applications. Chemical Reviews 99, 2293–2352.CrossRefGoogle ScholarPubMed
Card, P. B., Erbel, P. J. A. & Gardner, K. H. (2005). Structural basis of ARNT PAS-B dimerization: use of a common beta-sheet interface for hetero- and homodimerization. Journal of Molecular Biology 353, 664–677.CrossRefGoogle ScholarPubMed
Carr, H. Y. & Purcell, E. M. (1954). Effects of diffusion on free precession in nuclear magnetic resonance experiments. Physics Reviews 94, 630–638.CrossRefGoogle Scholar
Carver, J. P. & Richards, R. E. (1972). General 2-site solution for chemical exchange produced dependence of T2 upon Carr-Purcell pulse separation. Journal of Magnetic Resonance 6, 89–105.Google Scholar
Cavalli, A., Salvatella, X., Dobson, C. M. & Vendruscolo, M. (2007). Protein structure determination from NMR chemical shifts. Proceedings of the National Academy of Sciences of the United States of America 104, 9615–9620.CrossRefGoogle ScholarPubMed
Cavanagh, J., Fairbrother, W. J., Palmer, A. G., Skelton, N. J. & Rance, M. (2007). Protein NMR Spectroscopy: Principles and Practice. Elsevier, Amsterdam.Google Scholar
Cayley, P. J., Albrand, J. P., Feeney, J., Roberts, G. C., Piper, E. A. & Burgen, A. S. (1979). Nuclear magnetic resonance studies of the binding of trimethoprim to dihydrofolate reductase. Biochemistry 18, 3886–3895.Google Scholar
Cerofolini, L., Fields, G. B., Fragai, M., Geraldes, C. F., Luchinat, C., Parigi, G., Ravera, E., Svergun, D. I. & Teixeira, J. M. (2013). Examination of matrix metalloproteinase-1 in solution: a preference for the pro-collagenolysis state. Journal of Biological Chemistry 288, 30659–30671.Google Scholar
Chamberlain, A. K., Handel, T. M. & Marqusee, S. (1996). Detection of rare partially folded molecules in equilibrium with the native conformation of RNaseH. Nature Structural Biology 3, 782–787.CrossRefGoogle ScholarPubMed
Chamberlain, A. K. & Marqusee, S. (2000). Comparison of equilibrium and kinetic approaches for determining protein folding mechanisms. Advances in Protein Chemistry 53, 283–328.CrossRefGoogle ScholarPubMed
Cheng, H. & Markley, J. L. (1995). NMR spectroscopic studies of paramagnetic proteins: iron-sulfur proteins. Annual Review of Biophysics and Biomolecular Structure 24, 209–237.Google Scholar
Chevelkov, V., Xue, Y., Rao, D. K., Forman-Kay, J. D. & Skrynnikov, N. R. (2010). 15N H/D-SOLEXSY experiment for accurate measurement of amide solvent exchange rates: application to denatured drkN SH3. Journal of Biomolecular NMR 46, 227–244.CrossRefGoogle ScholarPubMed
Chou, J. J., Case, D. A. & Bax, A. (2003). Insights into the mobility of methyl-bearing side chains in proteins from (3)J(CC) and (3)J(CN) couplings. Journal of American Chemical Society 125, 8959–8966.Google Scholar
Choy, W. Y. & Forman-Kay, J. D. (2001). Calculation of ensembles of structures representing the unfolded state of an SH3 domain. Journal of Molecular Biology 308, 1011–1032.Google Scholar
Chu, R., Pei, W., Takei, J. & Bai, Y. (2002). Relationship between the native-state hydrogen exchange and folding pathways of a four-helix bundle protein. Biochemistry 41, 7998–8003.Google Scholar
Cliff, M. J., Craven, C. J., Marston, J. P., Hounslow, A. M., Clarke, A. R. & Waltho, J. P. (2009). The denatured state of N-PGK Is compact and predominantly disordered. Journal of Molecular Biology 385, 266–277.Google Scholar
Clore, G. M. (2000). Accurate and rapid docking of protein-protein complexes on the basis of intermolecular nuclear Overhauser enhancement data and dipolar couplings by rigid body minimization. Proceedings of the National Academy of Sciences of the United States of America 97, 9021–9025.CrossRefGoogle ScholarPubMed
Clore, G. M. (2008). Visualizing lowly-populated regions of the free energy landscape of macromolecular complexes by paramagnetic relaxation enhancement. Molecular Biosystems 4, 1058–1069.CrossRefGoogle ScholarPubMed
Clore, G. M. (2011). Exploring sparsely populated states of macromolecules by diamagnetic and paramagnetic NMR relaxation. Protein Science 20, 229–246.Google Scholar
Clore, G. M. (2013). Interplay between conformational selection and induced fit in multidomain protein-ligand binding probed by paramagnetic relaxation enhancement. Biophysical Chemistry 186, 3–12.Google Scholar
Clore, G. M. & Bewley, C. A. (2002). Using conjoined rigid body/torsion angle simulated annealing to determine the relative orientation of covalently linked protein domains from dipolar couplings. Journal of Magnetic Resonance 154, 329–335.Google Scholar
Clore, G. M., Driscoll, P. C., Wingfield, P. T. & Gronenborn, A. M. (1990a). Analysis of the backbone dynamics of interleukin-1 beta using two-dimensional inverse detected heteronuclear 15N-1H NMR spectroscopy. Biochemistry 29, 7387–7401.Google Scholar
Clore, G. M. & Gronenborn, A. M. (1982). Theory and applications of the transferred nuclear overhauser effect to the study of the conformations of small ligands bound to proteins. Journal of Magnetic Resonance 48, 402–417.Google Scholar
Clore, G. M. & Gronenborn, A. M. (1983). Theory of the time-dependent transferred nuclear overhauser effect – applications to structural-analysis of ligand protein complexes in solution. Journal of Magnetic Resonance 53, 423–442.Google Scholar
Clore, G. M. & Gronenborn, A. M. (1991). Structures of larger proteins in solution – 3-dimensional and 4-dimensional heteronuclear nmr-spectroscopy. Science 252, 1390–1399.Google Scholar
Clore, G. M. & Gronenborn, A. M. (1998). New methods of structure refinement for macromolecular structure determination by NMR. Proceedings of the National Academy of Sciences of the United States of America 95, 5891–5898.CrossRefGoogle ScholarPubMed
Clore, G. M. & Iwahara, J. (2009). Theory, practice, and applications of paramagnetic relaxation enhancement for the characterization of transient low-population states of biological macromolecules and their complexes. Chemical Reviews 109, 4108–4139.Google Scholar
Clore, G. M. & Schwieters, C. D. (2004a). Amplitudes of protein backbone dynamics and correlated motions in a small alpha/beta protein: correspondence of dipolar coupling and heteronuclear relaxation measurements. Biochemistry 43, 10678–10691.Google Scholar
Clore, G. M. & Schwieters, C. D. (2004b). How much backbone motion in ubiquitin is required to account for dipolar coupling data measured in multiple alignment media as assessed by independent cross-validation? Journal of American Chemical Society 126, 2923–2938.CrossRefGoogle Scholar
Clore, G. M. & Schwieters, C. D. (2006). Concordance of residual dipolar couplings, backbone order parameters and crystallographic B-factors for a small alpha/beta protein: a unified picture of high probability, fast atomic motions in proteins. Journal of Molecular Biology 355, 879–886.Google Scholar
Clore, G. M., Szabo, A., Bax, A., Kay, L. E., Driscoll, P. C. & Gronenborn, A. M. (1990b). Deviations from the simple two-parameter model-free approach to the interpretation of N-15 nuclear magnetic-relaxation of proteins. Journal of American Chemical Society 112, 4989–4991.Google Scholar
Clore, G. M., Tang, C. & Iwahara, J. (2007). Elucidating transient macromolecular interactions using paramagnetic relaxation enhancement. Current Opinion in Structural Biology 17, 603–616.CrossRefGoogle ScholarPubMed
Cole, R. & Loria, J. P. (2002). Evidence for flexibility in the function of ribonuclease A. Biochemistry 41, 6072–6081.Google Scholar
Columbus, L., Kalai, T., Jeko, J., Hideg, K. & Hubbell, W. L. (2001). Molecular motion of spin labeled side chains in alpha-helices: analysis by variation of side chain structure. Biochemistry 40, 3828–3846.Google Scholar
Conicella, A. E. & Fawzi, N. L. (2014). The C-terminal threonine of Abeta43 nucleates toxic aggregation via structural and dynamical changes in monomers and protofibrils. Biochemistry 20, 3095–3105.Google Scholar
Crisma, M., Deschamps, J. R., George, C., Flippen-Anderson, J. L., Kaptein, B., Broxterman, Q. B., Moretto, A., Oancea, S., Jost, M., Formaggio, F. & Toniolo, C. (2005). A topographically and conformationally constrained, spin-labeled, alpha-amino acid: crystallographic characterization in peptides. Journal of Peptide Research 65, 564–579.Google Scholar
Dasgupta, S., Hu, X., Keizers, P. H. J., Liu, W.-M., Luchinat, C., Nagulapalli, M., Overhand, M., Parigi, G., Sgheri, L. & Ubbink, M. (2011). Narrowing the conformational space sampled by two-domain proteins with paramagnetic probes in both domains. Journal of Biomolecular NMR 51, 253–263.Google Scholar
Davis, D. G., Perlman, M. E. & London, R. E. (1994). Direct measurements of the dissociation-rate constant for inhibitor-enzyme complexes via the T1 rho and T2 (CPMG) methods. Journal of Magnetic Resonance B 104, 266–275.Google Scholar
Dedmon, M. M., Lindorff-Larsen, K., Christodoulou, J., Vendruscolo, M. & Dobson, C. M. (2005). Mapping long-range interactions in alpha-synuclein using spin-label NMR and ensemble molecular dynamics simulations. Journal of American Chemical Society 127, 476–477.Google Scholar
Dedmon, M. M., Patel, C. N., Young, G. B. & Pielak, G. J. (2002). FlgM gains structure in living cells. Proceedings of the National Academy of Sciences of the United States of America 99, 12681–12684.CrossRefGoogle ScholarPubMed
Deshmukh, L., Schwieters, C. D., Grishaev, A., Ghirlando, R., Baber, J. L. & Clore, G. M. (2013). Structure and dynamics of full-length HIV-1 capsid protein in solution. Journal of American Chemical Society 135, 16133–16147.Google Scholar
Deverell, C., Morgan, R. E. & Strange, J. H. (1970). Studies of chemical exchange by nuclear magnetic relaxation in rotating frame. Molecular Physics 18, 553–559.Google Scholar
Dharmasiri, K. & Smith, D. L. (1996). Mass spectrometric determination of isotopic exchange rates of amide hydrogens located on the surfaces of proteins. Analytical Chemistry 68, 2340–2344.Google Scholar
Donaldson, L. W., Skrynnikov, N. R., Choy, W. Y., Muhandiram, D. R., Sarkar, B., Forman-Kay, J. D. & Kay, L. E. (2001). Structural characterization of proteins with an attached ATCUN motif by paramagnetic relaxation enhancement NMR spectroscopy. Journal of American Chemical Society 123, 9843–9847.CrossRefGoogle ScholarPubMed
Dvoretsky, A., Gaponenko, V. & Rosevear, P. R. (2002). Derivation of structural restraints using a thiol-reactive chelator. FEBS Letters 528, 189–192.CrossRefGoogle ScholarPubMed
Ebright, Y. W., Chen, Y., Pendergrast, P. S. & Ebright, R. H. (1992). Incorporation of an EDTA-metal complex at a rationally selected site within a protein – application to EDTA-iron DNA affinity cleaving with catabolite gene activator protein (CAP) and Cro. Biochemistry 31, 10664–10670.Google Scholar
Ehrhardt, M. R., Urbauer, J. L. & Wand, A. J. (1995). The energetics and dynamics of molecular recognition by calmodulin. Biochemistry 34, 2731–2738.Google Scholar
Eichmuller, C. & Skrynnikov, N. R. (2007). Observation of microsecond time-scale protein dynamics in the presence of Ln3+ ions: application to the N-terminal domain of cardiac troponin C. Journal of Biomolecular NMR 37, 79–95.Google Scholar
Eisenmesser, E. Z., Millet, O., Labeikovsky, W., Korzhnev, D. M., Wolf-Watz, M., Bosco, D. A., Skalicky, J. J., Kay, L. E. & Kern, D. (2005). Intrinsic dynamics of an enzyme underlies catalysis. Nature 438, 117–121.CrossRefGoogle ScholarPubMed
Englander, J. J., Del Mar, C., Li, W., Englander, S. W., Kim, J. S., Stranz, D. D., Hamuro, Y. & Woods, V. L. Jr. (2003). Protein structure change studied by hydrogen-deuterium exchange, functional labeling, and mass spectrometry. Proceedings of the National Academy of Sciences of the United States of America 100, 7057–7062.Google Scholar
Englander, S. W. (2006). Hydrogen exchange and mass spectrometry: a historical perspective. Journal of American Society for Mass Spectrometry 17, 1481–1489.Google Scholar
Englander, S. W. & Kallenbach, N. R. (1983). Hydrogen exchange and structural dynamics of proteins and nucleic acids. Quarterly Reviews of Biophysics 16, 521–655.Google Scholar
Englander, S. W., Mayne, L., Bai, Y. & Sosnick, T. R. (1997). Hydrogen exchange: the modern legacy of Linderstrom-Lang. Protein Science 6, 1101–1109.Google Scholar
Englander, S. W., Mayne, L. & Krishna, M. M. G. (2007). Protein folding and misfolding: mechanism and principles. Quarterly Reviews of Biophysics 40, 287–326.CrossRefGoogle ScholarPubMed
Ermacora, M. R., Delfino, J. M., Cuenoud, B., Schepartz, A. & Fox, R. O. (1992). Conformation-dependent cleavage of staphylococcal nuclease with a disulfide-linked iron chelate. Proceedings of the National Academy of Sciences of the United States of America 89, 6383–6387.Google Scholar
Eyles, S. J. & Kaltashov, I. A. (2004). Methods to study protein dynamics and folding by mass spectrometry. Methods 34, 88–99.Google Scholar
Farrow, N. A., Zhang, O., Forman-Kay, J. D. & Kay, L. E. (1994). A heteronuclear correlation experiment for simultaneous determination of 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium. Journal of Biomolecular NMR 4, 727–734.Google Scholar
Fawzi, N. L., Doucleff, M., Suh, J. Y. & Clore, G. M. (2010a). Mechanistic details of a protein-protein association pathway revealed by paramagnetic relaxation enhancement titration measurements. Proceedings of the National Academy of Sciences of the United States of America 107, 1379–1384.Google Scholar
Fawzi, N. L., Fleissner, M. R., Anthis, N. J., Kalai, T., Hideg, K., Hubbell, W. L. & Clore, G. M. (2011a). A rigid disulfide-linked nitroxide side chain simplifies the quantitative analysis of PRE data. Journal of Biomolecular NMR 51, 105–114.Google Scholar
Fawzi, N. L., Libich, D. S., Ying, J., Tugarinov, V. & Clore, G. M. (2014). Characterizing methyl-bearing sidechain contacts and dynamics mediating amyloid β protofibril interactions using 13Cmethyl-DEST and lifetime line broadening. Angewandte Chimie International Edition 53, 10345–10349.Google Scholar
Fawzi, N. L., Ying, J., Ghirlando, R., Torchia, D. A. & Clore, G. M. (2011b). Atomic-resolution dynamics on the surface of amyloid β protofibrils probed by solution NMR. Nature 480, 268–272.Google Scholar
Fawzi, N. L., Ying, J., Torchia, D. A. & Clore, G. M. (2010b). Kinetics of amyloid β monomer-to-oligomer exchange by NMR relaxation. Journal of American Chemical Society 132, 9948–9951.CrossRefGoogle ScholarPubMed
Fawzi, N. L., Ying, J., Torchia, D. A. & Clore, G. M. (2012). Probing exchange kinetics and atomic resolution dynamics in high-molecular-weight complexes using dark-state exchange saturation transfer NMR spectroscopy. Nature Protocols 7, 1523–1533.CrossRefGoogle ScholarPubMed
Felitsky, D. J., Lietzow, M. A., Dyson, H. J. & Wright, P. E. (2008). Modeling transient collapsed states of an unfolded protein to provide insights into early folding events. Proceedings of the National Academy of Sciences of the United States of America 105, 6278–6283.CrossRefGoogle ScholarPubMed
Ferreiro, D. U., Cho, S. S., Komives, E. A. & Wolynes, P. G. (2005). The energy landscape of modular repeat proteins: topology determines folding mechanism in the ankyrin family. Journal of Molecular Biology 354, 679–692.Google Scholar
Fesik, S. W., Gemmecker, G., Olejniczak, E. T. & Petros, A. M. (1991). Identification of solvent-exposed regions of enzyme-bound ligands by nuclear-magnetic-resonance. Journal of American Chemical Society 113, 7080–7081.Google Scholar
Fisher, C. K. & Stultz, C. M. (2011). Constructing ensembles for intrinsically disordered proteins. Current Opinion in Structural Biology 21, 426–431.Google Scholar
Fitzkee, N. C., Torchia, D. A. & Bax, A. (2011). Measuring rapid hydrogen exchange in the homodimeric 36 kDa HIV-1 integrase catalytic core domain. Protein Science 20, 500–512.Google Scholar
Fleissner, M. R., Bridges, M. D., Brooks, E. K., Cascio, D., Kalai, T., Hideg, K. & Hubbell, W. L. (2011). Structure and dynamics of a conformationally constrained nitroxide side chain and applications in EPR spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 108, 16241–16246.Google Scholar
Fleissner, M. R., Brustad, E. M., Kalai, T., Altenbach, C., Cascio, D., Peters, F. B., Hideg, K., Peuker, S., Schultz, P. G. & Hubbell, W. L. (2009). Site-directed spin labeling of a genetically encoded unnatural amino acid. Proceedings of the National Academy of Sciences of the United States of America 106, 21637–21642.CrossRefGoogle ScholarPubMed
Flippen-Anderson, J. L., George, C., Valle, G., Valente, E., Bianco, A., Formaggio, F., Crisma, M. & Toniolo, C. (1996). Crystallographic characterization of geometry and conformation of TOAC, a nitroxide spin-labelled C-alpha, C-alpha-disubstituted glycine, in simple derivatives and model peptides. International Journal of Peptide and Protein Research 47, 231–238.Google Scholar
Forge, V., Wijesinha, R. T., Balbach, J., Brew, K., Robinson, C. V., Redfield, C. & Dobson, C. M. (1999). Rapid collapse and slow structural reorganisation during the refolding of bovine alpha-lactalbumin. Journal of Molecular Biology 288, 673–688.Google Scholar
Forsén, S. & Hoffman, R. A. (1963). Study of moderately rapid chemical exchange reactions by means of nuclear magnetic double resonance. Journal of Chemical Physics 39, 2892–2901.Google Scholar
Fragai, M., Luchinat, C., Parigi, G. & Ravera, E. (2013). Conformational freedom of metalloproteins revealed by paramagnetism-assisted NMR. Coordination Chemistry Reviews 257, 2652–2667.Google Scholar
Fraser, J. S., Clarkson, M. W., Degnan, S. C., Erion, R., Kern, D. & Alber, T. (2009). Hidden alternative structures of proline isomerase essential for catalysis. Nature 462, 669–673.Google Scholar
Freed, J. H. (1978). Dynamic effects of pair correlation-functions on spin relaxation by translational diffusion in liquids .2. Finite jumps and independent T1 processes. Journal of Chemical Physics 68, 4034–4037.Google Scholar
Friedman, J. I., Mcmahon, M. T., Stivers, J. T. & Van Zijl, P. C. (2010). Indirect detection of labile solute proton spectra via the water signal using frequency-labeled exchange (FLEX) transfer. Journal of American Chemical Society 132, 1813–1815.Google Scholar
Fuentes, E. J. & Wand, A. J. (1998a). Local dynamics and stability of apocytochrome b562 examined by hydrogen exchange. Biochemistry 37, 3687–3698.Google Scholar
Fuentes, E. J. & Wand, A. J. (1998b). Local stability and dynamics of apocytochrome b562 examined by the dependence of hydrogen exchange on hydrostatic pressure. Biochemistry 37, 9877–9883.Google Scholar
Gaponenko, V., Howarth, J. W., Columbus, L., Gasmi-Seabrook, G., Yuan, J., Hubbell, W. L. & Rosevear, P. R. (2000). Protein global fold determination using site-directed spin and isotope labeling. Protein Science 9, 302–309.Google Scholar
Gardner, R. J., Longinetti, M. & Sgheri, L. (2005). Reconstruction of orientations of a moving protein domain from paramagnetic data. Inverse Problems 21, 879.Google Scholar
Gillespie, J. R. & Shortle, D. (1997a). Characterization of long-range structure in the denatured state of staphylococcal nuclease. I. Paramagnetic relaxation enhancement by nitroxide spin labels. Journal of Molecular Biology 268, 158–169.Google Scholar
Gillespie, J. R. & Shortle, D. (1997b). Characterization of long-range structure in the denatured state of staphylococcal nuclease. II. Distance restraints from paramagnetic relaxation and calculation of an ensemble of structures. Journal of Molecular Biology 268, 170–184.Google Scholar
Goedert, M. & Spillantini, M. G. (2006). A century of Alzheimer's disease. Science 314, 777–781.Google Scholar
Gottstein, D., Reckel, S., Dotsch, V. & Guntert, P. (2012). Requirements on paramagnetic relaxation enhancement data for membrane protein structure determination by NMR. Structure 20, 1019–1027.Google Scholar
Griffith, O. H. & Mcconnell, H. M. (1966). A nitroxide-maleimide spin label. Proceedings of the National Academy of Sciences of the United States of America 55, 8–11.Google Scholar
Grishaev, A., Anthis, N. J. & Clore, G. M. (2012). Contrast-matched small-angle X-ray scattering from a heavy-atom labeled protein in structure determination: application to a lead-substituted calmodulin–peptide complex. Journal of American Chemical Society 134, 14686–14689.Google Scholar
Gross, J. D., Moerke, N. J., Von Der Haar, T., Lugovskoy, A. A., Sachs, A. B., Mccarthy, J. E. G. & Wagner, G. (2003). Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4 G and eIF4E. Cell 115, 739–750.Google Scholar
Gueron, M. (1975). Nuclear-relaxation in macromolecules by paramagnetic-ions – novel mechanism. Journal of Magnetic Resonance 19, 58–66.Google Scholar
Gupta, R. K. & Redfield, A. G. (1970). Double nuclear magnetic resonance observation of electron exchange between ferri- and ferrocytochrome c. Science 169, 1204–1206.Google Scholar
Hancu, I., Dixon, W. T., Woods, M., Vinogradov, E., Sherry, A. D. & Lenkinski, R. E. (2010). CEST and PARACEST MR contrast agents. Acta Radiology 51, 910–923.Google Scholar
Hansen, A. L., Lundstrom, P., Velyvis, A. & Kay, L. E. (2012). Quantifying millisecond exchange dynamics in proteins by CPMG relaxation dispersion NMR using side-chain 1H probes. Journal of American Chemical Society 134, 3178–3189.Google Scholar
Hansen, A. L., Nikolova, E. N., Casiano-Negroni, A. & Al-Hashimi, H. M. (2009). Extending the range of microsecond-to-millisecond chemical exchange detected in labeled and unlabeled nucleic acids by selective carbon R1(rho) NMR spectroscopy. Journal of American Chemical Society 131, 3818–3819.Google Scholar
Hansen, D. F., Vallurupalli, P. & Kay, L. E. (2008a). Using relaxation dispersion NMR spectroscopy to determine structures of excited, invisible protein states. Journal of Biomolecular NMR 41, 113–120.Google Scholar
Hansen, D. F., Vallurupalli, P., Lundstrom, P., Neudecker, P. & Kay, L. E. (2008b). Probing chemical shifts of invisible states of proteins with relaxation dispersion NMR spectroscopy: how well can we do? Journal of American Chemical Society 130, 2667–2675.Google Scholar
Hanson, P., Millhauser, G., Formaggio, F., Crisma, M. & Toniolo, C. (1996). ESR characterization of hexameric, helical peptides using double TOAC spin labeling. Journal of American Chemical Society 118, 7618–7625.Google Scholar
Hass, M. A., Keizers, P. H., Blok, A., Hiruma, Y. & Ubbink, M. (2010). Validation of a lanthanide tag for the analysis of protein dynamics by paramagnetic NMR spectroscopy. Journal of American Chemical Society 132, 9952–9953.Google Scholar
Haussinger, D., Huang, J. R. & Grzesiek, S. (2009). DOTA-M8: an extremely rigid, high-affinity lanthanide chelating tag for PCS NMR spectroscopy. Journal of American Chemical Society 131, 14761–14767.Google Scholar
Helgstrand, M., Hard, T. & Allard, P. (2000). Simulations of NMR pulse sequences during equilibrium and non-equilibrium chemical exchange. Journal of Biomolecular NMR 18, 49–63.Google Scholar
Hernandez, G., Teng, C. L., Bryant, R. G. & Lemaster, D. M. (2002). O2 penetration and proton burial depth in proteins: applicability to fold family recognition. Journal of American Chemical Society 124, 4463–4472.Google Scholar
Hillisch, A., Lorenz, M. & Diekmann, S. (2001). Recent advances in FRET: distance determination in protein–DNA complexes. Current Opinion in Structural Biology 11, 201–207.Google Scholar
Hitchens, T. K. & Bryant, R. G. (1998). Pressure dependence of amide hydrogen–deuterium exchange rates for individual sites in T4 lysozyme. Biochemistry 37, 5878–5887.Google Scholar
Horwich, A. L. & Fenton, W. A. (2009). Chaperonin-mediated protein folding: using a central cavity to kinetically assist polypeptide chain folding. Quarterly Reviews of Biophysics 42, 83–116.Google Scholar
Hu, K., Vogeli, B. & Clore, G. M. (2007). Spin-state selective carbon-detected HNCO with TROSY optimization in all dimensions and double echo-antiecho sensitivity enhancement in both indirect dimensions. Journal of American Chemical Society 129, 5484–5491.Google Scholar
Huang, F., Pei, Y. Y., Zuo, H. H., Chen, J. L., Yang, Y. & Su, X. C. (2013). Bioconjugation of proteins with a paramagnetic NMR and fluorescent tag. Chemistry 19, 17141–17149.Google Scholar
Hubbell, W. L., Cafiso, D. S. & Altenbach, C. (2000). Identifying conformational changes with site-directed spin labeling. Nature Structural Biology 7, 735–739.Google Scholar
Hubbell, W. L., Lopez, C. J., Altenbach, C. & Yang, Z. (2013). Technological advances in site-directed spin labeling of proteins. Current Opinion in Structural Biology 23, 725–733.Google Scholar
Hughson, F. M., Wright, P. E. & Baldwin, R. L. (1990). Structural characterization of a partly folded apomyoglobin intermediate. Science 249, 1544–1548.Google Scholar
Hwang, L. P. & Freed, J. H. (1975). Dynamic effects of pair correlation-functions on spin relaxation by translational diffusion in liquids. Journal of Chemical Physics 63, 4017–4025.Google Scholar
Igumenova, T. I., Frederick, K. K. & Wand, A. J. (2006). Characterization of the fast dynamics of protein amino acid side chains using NMR relaxation in solution. Chemical Reviews 106, 1672–1699.Google Scholar
Ikegami, T., Verdier, L., Sakhaii, P., Grimme, S., Pescatore, B., Saxena, K., Fiebig, K. M. & Griesinger, C. (2004). Novel techniques for weak alignment of proteins in solution using chemical tags coordinating lanthanide ions. Journal of Biomolecular NMR 29, 339–349.Google Scholar
Ikura, M., Clore, G. M., Gronenborn, A. M., Zhu, G., Klee, C. B. & Bax, A. (1992). Solution structure of a calmodulin–target peptide complex by multidimensional NMR. Science 256, 632–638.Google Scholar
Inomata, K., Ohno, A., Tochio, H., Isogai, S., Tenno, T., Nakase, I., Takeuchi, T., Futaki, S., Ito, Y., Hiroaki, H. & Shirakawa, M. (2009). High-resolution multi-dimensional NMR spectroscopy of proteins in human cells. Nature 458, 106–109.Google Scholar
Ishima, R., Freedberg, D. I., Wang, Y. X., Louis, J. M. & Torchia, D. A. (1999). Flap opening and dimer-interface flexibility in the free and inhibitor-bound HIV protease, and their implications for function. Structure 7, 1047–1055.Google Scholar
Ishima, R. & Torchia, D. A. (1999). Estimating the time scale of chemical exchange of proteins from measurements of transverse relaxation rates in solution. Journal of Biomolecular NMR 14, 369–372.Google Scholar
Ishima, R. & Torchia, D. A. (2000). Protein dynamics from NMR. Nature Structural Biology 7, 740–743.Google Scholar
Ishima, R. & Torchia, D. A. (2003). Extending the range of amide proton relaxation dispersion experiments in proteins using a constant-time relaxation-compensated CPMG approach. Journal of BiomolecularNMR 25, 243–248.Google Scholar
Iwahara, J., Anderson, D. E., Murphy, E. C. & Clore, G. M. (2003). EDTA-derivatized deoxythymidine as a tool for rapid determination of protein binding polarity to DNA by intermolecular paramagnetic relaxation enhancement. Journal of American Chemical Society 125, 6634–6635.Google Scholar
Iwahara, J. & Clore, G. M. (2006a). Detecting transient intermediates in macromolecular binding by paramagnetic NMR. Nature 440, 1227–1230.Google Scholar
Iwahara, J. & Clore, G. M. (2006b). Direct observation of enhanced translocation of a homeodomain between DNA cognate sites by NMR exchange spectroscopy. Journal of American Chemical Society 128, 404–405.Google Scholar
Iwahara, J. & Clore, G. M. (2010). Structure-independent analysis of the breadth of the positional distribution of disordered groups in macromolecules from order parameters for long, variable-length vectors using NMR paramagnetic relaxation enhancement. Journal of American Chemical Society 132, 13346–13356.Google Scholar
Iwahara, J., Schwieters, C. D. & Clore, G. M. (2004a). Characterization of nonspecific protein-DNA interactions by H-1 paramagnetic relaxation enhancement. Journal of American Chemical Society 126, 12800–12808.Google Scholar
Iwahara, J., Schwieters, C. D. & Clore, G. M. (2004b). Ensemble approach for NMR structure refinement against (1)H paramagnetic relaxation enhancement data arising from a flexible paramagnetic group attached to a macromolecule. Journal of American Chemical Society 126, 5879–5896.Google Scholar
Iwahara, J., Tang, C. & Clore, G. M. (2007). Practical aspects of (1)H transverse paramagnetic relaxation enhancement measurements on macromolecules. Journal of Magnetic Resonance 184, 185–195.Google Scholar
Iwahara, J., Zweckstetter, M. & Clore, G. M. (2006). NMR structural and kinetic characterization of a homeodomain diffusing and hopping on nonspecific DNA. Proceedings of the National Academy of Sciences of the United States of America 103, 15062–15067.Google Scholar
Jain, N. U., Venot, A., Umemoto, K., Leffler, H. & Prestegard, J. H. (2001). Distance mapping of protein-binding sites using spin-labeled oligosaccharide ligands. Protein Science 10, 2393–2400.Google Scholar
Jen, J. (1978). Chemical exchange and NMR T2 relaxation – multisite case. Journal of Magnetic Resonance 30, 111–128.Google Scholar
Jennings, P. A. & Wright, P. E. (1993). Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science 262, 892–896.Google Scholar
Jensen, M. R., Lauritzen, C., Dahl, S. W., Pedersen, J. & Led, J. J. (2004). Binding ability of a HHP-tagged protein towards Ni2+ studied by paramagnetic NMR relaxation: the possibility of obtaining long-range structure information. Journal of Biomolecular. NMR 29, 175–185.Google Scholar
Jeschke, G. (2013). Conformational dynamics and distribution of nitroxide spin labels. Progress in Nuclear Magnetic Resonance Spectroscopy 72, 42–60.Google Scholar
Johnson, P. E., Brun, E., Mackenzie, L. F., Withers, S. G. & Mcintosh, L. P. (1999). The cellulose-binding domains from Cellulomonas fimi beta-1,4-glucanase CenC bind nitroxide spin-labeled cellooligosaccharides in multiple orientations. Journal of Molecular Biology 287, 609–625.Google Scholar
Kamerlin, S. C. L. & Warshel, A. (2010). Reply to Karplus: conformational dynamics have no role in the chemical step. Proceedings of the National Academy of Sciences of the United States of America 107, E72.Google Scholar
Karplus, M. (2010). Role of conformation transitions in adenylate kinase. Proceedings of the National Academy of Sciences of the United States of America 107, E71.Google Scholar
Kateb, F., Pelupessy, P. & Bodenhausen, G. (2007). Measuring fast hydrogen exchange rates by NMR spectroscopy. Journal of Magnetic Resonance 184, 108–113.Google Scholar
Kay, L. E., Keifer, P. & Saarinen, T. (1992). Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. Journal of American Chemical Society 114, 10663–10665.Google Scholar
Kay, L. E., Torchia, D. A. & Bax, A. (1989). Backbone dynamics of proteins as studied by N-15 inverse detected heteronuclear NMR-spectroscopy – application to Staphylococcal nuclease. Biochemistry 28, 8972–8979.CrossRefGoogle Scholar
Keizers, P. H. & Ubbink, M. (2011). Paramagnetic tagging for protein structure and dynamics analysis. Progress in Nuclear Magnetic Resonance Spectroscopy 58, 88–96.Google Scholar
Keizers, P. H. J., Desreux, J. F., Overhand, M. & Ubbink, M. (2007). Increased paramagnetic effect of a lanthanide protein probe by two-point attachment. Journal of American Chemical Society 129, 9292.Google Scholar
Keizers, P. H. J., Saragliadis, A., Hiruma, Y., Overhand, M. & Ubbink, M. (2008). Design, synthesis, and evaluation of a lanthanide chelating protein probe: CLaNP-5 yields predictable paramagnetic effects independent of environment. Journal of American Chemical Society 130, 14802–14812.Google Scholar
Kempf, J. G., Jung, J.-Y., Ragain, C., Sampson, N. S. & Loria, J. P. (2007). Dynamic requirements for a functional protein hinge. Journal of Molecular Biology 368, 131–149.Google Scholar
Klug, C. S. & Feix, J. B. (2008). Methods and applications of site-directed spin labeling EPR spectroscopy. Methods in Cell Biology 84, 617–658.Google Scholar
Konermann, L., Tong, X. & Pan, Y. (2008). Protein structure and dynamics studied by mass spectrometry: H/D exchange, hydroxyl radical labeling, and related approaches. Journal of Mass Spectrometry 43, 1021–1036.Google Scholar
Korzhnev, D. M. & Kay, L. E. (2008). Probing invisible, low-populated states of protein molecules by relaxation dispersion NMR spectroscopy: an application to protein folding. Accounts of Chemical Research 41, 442–451.Google Scholar
Korzhnev, D. M., Kloiber, K., Kanelis, V., Tugarinov, V. & Kay, L. E. (2004a). Probing slow dynamics in high molecular weight proteins by methyl-TROSY NMR spectroscopy: application to a 723-residue enzyme. Journal of American Chemical Society 126, 3964–3973.Google Scholar
Korzhnev, D. M., Neudecker, P., Zarrine-Afsar, A., Davidson, A. R. & Kay, L. E. (2006). Abp1p and fyn SH3 domains fold through similar low-populated intermediate states. Biochemistry 45, 10175–10183.Google Scholar
Korzhnev, D. M., Religa, T. L., Banachewicz, W., Fersht, A. R. & Kay, L. E. (2010). A transient and low-populated protein-folding intermediate at atomic resolution. Science 329, 1312–1316.Google Scholar
Korzhnev, D. M., Salvatella, X., Vendruscolo, M., Di Nardo, A. A., Davidson, A. R., Dobson, C. M. & Kay, L. E. (2004b). Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR. Nature 430, 586–590.Google Scholar
Kosen, P. A. (1989). Spin labeling of proteins. Methods in Enzymology 177, 86–121.Google Scholar
Kosen, P. A., Scheek, R. M., Naderi, H., Basus, V. J., Manogaran, S., Schmidt, P. G., Oppenheimer, N. J. & Kuntz, I. D. (1986). Two-dimensional 1H NMR of three spin-labeled derivatives of bovine pancreatic trypsin inhibitor. Biochemistry 25, 2356–2364.Google Scholar
Krishna, M. M., Hoang, L., Lin, Y. & Englander, S. W. (2004a). Hydrogen exchange methods to study protein folding. Methods 34, 51–64.Google Scholar
Krishna, M. M., Lin, Y., Mayne, L. & Englander, S. W. (2003). Intimate view of a kinetic protein folding intermediate: residue-resolved structure, interactions, stability, folding and unfolding rates, homogeneity. Journal of Molecular Biology 334, 501–513.Google Scholar
Krishna, M. M. G., Hoang, L., Lin, Y. & Englander, S. W. (2004b). Hydrogen exchange methods to study protein folding. Methods 34, 51–64.Google Scholar
Kristjansdottir, S., Lindorff-Larsen, K., Fieber, W., Dobson, C. M., Vendruscolo, M. & Poulsen, F. M. (2005). Formation of native and non-native interactions in ensembles of denatured ACBP molecules from paramagnetic relaxation enhancement studies. Journal of Molecular Biology 347, 1053–1062.Google Scholar
Lange, O. F., Lakomek, N.-A., Fares, C., Schroeder, G. F., Walter, K. F. A., Becker, S., Meiler, J., Grubmueller, H., Griesinger, C. & De Groot, B. L. (2008). Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 320, 1471–1475.Google Scholar
Li, P., Martins, I. R. & Rosen, M. K. (2011). The feasibility of parameterizing four-state equilibria using relaxation dispersion measurements. Journal of Biomolecular NMR 51, 57–70.Google Scholar
Liang, B. Y., Bushweller, J. H. & Tamm, L. K. (2006). Site-directed parallel spin-labeling and paramagnetic relaxation enhancement in structure determination of membrane proteins by solution NMR spectroscopy. Journal of American Chemical Society 128, 4389–4397.Google Scholar
Libich, D. S., Fawzi, N. L., Ying, J. & Clore, G. M. (2013). Probing the transient dark state of substrate binding to GroEL by relaxation-based solution NMR. Proceedings of the National Academy of Sciences of the United States of America 110, 11361–11366.Google Scholar
Lietzow, M. A., Jamin, M., Dyson, H. J. & Wright, P. E. (2002). Mapping long-range contacts in a highly unfolded protein. Journal of Molecular Biology 322, 655–662.CrossRefGoogle Scholar
Lindfors, H. E., De Koning, P. E., Drijfhout, J. W., Venezia, B. & Ubbink, M. (2008). Mobility of TOAC spin-labelled peptides binding to the Src SH3 domain studied by paramagnetic NMR. Journal of Biomolecular NMR 41, 157–167.Google Scholar
Lindfors, H. E., Venkata, B. S., Drijfhout, J. W. & Ubbink, M. (2011). Linker length dependent binding of a focal adhesion kinase derived peptide to the Src SH3-SH2 domains. FEBS Letters 585, 601–605.Google Scholar
Lipari, G. & Szabo, A. (1982a). Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules .1. Theory and range of validity. Journal of American Chemical Society 104, 4546–4559.Google Scholar
Lipari, G. & Szabo, A. (1982b). Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules .2. Analysis of experimental results. Journal of American Chemical Society 104, 4559–4570.Google Scholar
Liu, W. M., Keizers, P. H., Hass, M. A., Blok, A., Timmer, M., Sarris, A. J., Overhand, M. & Ubbink, M. (2012). A pH-sensitive, colorful, lanthanide-chelating paramagnetic NMR probe. Journal of American Chemical Society 134, 17306–17313.Google Scholar
Liu, Z., Gong, Z., Guo, D. C., Zhang, W. P. & Tang, C. (2014). Subtle dynamics of holo glutamine binding protein revealed with a rigid paramagnetic probe. Biochemistry 53, 1403–1409.Google Scholar
Long, D., Bouvignies, G. & Kay, L. E. (2014). Measuring hydrogen exchange rates in invisible protein excited states. Proceedings of the National Academy of Sciences of the United States of America 111, 8820–8825.Google Scholar
Long, D., Marshall, C. B., Bouvignies, G., Mazhab-Jafari, M. T., Smith, M. J., Ikura, M. & Kay, L. E. (2013). A comparative CEST NMR study of slow conformational dynamics of small GTPases complexed with GTP and GTP analogues. Angewandte Chemie International Edition English 52, 10771–10774.Google Scholar
Longinetti, M., Luchinat, C., Parigi, G. & Sgheri, L. (2006). Efficient determination of the most favoured orientations of protein domains from paramagnetic NMR data. Inverse Problems 22, 1485.Google Scholar
Loria, J. P., Berlow, R. B. & Watt, E. D. (2008). Characterization of enzyme motions by solution NMR relaxation dispersion. Accounts of Chemical Research 41, 214–221.Google Scholar
Luchinat, C., Nagulapalli, M., Parigi, G. & Sgheri, L. (2012). Maximum occurrence analysis of protein conformations for different distributions of paramagnetic metal ions within flexible two-domain proteins. Journal of Magnetic Resonance 215, 85–93.Google Scholar
Lundstrom, P. & Akke, M. (2005). Microsecond protein dynamics measured by 13Calpha rotating-frame spin relaxation. Chembiochem 6, 1685–1692.Google Scholar
Lundstrom, P., Hansen, D. F., Vallurupalli, P. & Kay, L. E. (2009a). Accurate measurement of alpha proton chemical shifts of excited protein states by relaxation dispersion NMR spectroscopy. Journal of American Chemical Society 131, 1915–1926.Google Scholar
Lundstrom, P., Lin, H. & Kay, L. E. (2009b). Measuring C-13(beta) chemical shifts of invisible excited states in proteins by relaxation dispersion NMR spectroscopy. Journal of Biomolecular NMR 44, 139–155.Google Scholar
Lundstrom, P., Vallurupalli, P., Religa, T. L., Dahlquist, F. W. & Kay, L. E. (2007). A single-quantum methyl C-13-relaxation dispersion experiment with improved sensitivity. Journal of BiomolecularNMR 38, 79–88.Google Scholar
Lyumkis, D., Julien, J. P., De Val, N., Cupo, A., Potter, C. S., Klasse, P. J., Burton, D. R., Sanders, R. W., Moore, J. P., Carragher, B., Wilson, I. A. & Ward, A. B. (2013). Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342, 1484–1490.Google Scholar
Macnaughtan, M. A., Kamar, M., Alvarez-Manilla, G., Venot, A., Glushka, J., Pierce, J. M. & Prestegard, J. H. (2007). NMR structural characterization of substrates bound to N-acetylglucosaminyltransferase V. Journal of Molecular Biology 366, 1266–1281.Google Scholar
Mahoney, N. M., Rastogi, V. K., Cahill, S. M., Girvin, M. E. & Almo, S. C. (2000). Binding orientation of proline-rich peptides in solution: polarity of the profilin-ligand interaction. Journal of American Chemical Society 122, 7851–7852.Google Scholar
Maity, H., Maity, M., Krishna, M. M. G., Mayne, L. & Englander, S. W. (2005). Protein folding: the stepwise assembly of foldon units. Proceedings of the National Academy of Sciences of the United States of America 102, 4741–4746.Google Scholar
Mal, T. K., Ikura, M. & Kay, L. E. (2002). The ATCUN domain as a probe of intermolecular interactions: application to calmodulin-peptide complexes. Journal of American Chemical Society 124, 14002–14003.Google Scholar
Marsh, J. A. & Forman-Kay, J. D. (2009). Structure and disorder in an unfolded state under nondenaturing conditions from ensemble models consistent with a large number of experimental restraints. Journal of Molecular Biology 391, 359–374.Google Scholar
Marsh, J. A., Neale, C., Jack, F. E., Choy, W.-Y., Lee, A. Y., Crowhurst, K. A. & Forman-Kay, J. D. (2007). Improved structural characterizations of the drkN SH3 domain unfolded state suggest a compact ensemble with native-like and non-native structure. Journal of Molecular Biology 367, 1494–1510.Google Scholar
Mayer, M. & Meyer, B. (1999). Characterization of ligand binding by saturation transfer difference NMR spectroscopy. Angewandte Chemie International Edition English 38, 1784–1788.Google Scholar
Mcconnell, H. M. (1958). Reaction rates by nuclear magnetic resonance. Journal of Chemical Physics 28, 430–431.Google Scholar
Meador, W. E., Means, A. R. & Quiocho, F. A. (1992). Target enzyme recognition by calmodulin: 2·4 A structure of a calmodulin–peptide complex. Science 257, 1251–1255.Google Scholar
Meiboom, S. (1961). Nuclear magnetic resonance study of proton transfer in water. Journal of Chemical Physics 34, 375.Google Scholar
Meiboom, S. & Gill, D. (1958). Modified spin-echo method for measuring nuclear relaxation times. Reviews of Scientific Instruments 29, 688–691.Google Scholar
Milov, A. D., Tsvetkov, Y. D., Gorbunova, E. Y., Mustaeva, L. G., Ovchinnikova, T. V. & Raap, J. (2002). Self-aggregation properties of spin-labeled zervamicin IIA as studied by PELDOR spectroscopy. Biopolymers 64, 328–336.Google Scholar
Mittermaier, A. & Kay, L. E. (2006). New tools provide new insights in NMR studies of protein dynamics. Science 312, 224–228.Google Scholar
Mittermaier, A. K. & Kay, L. E. (2009). Observing biological dynamics at atomic resolution using NMR. Trends in Biochemical Sciences 34, 601–611.Google Scholar
Miyashita, O., Onuchic, J. N. & Wolynes, P. G. (2003). Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins. Proceedings of the National Academy of Sciences of the United States of America 100, 12570–12575.Google Scholar
Miyashita, O., Wolynes, P. G. & Onuchic, J. N. (2005). Simple energy landscape model for the kinetics of functional transitions in proteins. Journal of Physical Chemistry B 109, 1959–1969.Google Scholar
Monaco, V., Formaggio, F., Crisma, M., Toniolo, C., Hanson, P., Millhauser, G., George, C., Deschamps, J. R. & Flippen-Anderson, J. L. (1999a). Determining the occurrence of a 3(10)-helix and an alpha-helix in two different segments of a lipopeptaibol antibiotic using TOAC, a nitroxide spin-labeled C-alpha-tetrasubstituted alpha-amino acid. Bioorganic and Medicinal Chemistry 7, 119–131.Google Scholar
Monaco, V., Formaggio, F., Crisma, M., Toniolo, C., Hanson, P. & Millhauser, G. L. (1999b). Orientation and immersion depth of a helical lipopeptaibol in membranes using TOAC as an ESR probe. Biopolymers 50, 239–253.Google Scholar
Montelione, G. T., Winkler, M. E., Burton, L. E., Rinderknecht, E., Sporn, M. B. & Wagner, G. (1989). Sequence-specific 1H-NMR assignments and identification of two small antiparallel beta-sheets in the solution structure of recombinant human transforming growth factor alpha. Proceedings of the National Academy of Sciences of the United States of America 86, 1519–1523.Google Scholar
Nadaud, P. S., Sengupta, I., Helmus, J. J. & Jaroniec, C. P. (2011). Evaluation of the influence of intermolecular electron–nucleus couplings and intrinsic metal binding sites on the measurement of 15N longitudinal paramagnetic relaxation enhancements in proteins by solid-state NMR. Journal of Biomolecular NMR 51, 293–302.Google Scholar
Nagulapalli, M., Parigi, G., Yuan, J., Gsponer, J., Deraos, G., Bamm, V. V., Harauz, G., Matsoukas, J., De Planque, M. R., Gerothanassis, I. P., Babu, M. M., Luchinat, C. & Tzakos, A. G. (2012). Recognition pliability is coupled to structural heterogeneity: a calmodulin intrinsically disordered binding region complex. Structure 20, 522–533.Google Scholar
Neudecker, P., Lundstrom, P. & Kay, L. E. (2009). Relaxation dispersion NMR spectroscopy as a tool for detailed studies of protein folding. Biophysical Journal 96, 2045–2054.Google Scholar
Neudecker, P., Robustelli, P., Cavalli, A., Walsh, P., Lundstrom, P., Zarrine-Afsar, A., Sharpe, S., Vendruscolo, M. & Kay, L. E. (2012). Structure of an intermediate state in protein folding and aggregation. Science 336, 362–366.Google Scholar
Neudecker, P., Zarrine-Afsar, A., Davidson, A. R. & Kay, L. E. (2007). Phi-Value analysis of a three-state protein folding pathway by NMR relaxation dispersion spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 104, 15717–15722.Google Scholar
Nodet, G., Salmon, L., Ozenne, V., Meier, S., Jensen, M. R. & Blackledge, M. (2009). Quantitative description of backbone conformational sampling of unfolded proteins at amino acid resolution from NMR residual dipolar couplings. Journal of American Chemical Society 131, 17908–17918.Google Scholar
Oganesyan, V. S. (2011). A general approach for prediction of motional EPR spectra from Molecular Dynamics (MD) simulations: application to spin labelled protein. Physical Chemistry and Chemical Physics 13, 4724–4737.Google Scholar
Ogawa, S. & Mcconnel, H. M. (1967). Spin-label study of hemoglobin conformations in solution. Proceedings of the National Academy of Sciences of the United States of America 58, 19-&.Google Scholar
Ohgushi, M. & Wada, A. (1983). ‘Molten-globule state’: a compact form of globular proteins with mobile side-chains. FEBS Letters 164, 21–24.Google Scholar
Olejniczak, E. T., Dobson, C. M., Karplus, M. & Levy, R. M. (1984). Motional averaging of proton nuclear Overhauser effects in proteins – predictions from a molecular-dynamics simulation of lysozyme. Journal of American Chemical Society 106, 1923–1930.Google Scholar
Ollerenshaw, J. E., Lidar, D. A. & Kay, L. E. (2003). Magnetic resonance realization of decoherence-free quantum computation. Physics Reviews Letters 91, 217904.Google Scholar
Onuchic, J. N., Lutheyschulten, Z. & Wolynes, P. G. (1997). Theory of protein folding: the energy landscape perspective. Annual Review of Physical Chemistry 48, 545–600.Google Scholar
Otten, R., Villali, J., Kern, D. & Mulder, F. A. (2010). Probing microsecond time scale dynamics in proteins by methyl 1H-Carr-Purcell-Meiboom-Gill relaxation dispersion NMR measurements. Application to activation of the signaling protein NtrC(r). Journal of American Chemical Society 132, 17004–17014.Google Scholar
Otting, G. (2010). Protein NMR using paramagnetic ions. Annual Review of Biophysics 39, 387–405.Google Scholar
Ozenne, V., Noel, J. K., Heidarsson, P. O., Brander, S., Poulsen, F. M., Jensen, M. R., Kragelund, B. B., Blackledge, M. & Danielsson, J. (2014). Exploring the minimally frustrated energy landscape of unfolded ACBP. Journal of Molecular Biology 426, 722–734.Google Scholar
Palmer, A. G. III (2014). Chemical exchange in biomacromolecules: past, present, and future. Journal of Magnetic Resonance 241, 3–17.Google Scholar
Palmer, A. G. III, Grey, M. J. & Wang, C. (2005). Solution NMR spin relaxation methods for characterizing chemical exchange in high-molecular-weight systems. Methods in Enzymology 394, 430–465.Google Scholar
Palmer, A. G. III, Kroenke, C. D. & Loria, J. P. (2001). Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods in Enzymology 339, 204–238.Google Scholar
Palmer, A. G. III & Massi, F. (2006). Characterization of the dynamics of biomacromolecules using rotating-frame spin relaxation NMR spectroscopy. Chemical Reviews 106, 1700–1719.Google Scholar
Pelikan, M., Hura, G. L. & Hammel, M. (2009). Structure and flexibility within proteins as identified through small angle X-ray scattering. General Physiology and Biophysics 28, 174–189.Google Scholar
Peng, J. W. & Wagner, G. (1994). Investigation of protein motions via relaxation measurements. Methods in Enzymology 239, 563–596.Google Scholar
Peterson, D. W., Zhou, H., Dahlquist, F. W. & Lew, J. (2008). A soluble oligomer of tau associated with fiber formation analyzed by NMR. Biochemistry 47, 7393–7404.Google Scholar
Petros, A. M., Mueller, L. & Kopple, K. D. (1990). NMR identification of protein surfaces using paramagnetic probes. Biochemistry 29, 10041–10048.Google Scholar
Pintacuda, G., Kaikkonen, A. & Otting, G. (2004a). Modulation of the distance dependence of paramagnetic relaxation enhancements by CSA × DSA cross-correlation. Journal of Magnetic Resonance 171, 233–243.Google Scholar
Pintacuda, G., Moshref, A., Leonchiks, A., Sharipo, A. & Otting, G. (2004b). Site-specific labelling with a metal chelator for protein-structure refinement. Journal of Biomolecular NMR 29, 351–361.Google Scholar
Pintacuda, G. & Otting, G. (2002). Identification of protein surfaces by NMR measurements with a paramagnetic Gd(III) chelate. Journal of American Chemical Society 124, 372–373.Google Scholar
Pisliakov, A. V., Cao, J., Kamerlin, S. C. L. & Warshel, A. (2009). Enzyme millisecond conformational dynamics do not catalyze the chemical step. Proceedings of the National Academy of Sciences of the United States of America 106, 17359–17364.Google Scholar
Post, C. B. (2003). Exchange-transferred NOE spectroscopy and bound ligand structure determination. Current Opinion in Structural Biology 13, 581–588.Google Scholar
Ramos, A. & Varani, G. (1998). A new method to detect long-range protein–RNA contacts: NMR detection of electron–proton relaxation induced by nitroxide spin-labeled RNA. Journal of American Chemical Society 120, 10992–10993.Google Scholar
Rao, B. D. (1989). Nuclear magnetic resonance line-shape analysis and determination of exchange rates. Methods in Enzymology 176, 279–311.Google Scholar
Redfield, A. G. (1957). On the theory of relaxation processes. Ibm Journal of Research and Development 1, 19–31.Google Scholar
Redfield, C. (2004). Using nuclear magnetic resonance spectroscopy to study molten globule states of proteins. Methods 34, 121–132.Google Scholar
Roder, H., Elove, G. A. & Englander, S. W. (1988). Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature 335, 700–704.Google Scholar
Roosild, T. P., Greenwald, J., Vega, M., Castronovo, S., Riek, R. & Choe, S. (2005). NMR structure of Mistic, a membrane-integrating protein for membrane protein expression. Science 307, 1317–1321.Google Scholar
Rueda, M., Ferrer-Costa, C., Meyer, T., Perez, A., Camps, J., Hospital, A., Gelpi, J. L. & Orozco, M. (2007). A consensus view of protein dynamics. Proceedings of the National Academy of Sciences of the United States of America 104, 796–801.Google Scholar
Rule, G. S. & Hitchens, T. K. (2006). Fundamentals of Protein NMR Spectroscopy. Springer, Dordrecht, The Netherlands.Google Scholar
Rumpel, S., Becker, S. & Zweckstetter, M. (2008). High-resolution structure determination of the CylR2 homodimer using paramagnetic relaxation enhancement and structure-based prediction of molecular alignment. Journal of Biomolecular NMR 40, 1–13.Google Scholar
Ruschak, A. M. & Kay, L. E. (2010). Methyl groups as probes of supra-molecular structure, dynamics and function. Journal of Biomolecular NMR 46, 75–87.Google Scholar
Russo, L., Maestre-Martinez, M., Wolff, S., Becker, S. & Griesinger, C. (2013). Interdomain dynamics explored by paramagnetic NMR. Journal of American Chemical Society 135, 17111–17120.Google Scholar
Sahu, D., Clore, G. M. & Iwahara, J. (2007). TROSY-based z-exchange spectroscopy: application to the determination of the activation energy for intermolecular protein translocation between specific sites on different DNA molecules. Journal of American Chemical Society 129, 13232–13237.Google Scholar
Sakakura, M., Noba, S., Luchette, P. A., Shimada, I. & Prosser, R. S. (2005). An NMR method for the determination of protein-binding interfaces using dioxygen-induced spin-lattice relaxation enhancement. Journal of American Chemical Society 127, 5826–5832.Google Scholar
Schanda, P. & Brutscher, B. (2005). Very fast two-dimensional NMR spectroscopy for real-time investigation of dynamic events in proteins on the time scale of seconds. Journal of American Chemical Society 127, 8014–8015.Google Scholar
Schmidt, P. G. & Kuntz, I. D. (1984). Distance measurements in spin-labeled lysozyme. Biochemistry 23, 4261–4266.Google Scholar
Schwartz, A. L. & Cutnell, J. D. (1983). One- and two-dimensional NMR studies of exchanging amide protons in glutathione. Journal of Magnetic Resonance 53, 398–411.Google Scholar
Schwieters, C. D. & Clore, G. M. (2001). The VMD-XPLOR visualization package for NMR structure refinement. Journal of Magnetic Resonance 149, 239–244.Google Scholar
Schwieters, C. D. & Clore, G. M. (2002). Reweighted atomic densities to represent ensembles of NMR structures. Journal of Biomolecular NMR 23, 221–225.Google Scholar
Schwieters, C. D., Kuszewski, J. J. & Clore, G. M. (2006). Using Xplor-NIH for NMR molecular structure determination. Progress in Nuclear Magnetic Resonance Spectroscopy 48, 47–62.Google Scholar
Schwieters, C. D., Kuszewski, J. J., Tjandra, N. & Clore, G. M. (2003). The Xplor-NIH NMR molecular structure determination package. Journal of Magnetic Resonance 160, 65–73.Google Scholar
Seeholzer, S. H. & Wand, A. J. (1989). Structural characterization of the interactions between calmodulin and skeletal muscle myosin light chain kinase: effect of peptide (576–594)G binding on the Ca2+-binding domains. Biochemistry 28, 4011–4020.Google Scholar
Sekhar, A. & Kay, L. E. (2013). NMR paves the way for atomic level descriptions of sparsely populated, transiently formed biomolecular conformers. Proceedings of the National Academy of Sciences of the United States of America 110, 12867–12874.Google Scholar
Selenko, P., Serber, Z., Gadea, B., Ruderman, J. & Wagner, G. (2006). Quantitative NMR analysis of the protein G B1 domain in Xenopus laevis egg extracts and intact oocytes. Proceedings of the National Academy of Sciences of the United States of America 103, 11904–11909.Google Scholar
Sengupta, I., Nadaud, P. S., Helmus, J. J., Schwieters, C. D. & Jaroniec, C. P. (2012). Protein fold determined by paramagnetic magic-angle spinning solid-state NMR spectroscopy. Nature Chemistry 4, 410–417.Google Scholar
Sengupta, I., Nadaud, P. S. & Jaroniec, C. P. (2013). Protein structure determination with paramagnetic solid-state NMR spectroscopy. Accounts of Chemical Research 46, 2117–2126.Google Scholar
Shen, Y. & Bax, A. (2013). Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks. Journal of Biomolecular NMR 56, 227–241.Google Scholar
Shen, Y., Lange, O., Delaglio, F., Rossi, P., Aramini, J. M., Liu, G., Eletsky, A., Wu, Y., Singarapu, K. K., Lemak, A., Ignatchenko, A., Arrowsmith, C. H., Szyperski, T., Montelione, G. T., Baker, D. & Bax, A. (2008). Consistent blind protein structure generation from NMR chemical shift data. Proceedings of the National Academy of Sciences of the United States of America 105, 4685–4690.Google Scholar
Shen, Y., Vernon, R., Baker, D. & Bax, A. (2009). De novo protein structure generation from incomplete chemical shift assignments. Journal of Biomolecular NMR 43, 63–78.Google Scholar
Shenkarev, Z. O., Paramonov, A. S., Balashova, T. A., Yakimenko, Z. A., Baru, M. B., Mustaeva, L. G., Raap, J., Ovchinnikova, T. V. & Arseniev, A. S. (2004). High stability of the hinge region in the membrane-active peptide helix of zervamicin: paramagnetic relaxation enhancement studies. Biochemical and Biophysical Research Communications 325, 1099–1105.Google Scholar
Shi, L. & Kay, L. E. (2014). Tracing an allosteric pathway regulating the activity of the HslV protease. Proceedings of the National Academy of Sciences of the United States of America 111, 2140–2145.Google Scholar
Silvestre-Ryan, J., Bertoncini, C. W., Fenwick, R. B., Esteban-Martin, S. & Salvatella, X. (2013). Average conformations determined from PRE data provide high-resolution maps of transient tertiary interactions in disordered proteins. Biophysical Journal 104, 1740–1751.Google Scholar
Skrynnikov, N. R., Dahlquist, F. W. & Kay, L. E. (2002). Reconstructing NMR spectra of “invisible” excited protein states using HSQC and HMQC experiments. Journal of American Chemical Society 124, 12352–12360.Google Scholar
Solomon, I. (1955). Relaxation processes in a system of two spins. Physics Reviews 99, 559–565.Google Scholar
Solomon, I. & Bloembergen, N. (1956). Nuclear magnetic interactions in the HF molecule. Journal of Chemical Physics 25, 261–266.Google Scholar
Song, J., Guo, L.-W., Muradov, H., Artemyev, N. O., Ruoho, A. E. & Markley, J. L. (2008). Intrinsically disordered gamma-subunit of cGMP phosphodiesterase encodes functionally relevant transient secondary and tertiary structure. Proceedings of the National Academy of Sciences of the United States of America 105, 1505–1510.Google Scholar
Spera, S., Ikura, M. & Bax, A. (1991). Measurement of the exchange rates of rapidly exchanging amide protons: application to the study of calmodulin and its complex with a myosin light chain kinase fragment. Journal of Biomolecular NMR 1, 155–165.Google Scholar
Sprangers, R. & Kay, L. E. (2007). Quantitative dynamics and binding studies of the 20S proteasome by NMR. Nature 445, 618–622.Google Scholar
Stan, G., Brooks, B. R., Lorimer, G. H. & Thirumalai, D. (2006). Residues in substrate proteins that interact with GroEL in the capture process are buried in the native state. Proceedings of the National Academy of Sciences of the United States of America 103, 4433–4438.CrossRefGoogle ScholarPubMed
Sugase, K., Dyson, H. J. & Wright, P. E. (2007). Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447, 1021–1025.Google Scholar
Swift, T. J. & Connick, R. E. (1962). NMR-relaxation mechanisms of O17 in aqueous solutions of paramagnetic cations and lifetime of water molecules in first coordination sphere. Journal of Chemical Physics 37, 307–320.CrossRefGoogle Scholar
Takayama, Y. & Clore, G. M. (2011). Intra- and intermolecular translocation of the bi-domain transcription factor Oct1 characterized by liquid crystal and paramagnetic NMR. Proceedings of the National Academy of Sciences of the United States of America 108, E169–E176.Google Scholar
Takayama, Y. & Clore, G. M. (2012). Interplay between minor and major groove-binding transcription factors Sox2 and Oct1 in translocation on DNA studied by paramagnetic and diamagnetic NMR. Journal of Biological Chemistry 287, 14349–14363.Google Scholar
Tang, C., Ghirlando, R. & Clore, G. M. (2008a). Visualization of transient ultra-weak protein self-association in solution using paramagnetic relaxation enhancement. Journal of American Chemical Society 130, 4048–4056.Google Scholar
Tang, C., Iwahara, J. & Clore, G. M. (2006). Visualization of transient encounter complexes in protein–protein association. Nature 444, 383–386.Google Scholar
Tang, C., Louis, J. M., Aniana, A., Suh, J. Y. & Clore, G. M. (2008b). Visualizing transient events in amino-terminal autoprocessing of HIV-1 protease. Nature 455, 693–696.Google Scholar
Tang, C., Schwieters, C. D. & Clore, G. M. (2007). Open-to-closed transition in apo maltose-binding protein observed by paramagnetic NMR. Nature 449, 1078–1082.Google Scholar
Thirumalai, D. & Lorimer, G. H. (2001). Chaperonin-mediated protein folding. Annual Review of Biophysics and Biomolecular Structure 30, 245–269.Google Scholar
Tjandra, N., Marquardt, J. & Clore, G. M. (2000). Direct refinement against proton-proton dipolar couplings in NMR structure determination of macromolecules. Journal of Magnetic Resonance 142, 393–396.Google Scholar
Todd, A. P., Cong, J. P., Levinthal, F., Levinthal, C. & Hubbell, W. L. (1989). Site-directed mutagenesis of colicin-E1 provides specific attachment sites for spin labels whose spectra are sensitive to local conformation. Proteins 6, 294–305.Google Scholar
Toledo Warshaviak, D., Khramtsov, V. V., Cascio, D., Altenbach, C. & Hubbell, W. L. (2013). Structure and dynamics of an imidazoline nitroxide side chain with strongly hindered internal motion in proteins. Journal of Magnetic Resonance 232, 53–61.Google Scholar
Trewhella, J. (1992). The solution structures of calmodulin and its complexes with synthetic peptides based on target enzyme binding domains. Cell Calcium 13, 377–390.Google Scholar
Trott, O. & Palmer, A. G. (2004). Theoretical study of R-1p rotating-frame and R-2 free-precession relaxation in the presence of n-site chemical exchange. Journal of Magnetic Resonance 170, 104–112.Google Scholar
Tugarinov, V., Hwang, P. M., Ollerenshaw, J. E. & Kay, L. E. (2003). Cross-correlated relaxation enhanced H-1-C-13 NMR spectroscopy of methyl groups in very high molecular weight proteins and protein complexes. Journal of American Chemical Society 125, 10420–10428.Google Scholar
Tugarinov, V., Kanelis, V. & Kay, L. E. (2006). Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy. Nature Protocols 1, 749–754.Google Scholar
Ubbink, M., Worrall, J. A. R., Canters, G. W., Groenen, E. J. J. & Huber, M. (2002). Paramagnetic resonance of biological metal centers. Annual Review of Biophysics and Biomolecular Structure 31, 393–422.Google Scholar
Udgaonkar, J. B. & Baldwin, R. L. (1988). NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature 335, 694–699.CrossRefGoogle ScholarPubMed
Ueda, T., Kato, A., Ogawa, Y., Torizawa, T., Kuramitsu, S., Iwai, S., Terasawa, H. & Shimada, I. (2004). NMR study of repair mechanism of DNA photolyase by FAD-induced paramagnetic relaxation enhancement. Journal of Biological Chemistry 279, 52574–52579.Google Scholar
Vallurupalli, P., Bouvignies, G. & Kay, L. E. (2011). Increasing the exchange time-scale that can be probed by CPMG relaxation dispersion NMR. Journal of Physical Chemistry B 115, 14891–14900.Google Scholar
Vallurupalli, P., Bouvignies, G. & Kay, L. E. (2012). Studying “invisible” excited protein states in slow exchange with a major state conformation. Journal of American Chemical Society 134, 8148–8161.Google Scholar
Vallurupalli, P., Bouvignies, G. & Kay, L. E. (2013). A computational study of the effects of (13) C-(13) C scalar couplings on (13) C CEST NMR spectra: towards studies on a uniformly (13) C-labeled protein. Chembiochem 14, 1709–1713.Google Scholar
Vallurupalli, P., Hansen, D. F. & Kay, L. E. (2008a). Probing structure in invisible protein states with anisotropic NMR chemical shifts. Journal of American Chemical Society 130, 2734–2735.Google Scholar
Vallurupalli, P., Hansen, D. F. & Kay, L. E. (2008b). Structures of invisible, excited protein states by relaxation dispersion NMR spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 105, 11766–11771.Google Scholar
Vallurupalli, P., Hansen, D. F., Stollar, E., Meirovitch, E. & Kay, L. E. (2007). Measurement of bond vector orientations in invisible excited states of proteins. Proceedings of the National Academy of Sciences of the United States of America 104, 18473–18477.Google Scholar
Vallurupalli, P. & Kay, L. E. (2006). Complementarity of ensemble and single-molecule measures of protein motion: a relaxation dispersion NMR study of an enzyme complex. Proceedings of the National Academy of Sciences of the United States of America 103, 11910–11915.Google Scholar
Vallurupalli, P. & Kay, L. E. (2013). Probing slow chemical exchange at carbonyl sites in proteins by chemical exchange saturation transfer NMR spectroscopy. Angewandte Chemie International Edition English 52, 4156–4159.CrossRefGoogle ScholarPubMed
Van Heel, M., Gowen, B., Matadeen, R., Orlova, E. V., Finn, R., Pape, T., Cohen, D., Stark, H., Schmidt, R., Schatz, M. & Patwardhan, A. (2000). Single-particle electron cryo-microscopy: towards atomic resolution. Quarterly Reviews of Biophysics 33, 307–369.Google Scholar
Van Zijl, P. C. & Yadav, N. N. (2011). Chemical exchange saturation transfer (CEST): what is in a name and what isn't? Magnetic Resonance in Medicines 65, 927–948.Google Scholar
Varani, L., Gunderson, S. I., Mattaj, I. W., Kay, L. E., Neuhaus, D. & Varani, G. (2000). The NMR structure of the 38 kDa U1A protein – PIE RNA complex reveals the basis of cooperativity in regulation of polyadenylation by human U1A protein. Nature Structural Biology 7, 329–335.Google Scholar
Venditti, V., Fawzi, N. L. & Clore, G. M. (2011). Automated sequence- and stereo-specific assignment of methyl-labeled proteins by paramagnetic relaxation and methyl-methyl nuclear Overhauser enhancement spectroscopy. Journal of Biomolecular NMR 51, 319–328.Google Scholar
Venditti, V., Fawzi, N. L. & Clore, G. M. (2012). An efficient protocol for incorporation of an unnatural amino acid in perdeuterated recombinant proteins using glucose-based media. Journal of Biomolecular NMR 52, 191–195.CrossRefGoogle ScholarPubMed
Villali, J. & Kern, D. (2010). Choreographing an enzyme's dance. Current Opinion in Structural Biology 14, 636–643.Google Scholar
Vinogradov, E., Sherry, A. D. & Lenkinski, R. E. (2013). CEST: from basic principles to applications, challenges and opportunities. Journal of Magnetic Resonance 229, 155–172.Google Scholar
Vise, P., Baral, B., Stancik, A., Lowry, D. F. & Daughdrill, G. W. (2007). Identifying long-range structure in the intrinsically unstructured transactivation domain of p53. Proteins 67, 526–530.Google Scholar
Vlasie, M. D., Comuzzi, C., Van Den Nieuwendijk, A. M. C. H., Prudencio, M., Overhand, M. & Ubbink, M. (2007). Long-range-distance NMR effects in a protein labeled with a lanthanide-DOTA chelate. Chemistry 13, 1715–1723.Google Scholar
Volkov, A. N., Ubbink, M. & Van Nuland, N. A. J. (2010). Mapping the encounter state of a transient protein complex by PRE NMR spectroscopy. Journal of Biomolecular NMR 48, 225–236.Google Scholar
Volkov, A. N., Worrall, J. A. R., Holtzmann, E. & Ubbink, M. (2006). Solution structure and dynamics of the complex between cytochrome c and cytochrome c peroxidase determined by paramagnetic NMR. Proceedings of the National Academy of Sciences of the United States of America 103, 18945–18950.Google Scholar
Wagner, G. & Wuthrich, K. (1982). Amide protein exchange and surface conformation of the basic pancreatic trypsin inhibitor in solution. Studies with two-dimensional nuclear magnetic resonance. Journal of Molecular Biology 160, 343–361.Google Scholar
Walsh, D. M. & Selkoe, D. J. (2007). A beta oligomers – a decade of discovery. Journal of Neurochemistry 101, 1172–1184.Google Scholar
Wand, A. J. & Englander, S. W. (1996). Protein complexes studied by NMR spectroscopy. Current Opinion in Biotechnology 7, 403–408.Google Scholar
Wang, L., Brock, A., Herberich, B. & Schultz, P. G. (2001). Expanding the genetic code of Escherichia coli. Science 292, 498–500.Google Scholar
Wang, X., Srisailam, S., Yee, A. A., Lemak, A., Arrowsmith, C., Prestegard, J. H. & Tian, F. (2007). Domain-domain motions in proteins from time-modulated pseudocontact shifts. Journal of Biomolecular NMR 39, 53–61.Google Scholar
Ward, K. M., Aletras, A. H. & Balaban, R. S. (2000). A new class of contrast agents for MRI based on proton chemical exchange dependent saturation transfer (CEST). Journal of Magnetic Resonance 143, 79–87.Google Scholar
Watt, E. D., Shimada, H., Kovrigin, E. L. & Loria, J. P. (2007). The mechanism of rate-limiting motions in enzyme function. Proceedings of the National Academy of Sciences of the United States of America 104, 11981–11986.Google Scholar
Weininger, U., Blissing, A. T., Hennig, J., Ahlner, A., Liu, Z., Vogel, H. J., Akke, M. & Lundstrom, P. (2013). Protein conformational exchange measured by 1H R1rho relaxation dispersion of methyl groups. Journal of Biomolecular NMR 57, 47–55.Google Scholar
Wickramasinghe, N. P., Kotecha, M., Samoson, A., Past, J. & Ishii, Y. (2007). Sensitivity enhancement in (13)C solid-state NMR of protein microcrystals by use of paramagnetic metal ions for optimizing (1)H T(1) relaxation. Journal of Magnetic Resonance 184, 350–356.Google Scholar
Wider, G., Neri, D. & Wuthrich, K. (1991). Studies of slow conformational equilibria in macromolecules by exchange of heteronuclear longitudinal 2-spin-order in a 2D difference correlation experiment. Journal of Biomolecular NMR 1, 93–98.Google Scholar
Woessner, D. E. (1962). Spin relaxation processes in a two-proton system undergoing anisotropic reorientation. Journal of Chemical Physics 36, 1–4.Google Scholar
Wohnert, J., Franz, K. J., Nitz, M., Imperiali, B. & Schwalbe, H. (2003). Protein alignment by a coexpressed lanthanide-binding tag for the measurement of residual dipolar couplings. Journal of American Chemical Society 125, 13338–13339.Google Scholar
Wolf-Watz, M., Thai, V., Henzler-Wildman, K., Hadjipavlou, G., Eisenmesser, E. Z. & Kern, D. (2004). Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nature Structural and Molecular Biology 11, 945–949.Google Scholar
Wolynes, P. G. (2005). Recent successes of the energy landscape theory of protein folding and function. Quarterly Review of Biophysics 38, 405–410.Google Scholar
Wright, P. E. & Dyson, H. J. (2009). Linking folding and binding. Current Opinion in Structural Biology 19, 31–38.Google Scholar
Xia, J., Deng, N. J. & Levy, R. M. (2013). NMR relaxation in proteins with fast internal motions and slow conformational exchange: model-free framework and Markov state simulations. Journal of Physical Chemistry B 117, 6625–6634.Google Scholar
Yamniuk, A. P. & Vogel, H. J. (2004). Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Molecular Biotechnology 27, 33–57.Google Scholar
Yan, S., Gawlak, G., Smith, J., Silver, L., Koide, A. & Koide, S. (2004). Conformational heterogeneity of an equilibrium folding intermediate quantified and mapped by scanning mutagenesis. Journal of Molecular Biology 338, 811–825.Google Scholar
Yan, S., Kennedy, S. D. & Koide, S. (2002). Thermodynamic and kinetic exploration of the energy landscape of Borrelia burgdorferi OspA by native-state hydrogen exchange. Journal of Molecular Biology 323, 363–375.Google Scholar
Zhang, Z. & Smith, D. L. (1993). Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation. Protein Science 2, 522–531.Google Scholar
Zhou, Z. H. (2008). Towards atomic resolution structural determination by single-particle cryo-electron microscopy. Current Opinion in Structural Biology 18, 218–228.Google Scholar
Zhuang, T., Chisholm, C., Chen, M. & Tamm, L. K. (2013). NMR-based conformational ensembles explain pH-gated opening and closing of OmpG channel. Journal of American Chemical Society 135, 15101–15113.Google Scholar