The client protein p53 adopts a molten globule–like state in the presence of Hsp90
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It is not currently known in what state (folded, unfolded or alternatively folded) client proteins interact with the chaperone Hsp90. We show that one client, the p53 DNA-binding domain, undergoes a structural change in the presence of Hsp90 to adopt a molten globule-like state. Addition of one- and two-domain constructs of Hsp90, as well as the full-length three-domain protein, to isotopically labeled p53 led to reduction in NMR signal intensity throughout p53, particularly in its central β-sheet. This reduction seems to be associated with a change of structure of p53 without formation of a distinct complex with Hsp90. Fluorescence and hydrogen-exchange measurements support a loosening of the structure of p53 in the presence of Hsp90 and its domains. We propose that Hsp90 interacts with p53 by multiple transient interactions, forming a dynamic heterogeneous manifold of conformational states that resembles a molten globule.
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p53 shows the strongest effects to the NTD-MD interface and the linker region.
“GR and MR both show notable effects with the CTD helix Cα2, which projects toward the MD (Fig. 6, B and D), while p53 shows the strongest effects to the NTD-MD interface and the linker region, consistent with previous studies (43, 53).”
From Client binding shifts the populations of dynamic Hsp90 conformations through an allosteric network (2021) · cites this paper as [43]
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MOLMOL: A program for display and analysis of macromolecular structures
Koradi, R., Billeter, M., & Kurt Wüthrich, A. (1996) · Journal of Molecular Graphics · doi:10.1016/0263-7855(96)00009-4 · Cited by 7,163 · see citing works
Vogelstein, B., Lane, D., & Levine, A. J. (2000) · Nature · doi:10.1038/35042675 · Cited by 6,607 · cited 1× · see citing works
“One Hsp90 client that has been extensively studied is the tumor suppressor p53 , a 393-residue transcription factor that is mutated in >50% of human cancer”
BackgroundNMR View: A computer program for the visualization and analysis of NMR data
Johnson, B. A., & Blevins, R. A. (1994) · Journal of Biomolecular NMR · doi:10.1007/bf00404272 · Cited by 3,093 · see citing works
Steroid Receptor Interactions with Heat Shock Protein and Immunophilin Chaperones*
Pratt, W. B., & Toft, D. O. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.3.0303 · Cited by 1,791 · see citing works
Protein Folding Intermediates: Native-State Hydrogen Exchange
Bai, Y., Sosnick, T. R., Mayne, L. C., & Englander, S. W. (1995) · Science · doi:10.1126/science.7618079 · Cited by 991 · see citing works
Crystal structure of an Hsp90–nucleotide–p23/Sba1 closed chaperone complex
Ali, M. M. U., Roe, S. M., Vaughan, C. K., Meyer, P., Panaretou, B., Piper, P. W., Prodromou, C., & Pearl, L. H. (2006) · Nature · doi:10.1038/nature04716 · Cited by 962 · see citing works
Wittekind, M. G., & Mueller, L. J. (1993) · Journal of Magnetic Resonance Series B · doi:10.1006/jmrb.1993.1033 · Cited by 871 · see citing works
Improved 3D triple-resonance NMR techniques applied to a 31 kDa protein
Grzesiek, S., & Bax, A. (1992) · Journal of Magnetic Resonance (1969) · doi:10.1016/0022-2364(92)90099-s · Cited by 746 · see citing works
Schanda, P., Kupče, Ē., & Brutscher, B. (2005) · Journal of Biomolecular NMR · doi:10.1007/s10858-005-4425-x · Cited by 712 · see citing works
Hsp90: Chaperoning signal transduction
Richter, K., & Büchner, J. (2001) · Journal of Cellular Physiology · doi:10.1002/jcp.1131 · Cited by 570 · see citing works
Yamazaki, T., Lee, W., Arrowsmith, C. H., Muhandiram, D. R., & Kay, L. E. (1994) · Journal of the American Chemical Society · doi:10.1021/ja00105a005 · Cited by 499 · see citing works
Baum, J., Dobson, C. M., Evans, P. A., & Hanley, C. (1989) · Biochemistry · doi:10.1021/bi00427a002 · Cited by 470 · see citing works
Shiau, A. K., Harris, S. F., Southworth, D. R., & Agard, D. A. (2006) · Cell · doi:10.1016/j.cell.2006.09.027 · Cited by 455 · see citing works
Multifactorial analysis of p53 alteration in human cancer: A review
Soussi, T., Legros, Y., Lubin, R., Ory, K., & Schlichtholz, B. (1994) · International Journal of Cancer · doi:10.1002/ijc.2910570102 · Cited by 351 · see citing works
Mutant conformation of p53 translated in vitro or in vivo requires functional HSP90.
Blagosklonny, M. V., Toretsky, J. A., Bohen, S. P., & Neckers, L. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.16.8379 · Cited by 312 · see citing works
Structure of an Hsp90-Cdc37-Cdk4 Complex
Vaughan, C. K., Gohlke, U., Sobott, F., Good, V. M., Ali, M. M. U., Prodromou, C., Robinson, C. V., Saibil, H. R., & Pearl, L. H. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.07.016 · Cited by 293 · see citing works
A residue-specific NMR view of the non-cooperative unfolding of a molten globule
Schulman, B. A., Kim, P. S., Dobson, C. M., & Redfield, C. (1997) · Nature Structural Biology · doi:10.1038/nsb0897-630 · Cited by 251 · see citing works
Chaperoning of Glucocorticoid Receptors
Pratt, W. B., Morishima, Y., Murphy, M. N., & Harrell, M. (2005) · Springer eBooks · doi:10.1007/3-540-29717-0_5 · Cited by 247 · see citing works
Hot-spot mutants of p53 core domain evince characteristic local structural changes
Wong, K., DeDecker, B. S., Freund, S. M. V., Proctor, M. R., Bycroft, M., & Fersht, A. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.15.8438 · Cited by 219 · see citing works
Whitesell, L. J., Sutphin, P. D., Pulcini, E. J., Martinez, J. D., & Cook, P. H. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.3.1517 · Cited by 207 · see citing works
An Antibody Binding Site on Cytochrome C Defined by Hydrogen Exchange and Two-Dimensional NMR
Paterson, Y. Y. W., Englander, S. W., & Röder, H. (1990) · Science · doi:10.1126/science.1697101 · Cited by 186 · see citing works
Solution structure of p53 core domain: Structural basis for its instability
Cañadillas, J. M. P., Tidow, H., Freund, S. M. V., Rutherford, T. J., Ang, H. C., & Fersht, A. R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510941103 · Cited by 174 · see citing works
Hsp90 Regulates the Activity of Wild Type p53 under Physiological and Elevated Temperatures
Müller, L., Schaupp, A., Walerych, D., Wegele, H., & Büchner, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407687200 · Cited by 154 · see citing works
Constantly Updated Knowledge of Hsp90
Terasawa, K. (2005) · The Journal of Biochemistry · doi:10.1093/jb/mvi056 · Cited by 151 · see citing works
Structural characterization of a highly–ordered ‘molten globule’ at low pH
Redfield, C., Smith, R. A., & Dobson, C. M. (1994) · Nature Structural & Molecular Biology · doi:10.1038/nsb0194-23 · Cited by 136 · see citing works
The Middle Domain of Hsp90 Acts as a Discriminator between Different Types of Client Proteins
Hawle, P., Siepmann, M., Harst, A., Siderius, M., Reusch, H. P., & Obermann, W. M. J. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.02188-05 · Cited by 127 · cited 1× · see citing works
“The complexes between Hsp90 and different clients may be quite different and may even involve different sites on the chaperon”
BackgroundNative and Non-native Secondary Structure and Dynamics in the pH 4 Intermediate of Apomyoglobin
Eliezer, D., Chung, J., Dyson, H. J., & Wright, P. E. (2000) · Biochemistry · doi:10.1021/bi992545f · Cited by 114 · see citing works
Self-citationKinetics and thermodynamics of the interaction of 1-anilino-naphthalene-8-sulfonate with proteins
Cattoni, D. I., Kaufman, S. B., & Flecha, F. L. G. (2009) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2009.08.007 · Cited by 99 · see citing works
CRINEPT-TROSY NMR reveals p53 core domain bound in an unfolded form to the chaperone Hsp90
Rüdiger, S., Freund, S. M. V., Veprintsev, D. B., & Fersht, A. R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.132393699 · Cited by 97 · see citing works
Recognition of DNA by p53 Core Domain and Location of Intermolecular Contacts of Cooperative Binding
Rippin, T. M., Freund, S. M. V., Veprintsev, D. B., & Fersht, A. R. (2002) · Journal of Molecular Biology · doi:10.1016/s0022-2836(02)00326-1 · Cited by 80 · see citing works
Localization of Sites of Interaction between p23 and Hsp90 in Solution
Martinez‐Yamout, M. A., Venkitakrishnan, R. P., Preece, N. E., Kroon, G. J. A., Wright, P. E., & Dyson, H. J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m601759200 · Cited by 66 · see citing works
Self-citationEliezer, D., Jennings, P. A., Dyson, H. J., & Wright, P. E. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01256-8 · Cited by 56 · see citing works
Self-citationMulder, F. A. A., Ayed, A., Yang, D., Arrowsmith, C. H., & Kay, L. E. (2000) · Journal of Biomolecular NMR · doi:10.1023/a:1008317825976 · Cited by 32 · see citing works
Greene, L. H., Wijesinha‐Bettoni, R., & Redfield, C. (2006) · Biochemistry · doi:10.1021/bi060229c · Cited by 18 · see citing works
Flagged first, then by citations
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Sorted by citations
Schopf, F. H., Biebl, M. M., & Buchner, J. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.20 · Cited by 1,540 · see citing works
The Hsp90 chaperone machinery: Conformational dynamics and regulation by co-chaperones
Li, J., Soroka, J., & Buchner, J. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.09.003 · Cited by 498 · see citing works
Structure, Function and Regulation of the Hsp90 Machinery
Büchner, J., & Li, J. (2013) · Biomedical Journal · doi:10.4103/2319-4170.113230 · Cited by 420 · see citing works
Hsp90 and Hsp70 chaperones: Collaborators in protein remodeling
Genest, O., Wickner, S., & Doyle, S. M. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.rev118.002806 · Cited by 384 · see citing works
Jackson, S. (2012) · Topics in current chemistry · doi:10.1007/128_2012_356 · Cited by 334 · see citing works
Structure, Function, and Regulation of the Hsp90 MachineryPreprint
Biebl, M. M., & Büchner, J. (2019) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a034017 · Cited by 308 · see citing works
Structural basis for protein antiaggregation activity of the trigger factor chaperone.
Saio, T., Guan, X., Rossi, P., Economou, A., & Kalodimos, C. G. (2014) · Science · doi:10.1126/science.1250494 · Cited by 289 · see citing works
Mutant p53 Aggregates into Prion-like Amyloid Oligomers and Fibrils
Bom, A. P. D. A., Rangel, L. P., da Costa, D. C. F., de Oliveira, G. A. P., Sanches, D., Braga, C. A. C. A., Gava, L. M., Ramos, C. H. I., Tiroli‐Cepeda, A. O., Stumbo, A. C., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.340638 · Cited by 284 · see citing works
The chaperone Hsp90: changing partners for demanding clients
Röhl, A., Rohrberg, J., & Büchner, J. (2013) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2013.02.003 · Cited by 268 · see citing works
High-Pressure Chemical Biology and Biotechnology
Silva, J. L., de Oliveira, A. C., Vieira, T. C. R. G., de Oliveira, G. A. P., Suarez, M. C., & Foguel, D. (2014) · Chemical Reviews · doi:10.1021/cr400204z · Cited by 222 · see citing works
Expanding the proteome: disordered and alternatively folded proteins
Dyson, H. J. (2011) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583511000060 · Cited by 173 · see citing works
Self-citationProtein dynamics and function from solution state NMR spectroscopy
Kovermann, M., Rogne, P., & Wolf‐Watz, M. (2016) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583516000019 · Cited by 172 · see citing works
The Fic protein Doc uses an inverted substrate to phosphorylate and inactivate EF-Tu
Castro-Roa, D., García-Pino, A., Gieter, S. D., van Nuland, N. A. J., Loris, R., & Zenkin, N. (2013) · Nature Chemical Biology · doi:10.1038/nchembio.1364 · Cited by 167 · see citing works
Modulation of the Hsp90 Chaperone Cycle by a Stringent Client Protein
Lorenz, O. R., Freiburger, L., Rutz, D. A., Krause, M., Zierer, B. K., Alvira, S., Cuéllar, J., Valpuesta, J. M., Madl, T., Sattler, M., et al. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.02.003 · Cited by 151 · see citing works
Burmann, B. M., Wang, C., & Hiller, S. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2677 · Cited by 132 · see citing works
Integration of the accelerator Aha1 in the Hsp90 co-chaperone cycle
Li, J., Richter, K., Reinstein, J., & Büchner, J. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2502 · Cited by 130 · see citing works
Herbert, C., Schieborr, U., Saxena, K., Juraszek, J., Smet, F. D., Alcouffe, C., Bianciotto, M., Saladino, G., Sibrac, D., Kudlinzki, D., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.02.018 · Cited by 130 · see citing works
Krois, A. S., Dyson, H. J., & Wright, P. E. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1814051115 · Cited by 127 · see citing works
Self-citationGenest, O., Reidy, M., Street, T. O., Hoskins, J. R., Camberg, J. L., Agard, D. A., Masison, D. C., & Wickner, S. (2013) · Molecular Cell · doi:10.1016/j.molcel.2012.11.017 · Cited by 118 · see citing works
Structural analysis of the interaction between Hsp90 and the tumor suppressor protein p53
Hagn, F., Lagleder, S., Retzlaff, M., Rohrberg, J., Demmer, O., Richter, K., Buchner, J., & Kessler, H. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2114 · Cited by 127 · see citing works
Mechanisms of amyloid formation revealed by solution NMR
Karamanos, T. K., Kalverda, A. P., Thompson, G. S., & Radford, S. E. (2015) · Progress in Nuclear Magnetic Resonance Spectroscopy · doi:10.1016/j.pnmrs.2015.05.002 · Cited by 115 · see citing works
Differential Enzyme Flexibility Probed Using Solid-State Nanopores
Hu, R., Rodrigues, J. V., Waduge, P., Yamazaki, H., Cressiot, B., Chishti, Y., Makowski, L., Yu, D., Shakhnovich, E. I., Zhao, Q., et al. (2018) · ACS Nano · doi:10.1021/acsnano.8b00734 · Cited by 111 · see citing works
Probing the diverse landscape of protein flexibility and binding
Marsh, J. A., Teichmann, S. A., & Forman-Kay, J. D. (2012) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2012.08.008 · Cited by 107 · see citing works
Heat Shock Protein 90 in Alzheimer’s Disease
Ou, J.-R., Tan, M., Xie, A., Yu, J., & Tan, L. (2014) · BioMed Research International · doi:10.1155/2014/796869 · Cited by 99 · see citing works
Hsp90: Friends, clients and natural foes
Verma, S., Goyal, S., Jamal, S., Singh, A. P., & Grover, A. (2016) · Biochimie · doi:10.1016/j.biochi.2016.05.018 · Cited by 90 · see citing works
Dahiya, V., Agam, G. N., Lawatscheck, J., Rutz, D. A., Lamb, D. C., & Büchner, J. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.03.026 · Cited by 92 · see citing works
Franke, J., Eichner, S., Zeilinger, C., & Kirschning, A. (2013) · Natural Product Reports · doi:10.1039/c3np70012g · Cited by 88 · see citing works
Oncogenic Gain of Function in Glioblastoma Is Linked to Mutant p53 Amyloid Oligomers
Pedrote, M. M., Motta, M. F., Ferretti, G. D. S., Norberto, D. R., Spohr, T. C. L. S., Lima, F. R. S., Gratton, E., Silva, J. L., & de Oliveira, G. A. P. (2020) · iScience · doi:10.1016/j.isci.2020.100820 · Cited by 89 · see citing works
Heat Shock Proteins and Disease Control in Aquatic Organisms
Sung, Y. Y., & MacRae, T. H. (2013) · Journal of Aquaculture Research & Development · doi:10.4172/2155-9546.s2-006 · Cited by 85 · see citing works
Dynamic Interaction of Hsp90 with Its Client Protein p53
Park, S. J., Kostić, M., & Dyson, H. J. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.05.030 · Cited by 79 · see citing works
Self-citationHsp90 structure and function studied by NMR spectroscopy
Didenko, T., Duarte, A. M. S., Karagöz, G. E., & Rüdiger, S. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.11.009 · Cited by 79 · see citing works
Small molecule modulators of protein-protein interactions: selected case studies
Aeluri, M., Chamakuri, S., Dasari, B., Guduru, S. K. R., Jimmidi, R., Jogula, S., & Arya, P. (2014) · Chemical Reviews · doi:10.1021/cr4004049 · Cited by 79 · see citing works
p53 protects against LPS-induced lung endothelial barrier dysfunction
Barabutis, N., Dimitropoulou, C., Birmpas, C., Joshi, A., Thangjam, G. S., & Catravas, J. D. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00334.2014 · Cited by 76 · see citing works
Functional principles and regulation of molecular chaperones
Dahiya, V., & Büchner, J. (2018) · Advances in protein chemistry and structural biology · doi:10.1016/bs.apcsb.2018.10.001 · Cited by 75 · see citing works
Quintana‐Gallardo, L., Martín‐Benito, J., Marcilla, M., Espadas, G., Sabidó, E., & Valpuesta, J. (2019) · Scientific Reports · doi:10.1038/s41598-019-41060-0 · Cited by 74 · see citing works
Silva, J. L., Rangel, L. P., da Costa, D. C. F., Cordeiro, Y., & Gallo, C. V. D. M. (2013) · Bioscience Reports · doi:10.1042/bsr20130065 · Cited by 70 · see citing works
Biaoxue, R., & Yang, S. (2017) · International Journal of Oncology · doi:10.3892/ijo.2017.4214 · Cited by 67 · see citing works
Zhuravleva, A., & Korzhnev, D. M. (2016) · Progress in Nuclear Magnetic Resonance Spectroscopy · doi:10.1016/j.pnmrs.2016.10.002 · Cited by 59 · see citing works
Client binding shifts the populations of dynamic Hsp90 conformations through an allosteric network
Lopez, A., Dahiya, V., Delhommel, F., Freiburger, L., Stehle, R., Asami, S., Rutz, D., Blair, L., Buchner, J., & Sattler, M. (2021) · Science Advances · doi:10.1126/sciadv.abl7295 · Cited by 59 · see citing works
Mechanistic basis for the recognition of a misfolded protein by the molecular chaperone Hsp90
Oroz, J., Kim, J. H., Chang, B. J., & Zweckstetter, M. (2017) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3380 · Cited by 58 · see citing works
Razzak, M. A., & Choi, S. S. (2021) · Food Chemistry · doi:10.1016/j.foodchem.2020.128981 · Cited by 57 · see citing works
Chaperone-Bound Clients: The Importance of Being Dynamic
Hiller, S. (2019) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2018.12.005 · Cited by 54 · see citing works
Heat stress: A risk factor for skin carcinogenesis
Calapre, L., Gray, E. S., & Ziman, M. R. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.05.039 · Cited by 55 · see citing works
Misfolding, Aggregation, and Disordered Segments in c-Abl and p53 in Human Cancer
de Oliveira, G. A. P., Rangel, L. P., da Costa, D. C. F., & Silva, J. L. (2015) · Frontiers in Oncology · doi:10.3389/fonc.2015.00097 · Cited by 55 · see citing works
Qadeer, A., Rabbani, G., Zaidi, N., Ahmad, E., Khan, J. M., & Khan, R. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050633 · Cited by 52 · see citing works
Allosteric Switching of Calmodulin in a Mycobacterium smegmatis porin A (MspA) Nanopore‐Trap
Liu, Y., Pan, T., Wang, K., Wang, Y., Yan, S., Wang, L., Zhang, S., Du, X., Jia, W., Zhang, P., et al. (2021) · Angewandte Chemie International Edition · doi:10.1002/anie.202110545 · Cited by 51 · see citing works
Elucidating the Mechanism of Substrate Recognition by the Bacterial Hsp90 Molecular Chaperone
Street, T. O., Zeng, X., Pellarin, R., Bonomi, M., Šali, A., Kelly, M. J. S., Feixia Chu, C., & Agard, D. A. (2014) · Journal of Molecular Biology · doi:10.1016/j.jmb.2014.04.001 · Cited by 50 · see citing works
Lebedev, I., Nemajerová, A., Foda, Z. H., Kornaj, M., Tong, M., Moll, U. M., & Seeliger, M. A. (2016) · Journal of Molecular Biology · doi:10.1016/j.jmb.2016.08.001 · Cited by 47 · see citing works
He, W.-T., Xue, W., Gao, Y., Hong, J.-Y., Yue, H.-W., Jiang, L.-L., & Hu, H.-Y. (2017) · Scientific Reports · doi:10.1038/s41598-017-13711-7 · Cited by 46 · see citing works
Molecular origins of binding affinity: seeking the Archimedean point
Kastritis, P. L., & Bonvin, A. M. J. J. (2013) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2013.07.001 · Cited by 43 · see citing works
Chaperones and chaperone–substrate complexes: Dynamic playgrounds for NMR spectroscopists
Burmann, B. M., & Hiller, S. (2015) · Progress in Nuclear Magnetic Resonance Spectroscopy · doi:10.1016/j.pnmrs.2015.02.004 · Cited by 40 · see citing works
Hsp90 interacts with AMPK and mediates acetyl-CoA carboxylase phosphorylation
Zhang, L., Yi, Y., Guo, Q., Sun, Y., Shun, M., Xiao, S., Geng, J., Zheng, Z., & Song, S. (2011) · Cellular Signalling · doi:10.1016/j.cellsig.2011.12.001 · Cited by 42 · see citing works
Hervás, R., & Oroz, J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21239186 · Cited by 43 · see citing works
The Molten Globule Concept: 45 Years Later
Bychkova, V. E., Semisotnov, G. V., Balobanov, V. A., & Finkelstein, A. V. (2018) · Biochemistry (Moscow) · doi:10.1134/s0006297918140043 · Cited by 39 · see citing works
Sun, M., Kotler, J. L. M., Liu, S., & Street, T. O. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.007050 · Cited by 38 · see citing works
Monomeric α-Synuclein Binds Congo Red Micelles in a Disordered Manner
Maltsev, A. S., Grishaev, A., & Bax, A. (2011) · Biochemistry · doi:10.1021/bi201435d · Cited by 33 · see citing works
Structural Mapping of a Chaperone–Substrate Interaction Surface
Callon, M., Burmann, B. M., & Hiller, S. (2014) · Angewandte Chemie International Edition · doi:10.1002/anie.201310963 · Cited by 33 · see citing works
Amyloidogenic behavior of different intermediate state of stem bromelain: A biophysical insight
Zaman, M., Ehtram, A., Chaturvedi, S. K., Nusrat, S., & Khan, R. H. (2016) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2016.05.107 · Cited by 31 · see citing works
Kumari, N., Mathe, V. L., & Dongre, P. M. (2018) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2018.12.184 · Cited by 27 · see citing works
Role of peroxynitrite induced structural changes on H2B histone by physicochemical method
Khan, M. A., Alam, K., Dixit, K., & Rizvi, M. M. A. (2015) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2015.10.085 · Cited by 27 · see citing works
Zhou, C., Zhang, C., Zhu, H., Liu, Z., Su, H., Zhang, X., Chen, T., Zhong, Y., Hu, H., Xiong, M., et al. (2020) · iScience · doi:10.1016/j.isci.2020.100857 · Cited by 25 · see citing works
Nusrat, S., Zaidi, N., Zaman, M., Islam, S., Ajmal, M., Siddiqi, M., Santra, M., & Khan, R. H. (2016) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2016.10.014 · Cited by 24 · see citing works
Hasan, S., & Naeem, A. (2020) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2020.06.127 · Cited by 24 · see citing works
New structural insights into Golgi Reassembly and Stacking Protein (GRASP) in solution
Mendes, L. F. S., Garcia, A. F., Kumagai, P. S., de Morais, F. R., Melo, F. A., Kmetzsch, L., Vainstein, M. H., Rodrigues, M. L., & Costa-Filho, A. J. (2016) · Scientific Reports · doi:10.1038/srep29976 · Cited by 24 · see citing works
Blacklock, K. M., & Verkhivker, G. M. (2013) · Journal of Chemical Information and Modeling · doi:10.1021/ci400434g · Cited by 25 · see citing works
Wang, F., Zhang, H., Wang, H., Qiu, T., He, B., & Yang, Q. (2022) · Medical Oncology · doi:10.1007/s12032-022-01777-x · Cited by 23 · see citing works
CD44 Receptor Unfolding Enhances Binding by Freeing Basic Amino Acids to Contact Carbohydrate Ligand
Favreau, A. J., Faller, C. E., & Guvench, O. (2013) · Biophysical Journal · doi:10.1016/j.bpj.2013.07.041 · Cited by 22 · see citing works
Non-equilibrium conformational dynamics in the function of molecular chaperones
Barducci, A., & Rios, P. D. L. (2015) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2015.02.008 · Cited by 21 · see citing works
Chaperone–client complexes: A dynamic liaison
Hiller, S., & Burmann, B. M. (2018) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2017.12.008 · Cited by 21 · see citing works
Bychkova, V. E., Dolgikh, D. A., Balobanov, V. A., & Finkelstein, A. V. (2022) · Molecules · doi:10.3390/molecules27144361 · Cited by 20 · see citing works
He, L., & Hiller, S. (2019) · ChemBioChem · doi:10.1002/cbic.201900215 · Cited by 18 · see citing works
Structural basis for the dynamic chaperoning of disordered clients by Hsp90
Qu, X., Zhao, S., Wan, C., Zhu, L., Ji, T., Rossi, P., Wang, J., Kalodimos, C. G., Wang, C., Xu, W., et al. (2024) · Nature Structural & Molecular Biology · doi:10.1038/s41594-024-01337-z · Cited by 19 · see citing works
Siddaramaiah, M., Satyamoorthy, K., Rao, B. S. S., Roy, S., Chandra, S., & Mahato, K. K. (2016) · Spectrochimica Acta Part A Molecular and Biomolecular Spectroscopy · doi:10.1016/j.saa.2016.11.017 · Cited by 19 · see citing works
Pawar, M. D., Busov, B., Chandrasekhar, A., Yao, J., Zacks, D. N., & Besirli, C. G. (2017) · Cell Death and Differentiation · doi:10.1038/cdd.2017.109 · Cited by 18 · see citing works
Siddiqi, M. K., Shahein, Y. E., Hussein, N. A., & Khan, R. H. (2016) · Journal of Molecular Structure · doi:10.1016/j.molstruc.2016.04.002 · Cited by 17 · see citing works
Jin, Y., Kotler, J. L. M., Wang, S., Huang, B., Halpin, J. C., & Street, T. O. (2021) · Journal of Molecular Biology · doi:10.1016/j.jmb.2021.166963 · Cited by 17 · see citing works
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Seidler, P. M., Shinsky, S. A., Hong, F., Li, Z., Cosgrove, M. S., & Gewirth, D. T. (2014) · Journal of Molecular Biology · doi:10.1016/j.jmb.2014.08.024 · Cited by 15 · see citing works
Wu, H.-W., Hyun, J.-S., Martinez-Yamout, M., Park, S. J., & Dyson, H. (2018) · Biochemistry · doi:10.1021/acs.biochem.7b01076 · Cited by 14 · see citing works
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Singh, S. K., Qiao, Z., Song, L., Jani, V., Rice, W., Eng, E., Coleman, R. A., & Liu, W. (2016) · Biophysical Journal · doi:10.1016/j.bpj.2016.11.1173 · Cited by 16 · see citing works
Transition of transferrin from native to fibrillar state: An implication for amyloid-linked diseases
Amani, S., & Naeem, A. (2014) · Biochemical Engineering Journal · doi:10.1016/j.bej.2014.08.004 · Cited by 15 · see citing works
Mendes, L. F. S., Batista, M., Judge, P. J., Watts, A. G., Redfield, C., & Costa-Filho, A. J. (2020) · FEBS Journal · doi:10.1111/febs.15206 · Cited by 14 · see citing works
Kim, H.-H., Hyun, J.-S., Choi, J., Choi, K.-E., Jee, J., & Park, S. J. (2018) · Scientific Reports · doi:10.1038/s41598-017-18332-8 · Cited by 17 · see citing works
Self-citationAluksanasuwan, S., Peerapen, P., Plumworasawat, S., Manissorn, J., & Thongboonkerd, V. (2019) · Analytical Biochemistry · doi:10.1016/j.ab.2019.113518 · Cited by 11 · see citing works
Rahkila, J., Ekholm, F. S., Ardá, A., Delgado, S., Savolainen, J., Jiménez‐Barbero, J., & Leino, R. P. (2018) · ChemBioChem · doi:10.1002/cbic.201800423 · Cited by 10 · see citing works
Non-Equilibrium Protein Folding and Activation by ATP-Driven Chaperones
Xu, H. (2022) · Biomolecules · doi:10.3390/biom12060832 · Cited by 10 · see citing works
Aggregation of zinc‐free p53 is inhibited by Hsp90 but not other chaperones
Wu, H., & Dyson, H. J. (2019) · Protein Science · doi:10.1002/pro.3726 · Cited by 9 · see citing works
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Backe, S. J., Sager, R., Meluni, K. A., Woodford, M. R., Bourboulia, D., & Mollapour, M. (2022) · Biomolecules · doi:10.3390/biom12070928 · Cited by 9 · see citing works
Molecular chaperones and their denaturing effect on client proteins
Hiller, S. (2020) · Journal of Biomolecular NMR · doi:10.1007/s10858-020-00353-7 · Cited by 8 · see citing works
A comparison of four technologies for detecting p53 aggregates in ovarian cancer
Heinzl, N., Kozieł, K., Maritschnegg, E., Berger, A., Pechriggl, E. J., Fiegl, H., Zeimet, A. G., Marth, C., Zeillinger, R., & Concin, N. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.976725 · Cited by 7 · see citing works
NMR Study of larger proteins using isotope labeling
Park, S. J. (2014) · Journal of the Korean Magnetic Resonance Society · doi:10.6564/jkmrs.2014.18.2.047 · Cited by 6 · see citing works
Self-citationATP-Driven Nonequilibrium Activation of Kinase Clients by the Molecular Chaperone Hsp90
Xu, H. (2020) · Biophysical Journal · doi:10.1016/j.bpj.2020.08.038 · Cited by 6 · see citing works
Walczak, M., Samatanga, B., van Drogen, F., Peter, M., Jelesarov, I., & Wider, G. (2013) · Angewandte Chemie International Edition · doi:10.1002/anie.201306702 · Cited by 6 · see citing works
Allosteric Switching of Calmodulin in a Mycobacterium smegmatis porin A (MspA) Nanopore‐Trap
Liu, Y., Pan, T., Wang, K., Wang, Y., Yan, S., Wang, L., Zhang, S., Du, X., Jia, W., Zhang, P., et al. (2021) · Angewandte Chemie · doi:10.1002/ange.202110545 · Cited by 6 · see citing works
Malik, A., Khan, J. M., Alhomida, A. S., & Ola, M. S. (2022) · Gels · doi:10.3390/gels8050273 · Cited by 6 · see citing works
An Insight to Heat Shock Protein 90: A Remedy for Multiple Problems
Yadav, M., Singh, A. K., Kumar, A., Thareja, S., & Kumar, P. (2022) · Current Pharmaceutical Design · doi:10.2174/1381612828666220829120630 · Cited by 6 · see citing works
Hydrophobicity-dependent effects of polymers on different protein conformations
Conniff, A. S., Breydo, L., Porto, T. S., Porto, A. L. F., & Uversky, V. N. (2016) · RSC Advances · doi:10.1039/c6ra07910e · Cited by 5 · see citing works
Kumari, N., Mathe, V. L., Krishna, C. M., & Dongre, P. M. (2021) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2021.1925155 · Cited by 5 · see citing works
Probing conformational change of T7 RNA polymerase and DNA complex by solid-state nanopores
Tong, X., Hu, R., Li, X., & Zhao, Q. (2018) · Chinese Physics B · doi:10.1088/1674-1056/27/11/118705 · Cited by 5 · see citing works
Using NMR to identify binding regions for N and C-terminal Hsp90 inhibitors using Hsp90 domains
McConnell, J. R., Dyson, H. J., & McAlpine, S. R. (2021) · RSC Medicinal Chemistry · doi:10.1039/d0md00387e · Cited by 5 · see citing works
Self-citationVerkhivker, G. M. (2014) · Israel Journal of Chemistry · doi:10.1002/ijch.201300143 · Cited by 4 · see citing works
- Authors
- Park, S. J., Borin, B. N., Martinez-Yamout, M. A., & Dyson, H. J.
- Affiliations
- Scripps Research Institute (US)
- Corresponding author
- Dyson, H Jane
- Venue
- Nature Structural & Molecular Biology
- Published
- 2011-04-03
- Volume
- 18
- Issue
- 5
- Pages
- 537-541
- ISSN
- 1545-9985 (ISSN-L)
- 1545-9993
- PMC
- PMC3087862
- OpenAlex
- W2074979923
- Cited by
- 128
- References
- 34
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 8 · 2021: 9 · 2020: 9 · 2019: 10 · 2018: 13 · 2017: 6 · 2016: 12 · 2015: 6 · 2014: 13 · 2013: 18 · 2012: 7
- FWCI
- 5.97
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Structural & Molecular Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of General Medical Sciences (GM57374, R01GM057374)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Keywords
- p53, HSP90, molten globule, protein conformation, DNA-binding domain, molecular chaperones, client proteins, transient interactions, conformational heterogeneity, protein folding, tumor suppressor
- MeSH terms
- Amino Acid Sequence, Binding Sites, Humans, Models, Molecular, Spectrometry, Fluorescence, Tumor Suppressor Protein p53, Protein Structure, Tertiary, Protein Folding, HSP90 Heat-Shock Proteins, Nuclear Magnetic Resonance, Biomolecular
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