ACS Publications. Most Trusted. Most Cited. Most Read
Probing Dynamic Conformations of the High-Molecular-Weight αB-Crystallin Heat Shock Protein Ensemble by NMR Spectroscopy

OR SEARCH CITATIONS

My Activity
Publications

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Am. Chem. Soc. 2012, 134, 37, 15343-15350
    Article

    Probing Dynamic Conformations of the High-Molecular-Weight αB-Crystallin Heat Shock Protein Ensemble by NMR Spectroscopy
    Click to copy article linkArticle link copied!

    View Author Information
    † Departments of Molecular Genetics and Chemistry, The University of Toronto, Toronto, Ontario M5S 1A8, Canada
    ‡ Department of Biochemistry, The University of Toronto, Toronto, Ontario M5S 1A8, Canada
    § Program in Molecular Structure, Hospital for Sick Children, 555 University Avenue, Toronto, Ontario M5G 1X8, Canada
    ⊥ Physical and Theoretical Chemistry Laboratory, Department of Chemistry, University of Oxford, South Parks Road, Oxford, Oxfordshire OX1 3QZ, U.K.
    [email protected]; [email protected]
    Other Access OptionsSupporting Information (1)

    Journal of the American Chemical Society

    Cite this: J. Am. Chem. Soc. 2012, 134, 37, 15343–15350
    Click to copy citationCitation copied!
    https://doi.org/10.1021/ja307874r
    Published August 23, 2012
    Copyright © 2012 American Chemical Society
    Request reuse permissions

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    Solution- and solid-state nuclear magnetic resonance (NMR) spectroscopy are highly complementary techniques for studying supra-molecular structure. Here they are employed for investigating the molecular chaperone αB-crystallin, a polydisperse ensemble of between 10 and 40 identical subunits with an average molecular mass of approximately 600 kDa. An IxI motif in the C-terminal region of each of the subunits is thought to play a critical role in regulating the size distribution of oligomers and in controlling the kinetics of subunit exchange between them. Previously published solid-state NMR and X-ray results are consistent with a bound IxI conformation, while solution NMR studies provide strong support for a highly dynamic state. Here we demonstrate through FROSTY (freezing rotational diffusion of protein solutions at low temperature and high viscosity) MAS (magic angle spinning) NMR that both populations are present at low temperatures (<0 °C), while at higher temperatures only the mobile state is observed. Solution NMR relaxation dispersion experiments performed under physiologically relevant conditions establish that the motif interchanges between flexible (highly populated) and bound (sparsely populated) states. This work emphasizes the importance of using multiple methods in studies of supra-molecules, especially for highly dynamic ensembles where sample conditions can potentially affect the conformational properties observed.

    Copyright © 2012 American Chemical Society

    Subjects

    what are subjects

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    Figures showing assignment of I159/161 δ1 methyl groups, solid-state NMR spectra, effects of pH and temperature on I159/161 and V169 1H NMR spectra, and 1H/13C CPMG RD profiles of αB-crystallin. This material is available free of charge via the Internet at http://pubs.acs.org.

    Terms & Conditions

    Electronic Supporting Information files are available without a subscription to ACS Web Editions. The American Chemical Society holds a copyright ownership interest in any copyrightable Supporting Information. Files available from the ACS website may be downloaded for personal use only. Users are not otherwise permitted to reproduce, republish, redistribute, or sell any Supporting Information from the ACS website, either in whole or in part, in either machine-readable form or any other form without permission from the American Chemical Society. For permission to reproduce, republish and redistribute this material, requesters must process their own requests via the RightsLink permission system. Information about how to use the RightsLink permission system can be found at http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!
    Citation Statements
    Explore this article's citation statements on scite.ai
    powered by  Scite

    This article is cited by 58 publications.

    1. Iva Pritišanac, Matteo T. Degiacomi, T. Reid Alderson, Marta G. Carneiro, Eiso AB, Gregg Siegal, and Andrew J. Baldwin . Automatic Assignment of Methyl-NMR Spectra of Supramolecular Machines Using Graph Theory. Journal of the American Chemical Society 2017, 139 (28) , 9523-9533. https://doi.org/10.1021/jacs.6b11358
    2. Loïc Salmon, Logan S. Ahlstrom, Scott Horowitz, Alex Dickson, Charles L. Brooks III, and James C. A. Bardwell . Capturing a Dynamic Chaperone–Substrate Interaction Using NMR-Informed Molecular Modeling. Journal of the American Chemical Society 2016, 138 (31) , 9826-9839. https://doi.org/10.1021/jacs.6b02382
    3. Scott P. Delbecq, Joel C. Rosenbaum, and Rachel E. Klevit . A Mechanism of Subunit Recruitment in Human Small Heat Shock Protein Oligomers. Biochemistry 2015, 54 (28) , 4276-4284. https://doi.org/10.1021/acs.biochem.5b00490
    4. Andrew J. Baldwin, Danielle L. Egan, Fredrick J. Warren, Paul D. Barker, Christopher M. Dobson, Peter J. Butterworth, and Peter R. Ellis . Investigating the Mechanisms of Amylolysis of Starch Granules by Solution-State NMR. Biomacromolecules 2015, 16 (5) , 1614-1621. https://doi.org/10.1021/acs.biomac.5b00190
    5. Ivano Bertini, Claudio Luchinat, Giacomo Parigi, and Enrico Ravera . SedNMR: On the Edge between Solution and Solid-State NMR. Accounts of Chemical Research 2013, 46 (9) , 2059-2069. https://doi.org/10.1021/ar300342f
    6. Abeeb Ajibade, Andrew Luan Liu, Xiaoqin Zou. Modeling protein flexibility in molecular docking. 2025https://doi.org/10.1016/B978-0-443-29808-0.00006-6
    7. Zihao Wang, Guodong Cao, Miranda P. Collier, Xingyu Qiu, Sophie Broadway-Stringer, Dominik Šaman, Jediael Z.Y. Ng, Navoneel Sen, Amar J. Azad, Charlotte Hooper, Johannes Zimmermann, Michael McDonough, Jürgen Brem, Patrick Rabe, Haigang Song, T. Reid Alderson, Christopher J. Schofield, Jani R. Bolla, Kristina Djinovic-Carugo, Dieter O. Fürst, Bettina Warscheid, Matteo T. Degiacomi, Timothy M. Allison, Georg K.A. Hochberg, Carol V. Robinson, Katja Gehmlich, Justin L.P. Benesch. Cardiac stress leads to regulation of Filamin C dimerisation via an ancient phosphorylation-modulated interaction with HSPB7. 2024https://doi.org/10.1101/2024.01.05.574393
    8. Fan Shi, Tong Zhang, Juan Li, Chaowei Shi, Shengqi Xiang. Studying large biomolecules as sedimented solutes with solid-state NMR. Biophysics Reports 2024, 10 (4) , 201. https://doi.org/10.52601/bpr.2024.240014
    9. Y. Hu, M. Liu. Structural Disorder in Chaperone Functions Probed by NMR. 2023, 38-54. https://doi.org/10.1039/BK9781839165986-00038
    10. Bin Sun, Peter M. Kekenes-Huskey. Myofilament-associated proteins with intrinsic disorder (MAPIDs) and their resolution by computational modeling. Quarterly Reviews of Biophysics 2023, 56 https://doi.org/10.1017/S003358352300001X
    11. Linda Cerofolini, Giacomo Parigi, Enrico Ravera, Marco Fragai, Claudio Luchinat. Solid-state NMR methods for the characterization of bioconjugations and protein-material interactions. Solid State Nuclear Magnetic Resonance 2022, 122 , 101828. https://doi.org/10.1016/j.ssnmr.2022.101828
    12. Rishav Mitra, Kevin Wu, Changhan Lee, James C.A. Bardwell. ATP-Independent Chaperones. Annual Review of Biophysics 2022, 51 (1) , 409-429. https://doi.org/10.1146/annurev-biophys-090121-082906
    13. Theodoros K. Karamanos, G. Marius Clore. Large Chaperone Complexes Through the Lens of Nuclear Magnetic Resonance Spectroscopy. Annual Review of Biophysics 2022, 51 (1) , 223-246. https://doi.org/10.1146/annurev-biophys-090921-120150
    14. Michael A. Skinnider, Nichollas E. Scott, Anna Prudova, Craig H. Kerr, Nikolay Stoynov, R. Greg Stacey, Queenie W.T. Chan, David Rattray, Jörg Gsponer, Leonard J. Foster. An atlas of protein-protein interactions across mouse tissues. Cell 2021, 184 (15) , 4073-4089.e17. https://doi.org/10.1016/j.cell.2021.06.003
    15. Laura Troussicot, Björn M. Burmann, Mikael Molin. Structural determinants of multimerization and dissociation in 2-Cys peroxiredoxin chaperone function. Structure 2021, 29 (7) , 640-654. https://doi.org/10.1016/j.str.2021.04.007
    16. Aaron T. Balana, Paul M. Levine, Timothy W. Craven, Somnath Mukherjee, Nichole J. Pedowitz, Stuart P. Moon, Terry T. Takahashi, Christian F. W. Becker, David Baker, Matthew R. Pratt. O-GlcNAc modification of small heat shock proteins enhances their anti-amyloid chaperone activity. Nature Chemistry 2021, 13 (5) , 441-450. https://doi.org/10.1038/s41557-021-00648-8
    17. T Reid Alderson, Elias Adriaenssens, Bob Asselbergh, Iva Pritišanac, Jonas Van Lent, Heidi Y Gastall, Marielle A Wälti, John M Louis, Vincent Timmerman, Andrew J Baldwin, Justin LP Benesch. A weakened interface in the P182L variant of HSP27 associated with severe Charcot‐Marie‐Tooth neuropathy causes aberrant binding to interacting proteins. The EMBO Journal 2021, 40 (8) https://doi.org/10.15252/embj.2019103811
    18. Henrik Müller, David M. Dias, Anna van der Zalm, Andrew J. Baldwin. αB-crystallin affects the morphology of Aβ(1-40) aggregates. 2021https://doi.org/10.1101/2021.03.07.433908
    19. Vitali Tugarinov, Theodoros K. Karamanos, G. Marius Clore. Optimized selection of slow-relaxing 13C transitions in methyl groups of proteins: application to relaxation dispersion. Journal of Biomolecular NMR 2020, 74 (12) , 673-680. https://doi.org/10.1007/s10858-020-00349-3
    20. Ana T. Marcos, Diego Amorós, Beatriz Muñoz-Cabello, Francisco Galán, Eloy Rivas Infante, Luis Alcaraz‐Mas, José M. Navarro‐Pando. A novel dominant mutation in CRYAB gene leading to a severe phenotype with childhood onset. Molecular Genetics & Genomic Medicine 2020, 8 (8) https://doi.org/10.1002/mgg3.1290
    21. Patrick Owusu‐Ansah, Xiaojie Yu, Richard Osae, Cunshan Zhou, Rong Zhang, Abdullateef T. Mustapha, Mo Li, Haile Ma. Optimization of thermosonication on Bacillus cereus from pork: Effects on inactivation and physicochemical properties. Journal of Food Process Engineering 2020, 43 (6) https://doi.org/10.1111/jfpe.13401
    22. Aaron T. Balana, Paul M. Levine, Somnath Mukherjee, Nichole J. Pedowitz, Stuart P. Moon, Terry T. Takahashi, Christian F. W. Becker, Matthew R. Pratt. O-GlcNAcylation of small heat shock proteins enhances their anti-amyloid chaperone activity. 2019https://doi.org/10.1101/869909
    23. Maria K. Janowska, Hannah E.R. Baughman, Christopher N. Woods, Rachel E. Klevit. Mechanisms of Small Heat Shock Proteins. Cold Spring Harbor Perspectives in Biology 2019, 11 (10) , a034025. https://doi.org/10.1101/cshperspect.a034025
    24. Axel Mogk, Carmen Ruger-Herreros, Bernd Bukau. Cellular Functions and Mechanisms of Action of Small Heat Shock Proteins. Annual Review of Microbiology 2019, 73 (1) , 89-110. https://doi.org/10.1146/annurev-micro-020518-115515
    25. T. Reid Alderson, Elias Adriaenssens, Bob Asselbergh, Iva Pritišanac, Heidi Y. Gastall, Marielle A. Wälti, John M. Louis, Vincent Timmerman, Andrew J. Baldwin, Justin L. P. Benesch. Dysregulated interactions triggered by a neuropathy-causing mutation in the IPV motif of HSP27. 2019https://doi.org/10.1101/708180
    26. Martin Haslbeck, Sevil Weinkauf, Johannes Buchner. Small heat shock proteins: Simplicity meets complexity. Journal of Biological Chemistry 2019, 294 (6) , 2121-2132. https://doi.org/10.1074/jbc.REV118.002809
    27. Olga Tkachenko, Justin L.P. Benesch, Andrew J. Baldwin. αB-crystallin inhibits amyloidogenesis by disassembling aggregation nuclei. 2018https://doi.org/10.1101/300541
    28. Hannah E.R. Baughman, Amanda F. Clouser, Rachel E. Klevit, Abhinav Nath. HspB1 and Hsc70 chaperones engage distinct tau species and have different inhibitory effects on amyloid formation. Journal of Biological Chemistry 2018, 293 (8) , 2687-2700. https://doi.org/10.1074/jbc.M117.803411
    29. Patrick C.A. van der Wel. Insights into protein misfolding and aggregation enabled by solid-state NMR spectroscopy. Solid State Nuclear Magnetic Resonance 2017, 88 , 1-14. https://doi.org/10.1016/j.ssnmr.2017.10.001
    30. Elias Adriaenssens, Thomas Geuens, Jonathan Baets, Andoni Echaniz-Laguna, Vincent Timmerman. Novel insights in the disease biology of mutant small heat shock proteins in neuromuscular diseases. Brain 2017, 140 (10) , 2541-2549. https://doi.org/10.1093/brain/awx187
    31. Serena Carra, Simon Alberti, Patrick A. Arrigo, Justin L. Benesch, Ivor J. Benjamin, Wilbert Boelens, Britta Bartelt-Kirbach, Bianca J.J.M. Brundel, Johannes Buchner, Bernd Bukau, John A. Carver, Heath Ecroyd, Cecilia Emanuelsson, Stephanie Finet, Nikola Golenhofen, Pierre Goloubinoff, Nikolai Gusev, Martin Haslbeck, Lawrence E. Hightower, Harm H. Kampinga, Rachel E. Klevit, Krzysztof Liberek, Hassane S. Mchaourab, Kathryn A. McMenimen, Angelo Poletti, Roy Quinlan, Sergei V. Strelkov, Melinda E. Toth, Elizabeth Vierling, Robert M. Tanguay. The growing world of small heat shock proteins: from structure to functions. Cell Stress and Chaperones 2017, 22 (4) , 601-611. https://doi.org/10.1007/s12192-017-0787-8
    32. T. Reid Alderson, Justin L.P. Benesch, Andrew J. Baldwin. Proline isomerization in the C-terminal region of HSP27. Cell Stress and Chaperones 2017, 22 (4) , 639-651. https://doi.org/10.1007/s12192-017-0791-z
    33. Boris I. Kurganov. Quantification of anti-aggregation activity of chaperones. International Journal of Biological Macromolecules 2017, 100 , 104-117. https://doi.org/10.1016/j.ijbiomac.2016.07.066
    34. Anastasia Zhuravleva, Dmitry M. Korzhnev. Protein folding by NMR. Progress in Nuclear Magnetic Resonance Spectroscopy 2017, 100 , 52-77. https://doi.org/10.1016/j.pnmrs.2016.10.002
    35. C. Yan, X. Zou. Modeling Protein Flexibility in Molecular Docking. 2017, 319-328. https://doi.org/10.1016/B978-0-12-409547-2.12351-0
    36. William M. Jacobs, Tuomas P. J. Knowles, Daan Frenkel, . Oligomers of Heat-Shock Proteins: Structures That Don’t Imply Function. PLOS Computational Biology 2016, 12 (2) , e1004756. https://doi.org/10.1371/journal.pcbi.1004756
    37. Jonathan M. Lamley, Carl Öster, Rebecca A. Stevens, Józef R. Lewandowski. Intermolecular Interactions and Protein Dynamics by Solid‐State NMR Spectroscopy. Angewandte Chemie 2015, 127 (51) , 15594-15598. https://doi.org/10.1002/ange.201509168
    38. Jonathan M. Lamley, Carl Öster, Rebecca A. Stevens, Józef R. Lewandowski. Intermolecular Interactions and Protein Dynamics by Solid‐State NMR Spectroscopy. Angewandte Chemie International Edition 2015, 54 (51) , 15374-15378. https://doi.org/10.1002/anie.201509168
    39. Donald Gagné, Rachel L. French, Chitra Narayanan, Miljan Simonović, Pratul K. Agarwal, Nicolas Doucet. Perturbation of the Conformational Dynamics of an Active-Site Loop Alters Enzyme Activity. Structure 2015, 23 (12) , 2256-2266. https://doi.org/10.1016/j.str.2015.10.011
    40. Andi Mainz, Jirka Peschek, Maria Stavropoulou, Katrin C Back, Benjamin Bardiaux, Sam Asami, Elke Prade, Carsten Peters, Sevil Weinkauf, Johannes Buchner, Bernd Reif. The chaperone αB-crystallin uses different interfaces to capture an amorphous and an amyloid client. Nature Structural & Molecular Biology 2015, 22 (11) , 898-905. https://doi.org/10.1038/nsmb.3108
    41. Jan‐Henrik Ardenkjaer‐Larsen, Gregory S. Boebinger, Arnaud Comment, Simon Duckett, Arthur S. Edison, Frank Engelke, Christian Griesinger, Robert G. Griffin, Christian Hilty, Hidaeki Maeda, Giacomo Parigi, Thomas Prisner, Enrico Ravera, Jan van Bentum, Shimon Vega, Andrew Webb, Claudio Luchinat, Harald Schwalbe, Lucio Frydman. Neue Ansätze zur Empfindlichkeitssteigerung in der biomolekularen NMR‐Spektroskopie. Angewandte Chemie 2015, 127 (32) , 9292-9317. https://doi.org/10.1002/ange.201410653
    42. Jan‐Henrik Ardenkjaer‐Larsen, Gregory S. Boebinger, Arnaud Comment, Simon Duckett, Arthur S. Edison, Frank Engelke, Christian Griesinger, Robert G. Griffin, Christian Hilty, Hidaeki Maeda, Giacomo Parigi, Thomas Prisner, Enrico Ravera, Jan van Bentum, Shimon Vega, Andrew Webb, Claudio Luchinat, Harald Schwalbe, Lucio Frydman. Facing and Overcoming Sensitivity Challenges in Biomolecular NMR Spectroscopy. Angewandte Chemie International Edition 2015, 54 (32) , 9162-9185. https://doi.org/10.1002/anie.201410653
    43. Theodoros K. Karamanos, Arnout P. Kalverda, Gary S. Thompson, Sheena E. Radford. Mechanisms of amyloid formation revealed by solution NMR. Progress in Nuclear Magnetic Resonance Spectroscopy 2015, 88-89 , 86-104. https://doi.org/10.1016/j.pnmrs.2015.05.002
    44. Raman Bakthisaran, Ramakrishna Tangirala, Ch. Mohan Rao. Small heat shock proteins: Role in cellular functions and pathology. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 2015, 1854 (4) , 291-319. https://doi.org/10.1016/j.bbapap.2014.12.019
    45. Björn M. Burmann, Sebastian Hiller. Chaperones and chaperone–substrate complexes: Dynamic playgrounds for NMR spectroscopists. Progress in Nuclear Magnetic Resonance Spectroscopy 2015, 86-87 , 41-64. https://doi.org/10.1016/j.pnmrs.2015.02.004
    46. David D Boehr, Xinran Liu, Xiaorong Yang. Targeting structural dynamics of the RNA-dependent RNA polymerase for anti-viral strategies. Current Opinion in Virology 2014, 9 , 194-200. https://doi.org/10.1016/j.coviro.2014.08.006
    47. Andrew J. Baldwin. An exact solution for R2,eff in CPMG experiments in the case of two site chemical exchange. Journal of Magnetic Resonance 2014, 244 , 114-124. https://doi.org/10.1016/j.jmr.2014.02.023
    48. Christine Slingsby, Graeme J. Wistow. Functions of crystallins in and out of lens: Roles in elongated and post-mitotic cells. Progress in Biophysics and Molecular Biology 2014, 115 (1) , 52-67. https://doi.org/10.1016/j.pbiomolbio.2014.02.006
    49. Georg K.A. Hochberg, Justin L.P. Benesch. Dynamical structure of αB-crystallin. Progress in Biophysics and Molecular Biology 2014, 115 (1) , 11-20. https://doi.org/10.1016/j.pbiomolbio.2014.03.003
    50. Dong Long, Guillaume Bouvignies, Lewis E. Kay. Measuring hydrogen exchange rates in invisible protein excited states. Proceedings of the National Academy of Sciences 2014, 111 (24) , 8820-8825. https://doi.org/10.1073/pnas.1405011111
    51. Rachel W. Martin. NMR Studies of Eye Lens Crystallins. 2014, 139-152. https://doi.org/10.1002/9780470034590.emrstm1354
    52. Tatyana B. Eronina, Natalia A. Chebotareva, Svetlana G. Roman, Sergey Yu. Kleymenov, Valentina F. Makeeva, Nikolay B. Poliansky, Konstantin O. Muranov, Boris I. Kurganov. Thermal denaturation and aggregation of apoform of glycogen phosphorylase b . Effect of crowding agents and chaperones. Biopolymers 2014, 101 (5) , 504-516. https://doi.org/10.1002/bip.22410
    53. Nicola Salvi. Introduction. 2014, 1-7. https://doi.org/10.1007/978-3-319-06170-2_1
    54. Marco Fragai, Claudio Luchinat, Tommaso Martelli, Enrico Ravera, Irit Sagi, Inna Solomonov, Yael Udi. SSNMR of biosilica-entrapped enzymes permits an easy assessment of preservation of native conformation in atomic detail. Chem. Commun. 2014, 50 (4) , 421-423. https://doi.org/10.1039/C3CC46896H
    55. Lucio Ferella, Claudio Luchinat, Enrico Ravera, Antonio Rosato. SedNMR: a web tool for optimizing sedimentation of macromolecular solutes for SSNMR. Journal of Biomolecular NMR 2013, 57 (4) , 319-326. https://doi.org/10.1007/s10858-013-9795-x
    56. B. I. Kurganov. Antiaggregation activity of chaperones and its quantification. Biochemistry (Moscow) 2013, 78 (13) , 1554-1566. https://doi.org/10.1134/S0006297913130129
    57. Marco Fragai, Claudio Luchinat, Giacomo Parigi, Enrico Ravera. Practical considerations over spectral quality in solid state NMR spectroscopy of soluble proteins. Journal of Biomolecular NMR 2013, 57 (2) , 155-166. https://doi.org/10.1007/s10858-013-9776-0
    58. Ivano Bertini, Gianluca Gallo, Magdalena Korsak, Claudio Luchinat, Jiafei Mao, Enrico Ravera. Formation Kinetics and Structural Features of Beta‐Amyloid Aggregates by Sedimented Solute NMR. ChemBioChem 2013, 14 (14) , 1891-1897. https://doi.org/10.1002/cbic.201300141
    59. Vera A. Borzova, Kira A. Markossian, Dmitriy A. Kara, Natalia A. Chebotareva, Valentina F. Makeeva, Nikolay B. Poliansky, Konstantin O. Muranov, Boris I. Kurganov, . Quantification of Anti-Aggregation Activity of Chaperones: A Test-System Based on Dithiothreitol-Induced Aggregation of Bovine Serum Albumin. PLoS ONE 2013, 8 (9) , e74367. https://doi.org/10.1371/journal.pone.0074367
    60. Gillian R. Hilton, Georg K. A. Hochberg, Arthur Laganowsky, Scott I. McGinnigle, Andrew J. Baldwin, Justin L. P. Benesch. C-terminal interactions mediate the quaternary dynamics of αB-crystallin. Philosophical Transactions of the Royal Society B: Biological Sciences 2013, 368 (1617) , 20110405. https://doi.org/10.1098/rstb.2011.0405
    61. Scott P. Delbecq, Rachel E. Klevit. One size does not fit all: The oligomeric states of αB crystallin. FEBS Letters 2013, 587 (8) , 1073-1080. https://doi.org/10.1016/j.febslet.2013.01.021
    62. Christine Slingsby, Graeme J. Wistow, Alice R. Clark. Evolution of crystallins for a role in the vertebrate eye lens. Protein Science 2013, 22 (4) , 367-380. https://doi.org/10.1002/pro.2229
    63. Andrew J. Baldwin, Lewis E. Kay. An R1ρ expression for a spin in chemical exchange between two sites with unequal transverse relaxation rates. Journal of Biomolecular NMR 2013, 55 (2) , 211-218. https://doi.org/10.1007/s10858-012-9694-6
    Download PDF
    Go to Journal of the American Chemical Society
    Get e-Alerts
    Get e-Alerts

    Journal of the American Chemical Society

    Cite this: J. Am. Chem. Soc. 2012, 134, 37, 15343–15350
    Click to copy citationCitation copied!
    https://doi.org/10.1021/ja307874r
    Published August 23, 2012
    Copyright © 2012 American Chemical Society
    Request reuse permissions

    Article Views

    1855

    Altmetric

    -

    Citations

    58
    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.