Uncovering a region of heat shock protein 90 important for client binding in E. coli and chaperone function in yeast
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The heat shock protein 90 (Hsp90) family of heat shock proteins is an abundantly expressed and highly conserved family of ATP-dependent molecular chaperones. Hsp90 facilitates remodeling and activation of hundreds of proteins. In this study, we developed a screen to identify Hsp90-defective mutants in E. coli. The mutations obtained define a region incorporating residues from the middle and C-terminal domains of E. coli Hsp90. The mutant proteins are defective in chaperone activity and client binding in vitro. We constructed homologous mutations in S. cerevisiae Hsp82 and identified several that caused defects in chaperone activity in vivo and in vitro. However, the Hsp82 mutant proteins were less severely defective in client binding to a model substrate than the corresponding E. coli mutant proteins. Our results identify a region in Hsp90 important for client binding in E. coli Hsp90 and suggest an evolutionary divergence in the mechanism of client interaction by bacterial and yeast Hsp90.
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The FK1 pocket sits roughly 17 Å away from the Hsp90 client-binding sites Y528, Q531 and M610.
“This pocket is approximately 17 Å from Hsp90 client binding sites, which include Y528, Q531, and M610”
From The structure of an Hsp90-immunophilin complex reveals cochaperone recognition of the client maturation state (2021) · cites this paper as Genest et al., 2013
The Discussion (page unavailable) identifies a client-binding region of Hsp90, supporting that general part of the claim. Our copy does not identify Y528, Q531, or M610 as client-binding sites or give an approximately 17 Å distance from an FK1 pocket (searched those residues, FK1, and the distance). (LLM, conf=0.78)
Experimental — accuracy not yet measuredIn the Hsp90:FKBP51:p23 structure, FKBP51 runs from its CTD-TPR contact along the Hsp90 middle domain, placing the N-terminal FK1 domain next to the sites where Hsp90 engages clients.
“In the Hsp90:FKBP51:p23 structure FKBP51 extends from the CTD-TPR interaction along the Hsp90 MD, enabling the N-terminal FK1 domain to be positioned adjacent Hsp90 client interaction sites”
From The structure of an Hsp90-immunophilin complex reveals cochaperone recognition of the client maturation state (2021) · cites this paper as Genest et al., 2013
The Discussion identifies an Hsp90 client-binding region in its middle and C-terminal domains, supporting the reference to client-interaction sites. It does not describe an Hsp90:FKBP51:p23 structure or establish that FKBP51’s FK1 domain sits next to those sites; its identified region is specifically in E. coli Hsp90. (LLM, conf=0.86)
Experimental — accuracy not yet measuredMutations in the Cα2 element or its surroundings impair GR activation in vitro and in vivo.
“This is consistent with the fact that mutations in this element or its surroundings have been shown to impair GR activation in vitro and in vivo (2, 60, 62).”
From Client binding shifts the populations of dynamic Hsp90 conformations through an allosteric network (2021) · cites this paper as [62]
These sites are extended and harbor short amphipathic binding motifs: 423KNIKLG428, 505IDEY508, 554LKEIL558, and 589MERIM593.
“These sites are extended and harbor short amphipathic binding motifs, i.e., 423KNIKLG428, 505IDEY508, 554LKEIL558, and 589MERIM593, which, in part, have been implicated in client binding in vivo (60–62).”
From Client binding shifts the populations of dynamic Hsp90 conformations through an allosteric network (2021) · cites this paper as [62]
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“Sti1-biotin (2 μM) and Ssa1 wild-type or mutant (4 μM) or Ydj1-biotin (1.2 μM) with Ssa1 wild-type or mutant (2 μM) were incubated for 5 min at 23 °C in reaction mixtures (50 μL) containing PD buffer as indicated.”
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Self-citationSattin, S., Tao, J., Vettoretti, G., Moroni, E., Pennati, M., Lopergolo, A., Morelli, L., Bugatti, A., Zuehlke, A. D., Moses, M., et al. (2015) · Chemistry - A European Journal · doi:10.1002/chem.201502211 · Cited by 66 · see citing works
Self-citationBiebl, M. M., Lopez, A., Rehn, A., Freiburger, L., Lawatscheck, J., Blank, B., Sattler, M., & Buchner, J. (2021) · Nature Communications · doi:10.1038/s41467-021-21063-0 · Cited by 58 · 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
Hsp90 Is Essential under Heat Stress in the Bacterium Shewanella oneidensis
Honoré, F. A., Méjean, V., & Genest, O. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.03.082 · Cited by 59 · see citing works
“Hsp90So was visualized with an anti-Hsp90Ec antibody (Genest et al., 2013), and TilS was visualized with an anti-CBP antibody (Millipore 07-482).”
BackgroundMethodInfluentialSelf-citationPaladino, A., Woodford, M. R., Backe, S. J., Sager, R., Kancherla, P., Daneshvar, M., Chen, V. Z., Bourboulia, D., Ahanin, E. F., Prodromou, C., et al. (2020) · Chemistry - A European Journal · doi:10.1002/chem.202000615 · Cited by 56 · 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
“Importantly, the same region was shown to be functionally relevant for client activation by yeast Hsp90 [20], attesting to conserved underlying mechanisms for Hsp90s from prokaryotes to eukaryotes.”
BackgroundInfluentialSelf-citationGorkovskiy, A., Reidy, M. J., Masison, D. C., & Wickner, R. B. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1704016114 · Cited by 49 · see citing works
“Hsp82 protein is defective in client binding and chaperone activity (77).”
BackgroundSelf-citationPartridge, J. R., Lavery, L. A., Elnatan, D., Naber, N. I., Cooke, R., & Agard, D. A. (2014) · eLife · doi:10.7554/elife.03487 · Cited by 48 · see citing works
Self-citationLigand Binding, Unbinding, and Allosteric Effects: Deciphering Small-Molecule Modulation of HSP90
D’Annessa, I., Raniolo, S., Limongelli, V., Marino, D. D., & Colombo, G. (2019) · Journal of Chemical Theory and Computation · doi:10.1021/acs.jctc.9b00319 · Cited by 48 · see citing works
Advances towards Understanding the Mechanism of Action of the Hsp90 Complex
Prodromou, C., & Bjorklund, D. M. (2022) · Biomolecules · doi:10.3390/biom12050600 · Cited by 47 · see citing works
Interaction of E. coli Hsp90 with DnaK Involves the DnaJ Binding Region of DnaK
Kravats, A. N., Doyle, S. M., Hoskins, J. R., Genest, O., Doody, E. E., & Wickner, S. (2016) · Journal of Molecular Biology · doi:10.1016/j.jmb.2016.12.014 · Cited by 46 · see citing works
“Hsp90 is a homodimer with each monomer consisting of three domains: an Nterminal domain that possesses an ATP binding site [15, 16]; a middle domain containing residues that participate in binding client proteins [7, 14, 15, 17]; and a Cterminal domain that is essential for dimerization and is also involved in client…”
BackgroundSelf-citationA switch point in the molecular chaperone Hsp90 responding to client interaction
Rutz, D. A., Luo, Q., Freiburger, L., Madl, T., Kaila, V. R. I., Sattler, M., & Buchner, J. (2018) · Nature Communications · doi:10.1038/s41467-018-03946-x · Cited by 37 · see citing works
Zuehlke, A. D., Reidy, M. J., Lin, C. P. C., LaPointe, P., Alsomairy, S., Lee, D. J., Rivera-Márquez, G. M., Beebe, K. E., Prince, T. L., Lee, S., et al. (2017) · Nature Communications · doi:10.1038/ncomms15328 · Cited by 38 · see citing works
Self-citationThe Bacterial Hsp90 Chaperone: Cellular Functions and Mechanism of Action
Wickner, S., Nguyen, T.-L. L., & Genest, O. (2021) · Annual Review of Microbiology · doi:10.1146/annurev-micro-032421-035644 · Cited by 40 · see citing works
Self-citationCryo-EM structures reveal a multistep mechanism of Hsp90 activation by co-chaperone Aha1
Liu, Y., Sun, M., Myasnikov, A. G., Elnatan, D., Delaeter, N., Nguyenquang, M., & Agard, D. A. (2020) · doi:10.1101/2020.06.30.180695 · Cited by 37 · see citing works
Self-citationBlacklock, K. M., & Verkhivker, G. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071936 · Cited by 38 · see citing works
Eckl, J. M., Scherr, M. J., Freiburger, L. A., Daake, M., Sattler, M., & Richter, K. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.693150 · Cited by 38 · see citing works
“It still remains an open question how a client is attached to Hsp90, in particular as binding sites in the N-terminal, middle, and C-terminal domains of Hsp90 have been shown to be important for client interactions (9, 25, 49).”
BackgroundReidy, M. J., Sharma, R., Roberts, B.-L., & Masison, D. C. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.700393 · Cited by 38 · see citing works
“Ssa1 was purified as described previously for HspA1A (33).”
MethodSelf-citationSànchez‐Martìn, C., Serapian, S. A., Colombo, G., & Rasola, A. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.01177 · Cited by 38 · see citing works
“This region has a key role in client binding (33) and is close to”
BackgroundHsp90 Co-chaperones Form Plastic Genetic Networks Adapted to Client Maturation
Biebl, M. M., Riedl, M., & Büchner, J. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108063 · Cited by 36 · see citing works
Roe, S. M., Wahab, B., Török, Z., Horváth, I., Vı́gh, L., & Prodromou, C. (2018) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2018.00051 · Cited by 35 · see citing works
“It is also noteworthy that the C-terminal domain of Hsp90 has been implicated as a client protein binding site (Genest et al., 2013) and client protein is known to activate the ATPase activity of Hsp90 (McLaughlin et al.”
BackgroundHeterologous Hsp90 promotes phenotypic diversity through network evolution
Koubková-Yu, T. C.-T., Chao, J.-C., & Leu, J. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2006450 · Cited by 34 · see citing works
How aberrant N-glycosylation can alter protein functionality and ligand binding: An atomistic view
Castelli, M., Yan, P., Rodina, A., Digwal, C. S., Panchal, P., Chiosis, G., Moroni, E., & Colombo, G. (2023) · Structure · doi:10.1016/j.str.2023.05.017 · Cited by 34 · see citing works
Czemeres, J., Buse, K., & Verkhivker, G. M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0190267 · Cited by 32 · see citing works
Maillot, N. J., Honoré, F. A., Byrne, D., Méjean, V., & Genest, O. (2019) · Communications Biology · doi:10.1038/s42003-019-0567-3 · Cited by 33 · see citing works
Self-citationHeat Shock Protein 90 Associates with the Per-Arnt-Sim Domain of Heme-free Soluble Guanylate Cyclase
Sarkar, A., Dai, Y., Haque, M. M., Seeger, F., Ghosh, A., Garcin, E. D., Montfort, W. R., Hazen, S. L., Misra, S., & Stuehr, D. J. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.645515 · Cited by 31 · see citing works
Bacterial Hsp90 Facilitates the Degradation of Aggregation-Prone Hsp70–Hsp40 Substrates
Fauvet, B., Finka, A., Castanié‐Cornet, M., Cirinesi, A.-M., Genevaux, P., Quadroni, M., & Goloubinoff, P. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.653073 · Cited by 28 · see citing works
Glucocorticoid receptor complexes form cooperatively with the Hsp90 co-chaperones Pp5 and FKBPs
Kaziales, A., Barkovits, K., Marcus, K., & Richter, K. (2020) · Scientific Reports · doi:10.1038/s41598-020-67645-8 · Cited by 24 · see citing works
Mechanistic Asymmetry in Hsp90 Dimers
Flynn, J. M., Mishra, P., & Bolon, D. N. A. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.03.017 · Cited by 26 · see citing works
Genome-scale Co-evolutionary Inference Identifies Functions and Clients of Bacterial Hsp90
Press, M. O., Li, H., Creanza, N., Krämer, G., Queitsch, C., Sourjik, V., & Borenstein, E. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003631 · Cited by 24 · see citing works
“The dependence of HtpG-client interactions upon the DnaK chaperone system, as observed by us and by others [14,15], argues that Hsp90A is well-integrated with other chaperone systems.”
BackgroundHsp90 of E. coli modulates assembly of FtsZ, the bacterial tubulin homolog
Balasubramanian, A., Markovski, M., Hoskins, J. R., Doyle, S. M., & Wickner, S. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1904014116 · Cited by 24 · see citing works
“coli causes a block in cell division and results in filamentous cells (22).”
BackgroundMethodResultInfluentialSelf-citationBlacklock, K. M., & Verkhivker, G. M. (2013) · Journal of Chemical Information and Modeling · doi:10.1021/ci400434g · Cited by 25 · see citing works
Dual Roles for Yeast Sti1/Hop in Regulating the Hsp90 Chaperone Cycle
Reidy, M., Kumar, S., Anderson, D. E., & Masison, D. C. (2018) · Genetics · doi:10.1534/genetics.118.301178 · Cited by 22 · see citing works
Self-citationHsp90, a team player in protein quality control and the stress response in bacteria
Wickramaratne, A. C., Wickner, S., & Kravats, A. N. (2024) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00176-22 · Cited by 23 · see citing works
“2A); this interaction region is conserved among bacterial, yeast, and eukaryotic ER chaperones (113, 116–121).”
BackgroundInfluentialSelf-citationInteractions of Escherichia coli molecular chaperone HtpG with DnaA replication initiator DNA
Grudniak, A., Markowska, K., & Wolska, K. I. (2015) · Cell Stress and Chaperones · doi:10.1007/s12192-015-0623-y · Cited by 23 · see citing works
Structural transitions modulate the chaperone activities of Grp94
Amankwah, Y. S., Fleifil, Y., Unruh, E., Collins, P., Wang, Y., Vitou, K., Bates, A., Obaseki, I., Sugoor, M., Alao, J. P., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2309326121 · Cited by 22 · see citing works
Verkhivker, G. M. (2018) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2018.04.008 · Cited by 20 · see citing works
Mangla, N., Singh, R., & Agarwal, N. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.00312-23 · Cited by 20 · see citing works
Evidence for Hsp90 Co-chaperones in Regulating Hsp90 Function and Promoting Client Protein Folding
Cox, M. B., & Johnson, J. L. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7477-1_28 · Cited by 20 · see citing works
J-domain Proteins form Binary Complexes with Hsp90 and Ternary Complexes with Hsp90 and Hsp70
Wickramaratne, A. C., Liao, J. R., Doyle, S. M., Hoskins, J. R., Puller, G. C., Scott, M. L., Alao, J. P., Obaseki, I., Dinan, J. C., Maity, T. K., et al. (2023) · Journal of Molecular Biology · doi:10.1016/j.jmb.2023.168184 · Cited by 19 · see citing works
Self-citationStructural 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
“These results indicate that Hsp90 M alone is responsible for client interaction, consistent with prior mutational studies 34,35 and the client recognition mode observed for other clients 36 .”
Triveri, A., Sànchez‐Martìn, C., Torielli, L., Serapian, S. A., Marchetti, F., D’Acerno, G., Pirota, V., Castelli, M., Moroni, E., Ferraro, M., et al. (2022) · Journal of Molecular Biology · doi:10.1016/j.jmb.2022.167468 · Cited by 18 · see citing works
Johnson, J. L., Zuehlke, A. D., Tenge, V. R., & Langworthy, J. C. (2014) · Current Genetics · doi:10.1007/s00294-014-0432-3 · Cited by 17 · see citing works
“However, recent studies provide new insights into how clients contact Hsp90 and how they may influence conformation (Genest et al. 2013; Lorenz et al. 2014; Street et al. 2011).”
BackgroundHSP70-HSP90 Chaperone Networking in Protein-Misfolding Disease
Prodromou, C., Aran-Guiu, X., Oberoi, J., Perna, L., Chapple, J. P., & van der Spuy, J. (2022) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-3-031-14740-1_13 · Cited by 17 · see citing works
“The FK1 domain is positioned adjacent to HSP90 client interaction sites (Genest et al., 2013; Verba et al., 2016) and may provide a means by which the PPIase activity of the FK1 domain may act on specific client proline residues.”
Cryo-EM reveals the dynamic interplay between mitochondrial Hsp90 and SdhB folding intermediates
Liu, Y., Elnatan, D., Sun, M., Myasnikov, A. G., & Agard, D. A. (2020) · doi:10.1101/2020.10.06.327627 · Cited by 16 · see citing works
Self-citationThe Hsp90 Cochaperones Cpr6, Cpr7, and Cns1 Interact with the Intact Ribosome
Tenge, V. R., Zuehlke, A. D., Shrestha, N., & Johnson, J. L. (2014) · Eukaryotic Cell · doi:10.1128/ec.00170-14 · Cited by 16 · see citing works
“Hsc82 residues I588 and M589 are homologous to Hsp82 I592 and M593, which are located in a putative clientbinding site (53).”
BackgroundCharacterization of the Grp94/OS-9 Chaperone–Lectin Complex
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
“22 NMC (73-754) into cassette 1 and OS-9 full length (26-666) or MRH truncation (230-666) into cassette 4.”
InfluentialHidden information on protein function in censuses of proteome foldedness
Cox, D., Ang, C.-S., Nillegoda, N. B., Reid, G. E., & Hatters, D. M. (2022) · Nature Communications · doi:10.1038/s41467-022-29661-2 · Cited by 16 · see citing works
Serapian, S. A., Moroni, E., Ferraro, M., & Colombo, G. (2021) · ACS Catalysis · doi:10.1021/acscatal.1c00692 · Cited by 15 · see citing works
The prophage-encoded transcriptional regulator AppY has pleiotropic effects on E. coli physiology
Derdouri, N., Ginet, N., Denis, Y., Ansaldi, M., & Battesti, A. (2023) · PLoS Genetics · doi:10.1371/journal.pgen.1010672 · Cited by 15 · see citing works
“4:10000 dilution), or a Flag antibody (SIGMA—1:10000 dilution) for FlhC-SPA detection and with HtpG antibody [92] (1:100000 dilution) as a loading control.”
MethodHeat Shock Proteins: Potential Modulators and Candidate Biomarkers of Peripartum Cardiomyopathy
Chakafana, G., Spracklen, T. F., Kamuli, S., Zininga, T., Shonhai, A., Ntusi, N., & Sliwa, K. S. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.633013 · Cited by 14 · see citing works
“Additionally, Hsp70 also forms functional networks with Hsp40 (54), Hsp90 (55), and sHsps (56).”
BackgroundZuehlke, A., Wren, N. S., Tenge, V. R., & Johnson, J. L. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.504142 · Cited by 15 · see citing works
Corteggiani, M., Bossuet‐Greif, N., Nougayrède, J., Byrne, D., Ilbert, M., Dementin, S., Giudici‐Orticoni, M., Méjean, V., Oswald, É., & Genest, O. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2201779119 · Cited by 14 · see citing works
Self-citationATP plays a structural role in Hsp90 function
Reidy, M. J., & Masison, D. C. (2025) · Nature Communications · doi:10.1038/s41467-025-61962-0 · Cited by 12 · see citing works
Self-citationJin, J., Tian, R., Pasculescu, A., Dai, A. Y., Williton, K., Taylor, L., Savitski, M. M., Bantscheff, M., Woodgett, J. R., Pawson, T. J., et al. (2016) · Molecular and Cellular Biology · doi:10.1128/mcb.01045-15 · Cited by 12 · see citing works
“Despite intensive research using various model systems, the exact mechanism for how the HSP90 chaperone dynamically engages its kinase clients remains unclear (36, 37).”
BackgroundReidy, M. J., & Masison, D. C. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.06.015 · Cited by 12 · see citing works
“We deleted the HSC82 and HSP82 genes in strains W303 [26], BY4741 [27], and YPH499 [28], in a manner similar to our 779-6Aderived strain [29] (see Table 1 and Materials and Methods).”
ResultSelf-citationCracking the chaperone code through the computational microscope
Guarra, F., Sciva, C., Bonollo, G., Pasala, C., Chiosis, G., Moroni, E., & Colombo, G. (2024) · Cell Stress and Chaperones · doi:10.1016/j.cstres.2024.08.001 · Cited by 11 · see citing works
D’Annessa, I., Moroni, E., & Colombo, G. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.166728 · Cited by 11 · see citing works
Hohrman, K., Gonçalves, D. L., Morano, K. A., & Johnson, J. L. (2021) · Genetics · doi:10.1093/genetics/iyab009 · Cited by 11 · see citing works
Verkhivker, G. M. (2022) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.2c03464 · Cited by 11 · see citing works
Computational Modeling of the Hsp90 Interactions with Cochaperones and Small-Molecule Inhibitors
Verkhivker, G. M. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7477-1_19 · Cited by 10 · see citing works
The development of cancers research based on mitochondrial heat shock protein 90
Xiang, Y., Liu, X., Sun, Q., Liao, K., Liu, X., Zhao, Z., Feng, L., Liu, Y., & Wang, B. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1296456 · Cited by 10 · see citing works
Structural Communication between the E. coli Chaperones DnaK and Hsp90
Grindle, M. P., Carter, B., Alao, J. P., Connors, K., Tehver, R., & Kravats, A. N. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22042200 · Cited by 10 · see citing works
“These substrate binding residues were shown to be defective in ATPase activity and in protein remodeling assays with the DnaK chaperone system [71], which is supported by their importance in transmitting allosteric signals.”
BackgroundInfluentialGlobal transcriptomic response of Escherichia coli to p-coumaric acid
Rodríguez-Ochoa, J. I., Fragoso-Jiménez, J. C., Flores, N., Martínez, L. M., Bolívar, F. G., Martı́nez, A., & Gosset, G. (2022) · Microbial Cell Factories · doi:10.1186/s12934-022-01874-6 · Cited by 9 · see citing works
Wang, R. Y.-R., Noddings, C. M., Kirschke, E., Myasnikov, A. G., Johnson, J. L., & Agard, D. A. (2020) · doi:10.1101/2020.11.05.370247 · Cited by 10 · see citing works
“48 Genest, O., Hoskins, J. R., Kravats, A. N., Doyle, S. M. & Wickner, S. Hsp70 and Hsp90 of E. coli Directly Interact for Collaboration in Protein Remodeling. J Mol Biol 427, 3877-3889, doi:10.1016/j.jmb.2015.10.010 (2015). 49 Flynn, J.”
InfluentialSelf-citationHsp90, DnaK, and ClpB collaborate in protein reactivation
Hoskins, J. R., Wickramaratne, A. C., Jewell, C. P., Jenkins, L. M. M., & Wickner, S. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2422640122 · Cited by 6 · see citing works
Self-citationARSD is responsible for carcinoma and amyloidosis of breast epithelial cells
Lin, Y., Fan, L., Zhang, R., Pan, H., & Li, Y. (2022) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2022.151199 · Cited by 6 · see citing works
Saccharomyces cerevisiae as a tool for deciphering Hsp90 molecular chaperone function
Backe, S. J., Mollapour, M., & Woodford, M. R. (2023) · Essays in Biochemistry · doi:10.1042/ebc20220224 · Cited by 5 · see citing works
Verkhivker, G. M. (2014) · Israel Journal of Chemistry · doi:10.1002/ijch.201300143 · Cited by 4 · see citing works
Astl, L., Stetz, G., & Verkhivker, G. M. (2020) · Journal of Chemical Theory and Computation · doi:10.1021/acs.jctc.0c00503 · Cited by 4 · see citing works
- Authors
- Genest, O., Reidy, M., Street, T. O., Hoskins, J. R., Camberg, J. L., Agard, D. A., Masison, D. C., & Wickner, S.
- Affiliations
- National Institutes of Health (US)
- University of California, San Francisco (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Wickner, Sue
- ORCID
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2013-02
- Volume
- 49
- Issue
- 3
- Pages
- 464-473
- ISSN
- 1097-2765 (ISSN-L)
- PMC
- PMC3570620
- OpenAlex
- W2109982971
- Cited by
- 118
- References
- 47
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 5 · 2023: 7 · 2022: 10 · 2021: 10 · 2020: 12 · 2019: 8 · 2018: 13 · 2017: 13 · 2016: 5 · 2015: 10 · 2014: 12 · 2013: 7
- FWCI
- 3.73
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health
- National Cancer Institute (ZIABC008710)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Keywords
- HSP90, molecular chaperones, Hsp82, chaperone activity, evolutionary divergence, Escherichia coli, Saccharomyces cerevisiae, ATP-dependent chaperones
- MeSH terms
- Amino Acid Sequence, Amino Acids, Escherichia coli, Molecular Sequence Data, Mutation, Protein Binding, Saccharomyces cerevisiae, Structure-Activity Relationship, Protein Structure, Tertiary, HSP90 Heat-Shock Proteins, Saccharomyces cerevisiae Proteins, Escherichia coli Proteins, Mutant Proteins
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