Carlomagno, T., Maurer, M., Hennig, M., and Griesinger, C.: Ubiquitin Backbone Motion Studied via
Dipolar-Dipolar and
CSA-Dipolar Cross-Correlated Relaxation, J. Am. Chem. Soc., 122, 5105–5113,
https://doi.org/10.1021/ja993845n, 2000.
a
Cisnetti, F., Loth, K., Pelupessy, P., and Bodenhausen, G.: Determination of Chemical Shift Anisotropy Tensors of Carbonyl Nuclei in Proteins through Cross-Correlated Relaxation in NMR, ChemPhysChem, 5, 807–814,
https://doi.org/10.1002/cphc.200301041, 2004.
a,
b,
c,
d,
e
Clore, G. M. and Iwahara, J.: Theory, Practice, and Applications of Paramagnetic Relaxation Enhancement for the Characterization of Transient Low-Population States of Biological Macromolecules and Their Complexes, Chem. Rev., 109, 4108–4139,
https://doi.org/10.1021/cr900033p, 2009.
a
Clore, G. M., Szabo, A., Bax, A., Kay, L. E., Driscoll, P. C., and Gronenborn, A. M.: Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins, J. Am. Chem. Soc., 112, 4989–4991,
https://doi.org/10.1021/ja00168a070, 1990.
a,
b,
c
Corey, R. B., Pauling, L. C., and Astbury, W. T.: Fundamental dimensions of polypeptide chains, P. Roy. Soc. Lond. B Bio., 141, 10–20,
https://doi.org/10.1098/rspb.1953.0011, 1953.
a,
b
Cornilescu, G., Marquardt, J. L., Ottiger, M., and Bax, A.: Validation of Protein Structure from Anisotropic Carbonyl Chemical Shifts in a Dilute Liquid Crystalline Phase, J. Am. Chem. Soc., 120, 6836–6837,
https://doi.org/10.1021/ja9812610, 1998.
a
Daragan, V. A. and Mayo, K. H.: Using the Model Free Approach to Analyze NMR Relaxation Data in Cases of Anisotropic Molecular Diffusion, J. Phys. Chem. B, 103, 6829–6834,
https://doi.org/10.1021/jp9911393, 1999.
a
Dayie, K. T. and Wagner, G.: Carbonyl Carbon Probe of Local Mobility in
13C,15N-Enriched Proteins Using High-Resolution Nuclear Magnetic Resonance, J. Am. Chem. Soc., 119, 7797–7806,
https://doi.org/10.1021/ja9633880, 1997.
a
Deschamps, M.: Cross-Correlated Relaxation with Anisotropic Reorientation and Small Amplitude Local Motions, J. Phys. Chem. A, 106, 2438–2445,
https://doi.org/10.1021/jp013407e, 2002.
a
Eastman, P., Swails, J., Chodera, J. D., McGibbon, R. T., Zhao, Y., Beauchamp, K. A., Wang, L.-P., Simmonett, A. C., Harrigan, M. P., Stern, C. D., Wiewiora, R. P., Brooks, B. R., and Pande, V. S.: OpenMM 7: Rapid development of high performance algorithms for molecular dynamics, PLOS Comput. Biol., 13, 1–17,
https://doi.org/10.1371/journal.pcbi.1005659, 2017.
a
Ferrage, F., Pelupessy, P., Cowburn, D., and Bodenhausen, G.: Protein Backbone Dynamics through
Cross-Relaxation in NMR Spectroscopy, J. Am. Chem. Soc., 128, 11072–11078,
https://doi.org/10.1021/ja0600577, 2006.
a
Ghose, R., Huang, K., and Prestegard, J. H.: Measurement of Cross Correlation between Dipolar Coupling and Chemical Shift Anisotropy in the Spin Relaxation of
13C,
15N-Labeled Proteins, J. Magn. Reson., 135, 487–499,
https://doi.org/10.1006/jmre.1998.1602, 1998.
a,
b,
c
Gopal, S. M., Wingbermühle, S., Schnatwinkel, J., Juber, S., Herrmann, C., and Schäfer, L. V.: Conformational Preferences of an Intrinsically Disordered Protein Domain: A Case Study for Modern Force Fields, J. Phys. Chem. B, 125, 24–35,
https://doi.org/10.1021/acs.jpcb.0c08702, 2021.
a
Grudzia̧ż, K., Zawadzka-Kazimierczuk, A., and Koźmiński, W.: High-dimensional NMR methods for intrinsically disordered proteins studies, nMR Methods of Characterizing Biomolecular Structural Dynamics and Conformational Ensembles, Methods, 148, 81–87,
https://doi.org/10.1016/j.ymeth.2018.04.031, 2018.
a
Halle, B.: The physical basis of model-free analysis of NMR relaxation data from proteins and complex fluids, J. Chem. Phys., 131, 1–224507,
https://doi.org/10.1063/1.3269991, 2009.
a,
b,
c
Halle, B. and Wennerström, H.: Interpretation of magnetic resonance data from water nuclei in heterogeneous systems, J. Chem. Phys., 75, 1928–1943,
https://doi.org/10.1063/1.442218, 1981.
a,
b
Hsu, A., Ferrage, F., and Palmer, A. G.: Analysis of NMR Spin-Relaxation Data Using an Inverse Gaussian Distribution Function, Biophys. J., 115, 2301–2309,
https://doi.org/10.1016/j.bpj.2018.10.030, 2018.
a,
b
Idiyatullin, D., Daragan, V. A., and Mayo, K. H.: A New Approach to Visualizing Spectral Density Functions and Deriving Motional Correlation Time Distributions: Applications to an
α-Helix-Forming Peptide and to a Well-Folded Protein, J. Magn. Reson., 152, 132–148,
https://doi.org/10.1006/jmre.2001.2372, 2001.
a,
b,
c,
d
Iwahara, J., Schwieters, C. D., and Clore, G. M.: Ensemble Approach for NMR Structure Refinement against 1H Paramagnetic Relaxation Enhancement Data Arising from a Flexible Paramagnetic Group Attached to a Macromolecule, J. Am. Chem. Soc., 126, 5879–5896,
https://doi.org/10.1021/ja031580d, 2004.
a
Kadeřávek, P., Zapletal, V., Rabatinová, A., Krásný, L., Sklenář, V., and Žídek, L.: Spectral density mapping protocols for analysis of molecular motions in disordered proteins, J. Biomol. NMR, 58, 193–207,
https://doi.org/10.1007/s10858-014-9816-4, 2014.
a,
b,
c,
d
Kadeřávek, P., Grutsch, S., Salvi, N., Tollinger, M., Žídek, L., Bodenhausen, G., and Ferrage, F.: Cross-correlated relaxation measurements under adiabatic sweeps: determination of local order in proteins, J. Biomol. NMR, 63, 353–365,
https://doi.org/10.1007/s10858-015-9994-8, 2015.
a,
b
Kämpf, K., Izmailov, S. A., Rabdano, S. O., Groves, A. T., Podkorytov, I. S., and Skrynnikov, N. R.: What Drives 15N Spin Relaxation in Disordered Proteins? Combined NMR/MD Study of the H4 Histone Tail, Biophys. J., 115, 2348–2367,
https://doi.org/10.1016/j.bpj.2018.11.017, 2018.
a,
b,
c
Kauffmann, C., Zawadzka-Kazimierczuk, A., Kontaxis, G., and Konrat, R.: Using Cross-Correlated Spin Relaxation to Characterize Backbone Dihedral Angle Distributions of Flexible Protein Segments, ChemPhysChem, 22, 18–28,
https://doi.org/10.1002/cphc.202000789, 2021.
a
Khan, S., Charlier, C., Augustyniak, R., Salvi, N., Déjean, V., Bodenhausen, G., Lequin, O., Pelupessy, P., and Ferrage, F.: Distribution of Pico- and Nanosecond Motions in Disordered Proteins from Nuclear Spin Relaxation, Biophys. J., 109, 988–999,
https://doi.org/10.1016/j.bpj.2015.06.069, 2015.
a,
b,
c
Křížová, H., Žídek, L., Stone, M. J., Novotny, M. V., and Sklenář, V.: Temperature-dependent spectral density analysis applied to monitoring backbone dynamics of major urinary protein-I complexed with the pheromone 2-
sec-butyl-4,5-dihydrothiazole*, J. Biomol. NMR, 28, 369–384,
https://doi.org/10.1023/B:JNMR.0000015404.61574.65, 2004.
a
Kroenke, C. D., Loria, J. P., Lee, L. K., Rance, M., and Palmer, A. G.: Longitudinal and Transverse
1H−15N Dipolar/
15N Chemical Shift Anisotropy Relaxation Interference: Unambiguous Determination of Rotational Diffusion Tensors and Chemical Exchange Effects in Biological Macromolecules, J. Am. Chem. Soc., 120, 7905–7915,
https://doi.org/10.1021/ja980832l, 1998.
a,
b,
c
Kümmerer, F., Orioli, S., Harding-Larsen, D., Hoffmann, F., Gavrilov, Y., Teilum, K., and Lindorff-Larsen, K.: Fitting side-chain NMR relaxation data using molecular simulations, bioRxiv,
https://doi.org/10.1101/2020.08.18.256024, 2020.
a
Lienin, S. F., Bremi, T., Brutscher, B., Brüschweiler, R., and Ernst, R. R.: Anisotropic Intramolecular Backbone Dynamics of Ubiquitin Characterized by NMR Relaxation and MD Computer Simulation, J. Am. Chem. Soc., 120, 9870–9879,
https://doi.org/10.1021/ja9810179, 1998.
a
Lipari, G. and Szabo, A.: Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity, J. Am. Chem. Soc., 104, 4546–4559,
https://doi.org/10.1021/ja00381a009, 1982.
a,
b,
c,
d,
e,
f
Loth, K., Pelupessy, P., and Bodenhausen, G.: Chemical Shift Anisotropy Tensors of Carbonyl, Nitrogen, and Amide Proton Nuclei in Proteins through Cross-Correlated Relaxation in NMR Spectroscopy, J. Am. Chem. Soc., 127, 6062–6068,
https://doi.org/10.1021/ja042863o, 2005.
a,
b,
c
Mantsyzov, A. B., Maltsev, A. S., Ying, J., Shen, Y., Hummer, G., and Bax, A.: A maximum entropy approach to the study of residue-specific backbone angle distributions in
α-synuclein, an intrinsically disordered protein, Protein Sci., 23, 1275–1290,
https://doi.org/10.1002/pro.2511, 2014.
a,
b,
c,
d,
e,
f,
g
Mantsyzov, A. B., Shen, Y., Lee, J. H., Hummer, G., and Bax, A.: MERA: a webserver for evaluating backbone torsion angle distributions in dynamic and disordered proteins from NMR data, J. Biomol. NMR, 63, 85–95,
https://doi.org/10.1007/s10858-015-9971-2, 2015.
a,
b
Marcellini, M., Nguyen, M.-H., Martin, M., Hologne, M., and Walker, O.: Accurate Prediction of Protein NMR Spin Relaxation by Means of Polarizable Force Fields. Application to Strongly Anisotropic Rotational Diffusion, J. Phys. Chem. B, 124, 5103–5112,
https://doi.org/10.1021/acs.jpcb.0c01922, 2020.
a,
b,
c,
d
Markwick, P. R. L., Sprangers, R., and Sattler, M.: Local Structure and Anisotropic Backbone Dynamics from Cross-Correlated NMR Relaxation in Proteins, Angew. Chem. Int. Edit., 44, 3232–3237,
https://doi.org/10.1002/anie.200462495, 2005.
a
Meirovitch, E., Shapiro, Y. E., Polimeno, A., and Freed, J. H.: Protein Dynamics from NMR: The Slowly Relaxing Local Structure Analysis Compared with Model-Free Analysis, J. Phys. Chem. A, 110, 8366–8396,
https://doi.org/10.1021/jp056975t, 2006.
a
Modig, K. and Poulsen, F. M.: Model-independent interpretation of NMR relaxation data for unfolded proteins: the acid-denatured state of ACBP, J. Biomol. NMR, 42, 163–177,
https://doi.org/10.1007/s10858-008-9280-0, 2008.
a,
b
Nodet, G., Abergel, D., and Bodenhausen, G.: Predicting NMR Relaxation Rates in Anisotropically Tumbling Proteins through Networks of Coupled Rotators, ChemPhysChem, 9, 625–633,
https://doi.org/10.1002/cphc.200700732, 2008.
a
Ottiger, M. and Bax, A.: Determination of Relative
N−HN,
,
, and
Cα−Hα Effective Bond Lengths in a Protein by NMR in a Dilute Liquid Crystalline Phase, J. Am. Chem. Soc., 120, 12334–12341,
https://doi.org/10.1021/ja9826791, 1998.
a
Pelupessy, P., Espallargas, G. M., and Bodenhausen, G.: Symmetrical reconversion: measuring cross-correlation rates with enhanced accuracy, J. Magn. Reson., 161, 258–264,
https://doi.org/10.1016/S1090-7807(02)00190-8, 2003.
a,
b,
c
Pelupessy, P., Ferrage, F., and Bodenhausen, G.: Accurate Measurement of Longitudinal Cross-Relaxation Rates in Nuclear Magnetic Resonance, J. Chem. Phys., 126, 134 508, 1–10,
https://doi.org/10.1063/1.2715583, 2007.
a,
b,
c
Piana, S., Donchev, A. G., Robustelli, P., and Shaw, D. E.: Water Dispersion Interactions Strongly Influence Simulated Structural Properties of Disordered Protein States, J. Phys. Chem. B, 119, 5113–5123,
https://doi.org/10.1021/jp508971m, 2015.
a
Piana, S., Robustelli, P., Tan, D., Chen, S., and Shaw, D. E.: Development of a Force Field for the Simulation of Single-Chain Proteins and Protein–Protein Complexes, J. Chem. Theory Comput., 16, 2494–2507,
https://doi.org/10.1021/acs.jctc.9b00251, 2020.
a
Rauscher, S., Gapsys, V., Gajda, M. J., Zweckstetter, M., de Groot, B. L., and Grubmüller, H.: Structural Ensembles of Intrinsically Disordered Proteins Depend Strongly on Force Field: A Comparison to Experiment, J. Chem. Theory Comput., 11, 5513–5524,
https://doi.org/10.1021/acs.jctc.5b00736, 2015.
a
Robustelli, P., Piana, S., and Shaw, D. E.: Developing a molecular dynamics force field for both folded and disordered protein states, P. Natl. Acad. Sci. USA, 115, E4758–E4766,
https://doi.org/10.1073/pnas.1800690115, 2018.
a
Salomon-Ferrer, R., Götz, A. W., Poole, D., Le Grand, S., and Walker, R. C.: Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit Solvent Particle Mesh Ewald, J. Chem. Theory Comput., 9, 3878–3888,
https://doi.org/10.1021/ct400314y, 2013.
a
Salvi, N., Abyzov, A., and Blackledge, M.: Multi-Timescale Dynamics in Intrinsically Disordered Proteins from NMR Relaxation and Molecular Simulation, J. Phys. Chem. Lett., 7, 2483–2489,
https://doi.org/10.1021/acs.jpclett.6b00885, 2016.
a
Salvi, N., Abyzov, A., and Blackledge, M.: Analytical Description of NMR Relaxation Highlights Correlated Dynamics in Intrinsically Disordered Proteins, Angew. Chem. Int. Edit., 56, 14020–14024,
https://doi.org/10.1002/anie.201706740, 2017.
a,
b,
c,
d,
e,
f
Schwalbe, H., Carlomagno, T., Hennig, M., Junker, J., Reif, B., Richter, C., and Griesinger, C.: [2] - Cross-Correlated Relaxation for Measurement of Angles between Tensorial Interactions, in: Nuclear Magnetic Resonance of Biological Macromolecules Part A, edited by: James, T. L., Dötsch, V., and Schmitz, U., Academic Press, London and San Diego, Methods in Enzymology, 338, 35–81,
https://doi.org/10.1016/S0076-6879(02)38215-6, 2002.
a
Shea, J.-E., Best, R. B., and Mittal, J.: Physics-based computational and theoretical approaches to intrinsically disordered proteins, Curr. Opin. Struc. Biol., 67, 219–225,
https://doi.org/10.1016/j.sbi.2020.12.012, 2021.
a
Smith, A. A., Ernst, M., and Meier, B. H.: Because the Light is Better Here: Correlation-Time Analysis by NMR Spectroscopy, Angew. Chem. Int. Edit., 56, 13590–13595,
https://doi.org/10.1002/anie.201707316, 2017.
a,
b
Smith, A. A., Ernst, M., Meier, B. H., and Ferrage, F.: Reducing bias in the analysis of solution-state NMR data with dynamics detectors, J. Chem. Phys., 151, 034102,
https://doi.org/10.1063/1.5111081, 2019.
a,
b
Stone, J. E., Phillips, J. C., Freddolino, P. L., Hardy, D. J., Trabuco, L. G., and Schulten, K.: Accelerating molecular modeling applications with graphics processors, J. Comput. Chem., 28, 2618–2640,
https://doi.org/10.1002/jcc.20829, 2007.
a
Stone, J. E., Hardy, D. J., Ufimtsev, I. S., and Schulten, K.: GPU-accelerated molecular modeling coming of age, J. Mol. Graph. Model., 29, 116–125,
https://doi.org/10.1016/j.jmgm.2010.06.010, 2010.
a
Tjandra, N., Szabo, A., and Bax, A.: Protein Backbone Dynamics and
15N Chemical Shift Anisotropy from Quantitative Measurement of Relaxation Interference Effects, J. Am. Chem. Soc., 118, 6986–6991,
https://doi.org/10.1021/ja960510m, 1996.
a,
b,
c,
d
Tugarinov, V., Liang, Z., Shapiro, Y. E., Freed, J. H., and Meirovitch, E.: A Structural Mode-Coupling Approach to
15N NMR Relaxation in Proteins, J. Am. Chem. Soc., 123, 3055–3063,
https://doi.org/10.1021/ja003803v, 2001.
a
Vögeli, B.: Comprehensive description of NMR cross-correlated relaxation under anisotropic molecular tumbling and correlated local dynamics on all time scales, J. Chem. Phys., 133, 014 501,
https://doi.org/10.1063/1.3454734, 2010.
a,
b
Vögeli, B. and Yao, L.: Correlated Dynamics between Protein HN and HC Bonds Observed by NMR Cross Relaxation, J. Am. Chem. Soc., 131, 3668–3678,
https://doi.org/10.1021/ja808616v, 2009.
a,
b,
c,
d
Vugmeyster, L., Pelupessy, P., Vugmeister, B. E., Abergel, D., and Bodenhausen, G.: Cross-correlated relaxation in NMR of macromolecules in the presence of fast and slow internal dynamics, highly polarized nuclear spin systems and dipolar interactions in NMR, C. R. Phys., 5, 377–386,
https://doi.org/10.1016/j.crhy.2004.02.004, 2004.
a
Wang, T., Weaver, D. S., Cai, S., and Zuiderweg, E. R. P.: Quantifying Lipari–Szabo modelfree parameters from
13CO NMR relaxation experiments, J. Biomol. NMR, 36, 79–102,
https://doi.org/10.1007/s10858-006-9047-4, 2006.
a,
b
Woessner, D. E.: Spin Relaxation Processes in a Two-Proton System Undergoing Anisotropic Reorientation, J. Chem. Phys., 36, 1–4,
https://doi.org/10.1063/1.1732274, 1962.
a
Xue, Y., Podkorytov, I. S., Rao, D. K., Benjamin, N., Sun, H., and Skrynnikov, N. R.: Paramagnetic relaxation enhancements in unfolded proteins: Theory and application to drkN SH3 domain, Protein Sci., 18, 1401–1424,
https://doi.org/10.1002/pro.153, 2009.
a
Ying, J., Roche, J., and Bax, A.: Homonuclear decoupling for enhancing resolution and sensitivity in NOE and RDC measurements of peptides and proteins, a special “JMR Perspectives” issue: Foresights in Biomolecular Solution-State NMR Spectroscopy – From Spin Gymnastics to Structure and Dynamics, J. Magn. Reson., 241, 97–102,
https://doi.org/10.1016/j.jmr.2013.11.006, 2014.
a
Zerbetto, M., Buck, M., Meirovitch, E., and Polimeno, A.: Integrated Computational Approach to the Analysis of NMR Relaxation in Proteins: Application to ps-ns Main Chain
15N−1H and Global Dynamics of the Rho GTPase Binding Domain of Plexin-B1, J. Phys. Chem. B, 115, 376–388,
https://doi.org/10.1021/jp108633v, 2011.
a
Zerze, G. H., Zheng, W., Best, R. B., and Mittal, J.: Evolution of All-Atom Protein Force Fields to Improve Local and Global Properties, J. Phys. Chem. Lett., 10, 2227–2234,
https://doi.org/10.1021/acs.jpclett.9b00850, 2019.
a
