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Structure, Function, and Regulation of the Hsp90 Machinery

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Biebl, Maximilian M., Buchner, Johannes·2019·Cold Spring Harbor Perspectives in Biology

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Abstract

Heat shock protein 90 (Hsp90) is a molecular chaperone involved in the maturation of a plethora of substrates ("clients"), including protein kinases, transcription factors, and E3 ubiquitin ligases, positioning Hsp90 as a central regulator of cellular proteostasis. Hsp90 undergoes large conformational changes during its ATPase cycle. The processing of clients by cytosolic Hsp90 is assisted by a cohort of cochaperones that affect client recruitment, Hsp90 ATPase function or conformational rearrangements in Hsp90. Because of the importance of Hsp90 in regulating central cellular pathways, strategies for the pharmacological inhibition of the Hsp90 machinery in diseases such as cancer and neurodegeneration are being developed. In this review, we summarize recent structural and mechanistic progress in defining the function of organelle-specific and cytosolic Hsp90, including the impact of individual cochaperones on the maturation of specific clients and complexes with clients as well as ways of exploiting Hsp90 as a drug target.

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The epichaperome is an integrated chaperome network that facilitates tumour survival
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Molecular chaperone TRAP1 regulates a metabolic switch between mitochondrial respiration and aerobic glycolysis
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Systematic analysis of complex genetic interactions
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“Interestingly, although the PPIase activity of FKBPs seems irrelevant for GR activation, the differences between FKBP51 and FKBP52 seem to be largely defined by the structure of the PPIase domain (Riggs et al. 2007; Storer et al. 2011).”
Background
Identification of a Protein with Homology to hsp90 That Binds the Type 1 Tumor Necrosis Factor Receptor
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p50cdc37 Acting in Concert with Hsp90 Is Required for Raf-1 Function
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Human heat shock factors 1 and 2 are differentially activated and can synergistically induce hsp70 gene transcription.
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The large conformational changes of Hsp90 are only weakly coupled to ATP hydrolysis
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Chaperone Regulation of the Heat Shock Protein Response
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An Interaction Network Predicted from Public Data as a Discovery Tool: Application to the Hsp90 Molecular Chaperone Machine
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Heat shock protein 90 in neurodegenerative diseases
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Asymmetric Activation of the Hsp90 Dimer by Its Cochaperone Aha1
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Stimulation of the weak ATPase activity of human Hsp90 by a client protein 1 1Edited by G. von Heijne
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Nucleotides and Two Functional States of hsp90
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Overexpression of the FK506-Binding Immunophilin FKBP51 Is the Common Cause of Glucocorticoid Resistance in Three New World Primates
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Molecular basis for TPR domain‐mediated regulation of protein phosphatase 5
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Polypeptide release by Hsp90 involves ATP hydrolysis and is enhanced by the co-chaperone p23
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The architecture of functional modules in the Hsp90 co‐chaperone Sti1/Hop
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Akt and CHIP coregulate tau degradation through coordinated interactions
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Ligand Discrimination by TPR Domains
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Species-Dependent Ensembles of Conserved Conformational States Define the Hsp90 Chaperone ATPase Cycle
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HSP90 inhibitors: current development and potential in cancer therapy
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“Notably, derivatives of RD and GA have been explored in phase II and phase III clinical trials, but they were discontinued owing to lack of efficacy at the tolerated doses (Sidera and Patsavoudi 2014; Khandelwal et al. 2016).”
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Constitutive binding of yeast heat shock factor to DNA in vivo.
Jakobsen, B. K., & Pelham, H. R. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.11.5040 · Cited by 222
Hsp90 Recognizes a Common Surface on Client Kinases
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Multiplexed Proteome Dynamics Profiling Reveals Mechanisms Controlling Protein Homeostasis
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In Vivo Analysis of the Hsp90 Cochaperone Sti1 (p60)
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Co-chaperone regulation of conformational switching in the Hsp90 ATPase cycle
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The Physical Association of Multiple Molecular Chaperone Proteins with Mutant p53 Is Altered by Geldanamycin, an hsp90-Binding Agent
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Hsp90-Dependent Activation of Protein Kinases Is Regulated by Chaperone-Targeted Dephosphorylation of Cdc37
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The Co-chaperone p23 Arrests the Hsp90 ATPase Cycle to Trap Client Proteins
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“The general model of the Hsp90 ATPase cycle is applicable to all Hsp90 paralogs and isoforms.”
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Isolation of Hsp90 mutants by screening for decreased steroid receptor function.
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Development of a Purine-Scaffold Novel Class of Hsp90 Binders that Inhibit the Proliferation of Cancer Cells and Induce the Degradation of Her2 Tyrosine Kinase
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Sti1 Is a Non-competitive Inhibitor of the Hsp90 ATPase
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Differential interactions of p23 and the TPR-containing proteins Hop, Cyp40, FKBP52 and FKBP51 with Hsp90 mutants
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Heat Shock Protein 75 (TRAP1) Antagonizes Reactive Oxygen Species Generation and Protects Cells from Granzyme M-mediated Apoptosis
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Folding of Toll-like receptors by the HSP90 paralogue gp96 requires a substrate-specific cochaperone
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TRAP-1, the mitochondrial Hsp90
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Polypeptide components of two 8 S forms of chicken oviduct progesterone receptor.
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Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation
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Functional analysis of the hsp90-associated human peptidyl prolyl Cis/Trans isomerases FKBP51, FKBP52 and cyp40 1 1Edited by R. Huber
Pirkl, F., & Buchner, J. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4595 · Cited by 179 · cited 2×
“In conjunction with an environmental trigger, these factors can contribute to the onset of affective mood diseases and have further pleiotropic effects because FKBP51 competes with other cochaperones for Hsp90 binding (Pirkl and Buchner 2001; Schulke et al. 2010).”
Background
Ancient heat shock gene is dispensable
Bardwell, J. C., & Craig, E. A. (1988) · Journal of Bacteriology · doi:10.1128/jb.170.7.2977-2983.1988 · Cited by 179
Brain-Permeable Small-Molecule Inhibitors of Hsp90 Prevent α-Synuclein Oligomer Formation and Rescue α-Synuclein-Induced Toxicity
Putcha, P., Danzer, K. M., Kranich, L. R., Scott, A., Silinski, M., Mabbett, S., Hicks, C. D., Veal, J. M., Steed, P. M., Hyman, B. T., et al. (2010) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.109.158436 · Cited by 179
Cyclophilin 40 (CyP-40), Mapping of Its hsp90 Binding Domain and Evidence That FKBP52 Competes with CyP-40 for hsp90 Binding
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Hsp90: Breaking the Symmetry
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Defining the Essential Function of Yeast Hsf1 Reveals a Compact Transcriptional Program for Maintaining Eukaryotic Proteostasis
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The R2TP complex: Discovery and functions
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Biological and Structural Basis for Aha1 Regulation of Hsp90 ATPase Activity in Maintaining Proteostasis in the Human Disease Cystic Fibrosis
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Tumor necrosis factor-associated protein 1 (TRAP-1) protects cells from oxidative stress and apoptosis
Gesualdi, N. M., Chirico, G., Pirozzi, G., Costantino, E., Landriscina, M., & Esposito, F. (2007) · Stress · doi:10.1080/10253890701314863 · Cited by 171
Hsp90 is regulated by a switch point in the C‐terminal domain
Retzlaff, M., Stahl, M., Eberl, H. C., Lagleder, S., Beck, J., Kessler, H., & Buchner, J. (2009) · EMBO reports · doi:10.1038/embor.2009.153 · Cited by 171
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Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery
Meyer, P., Prodromou, C., Liao, C., Hu, B., Mark Roe, S., Vaughan, C. K., Vlasic, I., Panaretou, B., Piper, P. W., & Pearl, L. H. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600060 · Cited by 166
Threonine 22 Phosphorylation Attenuates Hsp90 Interaction with Cochaperones and Affects Its Chaperone Activity
Mollapour, M., Tsutsumi, S., Truman, A. W., Xu, W., Vaughan, C. K., Beebe, K., Konstantinova, A., Vourganti, S., Panaretou, B., Piper, P. W., et al. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.02.011 · Cited by 165
GRP94 Is Essential for Mesoderm Induction and Muscle Development Because It Regulates Insulin-like Growth Factor Secretion
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Substrate Transfer from the Chaperone Hsp70 to Hsp90
Wegele, H., Wandinger, S. K., Schmid, A. B., Reinstein, J., & Buchner, J. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.12.008 · Cited by 162
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The Charged Linker Region Is an Important Regulator of Hsp90 Function
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Interaction of Radicicol with Members of the Heat Shock Protein 90 Family of Molecular Chaperones
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Structural Asymmetry in the Closed State of Mitochondrial Hsp90 (TRAP1) Supports a Two-Step ATP Hydrolysis Mechanism
Lavery, L. A., Partridge, J. R., Ramelot, T. A., Elnatan, D., Kennedy, M. A., & Agard, D. A. (2014) · Molecular Cell · doi:10.1016/j.molcel.2013.12.023 · Cited by 160
The phosphatase Ppt1 is a dedicated regulator of the molecular chaperone Hsp90
Wandinger, S. K., Suhre, M. H., Wegele, H., & Büchner, J. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7600930 · Cited by 160
HSP induction mediates selective clearance of tau phosphorylated at proline-directed Ser/Thr sites but not KXGS (MARK) sites
Dickey, C. A., Dunmore, J., Lu, B., Wang, J., Lee, W. C., Kamal, A., Burrows, F., Eckman, C., Hutton, M., & Petrucelli, L. (2006) · The FASEB Journal · doi:10.1096/fj.05-5343fje · Cited by 160
The Co-chaperone Sba1 connects the ATPase reaction of Hsp90 to the progression of the chaperone cycle
Richter, K., Walter, S., & Buchner, J. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.07.064 · Cited by 159 · cited 5×
“Notably, ATP is bound to the Hsp90:p23 complex, suggesting a noncompetitive mechanism of inhibition (Sullivan et al. 1997; Richter et al. 2004; Ali et al. 2006).”
BackgroundInfluential
Tumor Selectivity of Hsp90 Inhibitors: The Explanation Remains Elusive
Chiosis, G., & Neckers, L. (2006) · ACS Chemical Biology · doi:10.1021/cb600224w · Cited by 158
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 157
Mixed Hsp90–cochaperone complexes are important for the progression of the reaction cycle
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Hsp90 Chaperones Wild-type p53 Tumor Suppressor Protein
Walerych, D., Kudla, G., Gutkowska, M., Wawrzynów, B., Muller, L., King, F. W., Helwak, A., Boros, J., Żylicz, M., & Żylicz, M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407601200 · Cited by 155
Hsp90 and FKBP51: complex regulators of psychiatric diseases
Criado‐Marrero, M., Rein, T., Binder, E. B., Porter, J. T., Koren, J., & Blair, L. J. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0532 · Cited by 155
HSP90 inhibitors disrupt a transient HSP90-HSF1 interaction and identify a noncanonical model of HSP90-mediated HSF1 regulation
Kijima, T., Prince, T. L., Tigue, M. L., Yim, K. H., Schwartz, H., Beebe, K. E., Lee, S., Budzyński, M. A., Williams, H., Trepel, J. B., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-25404-w · Cited by 154
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 · cited 13×
“The binding site is in agreement with previous mutational studies and overlaps with the Aha1-binding site suggesting competitive binding (Lorenz et al. 2014).”
BackgroundMethodResultInfluential
Genetic variation in FKBP5 associated with the extent of stress hormone dysregulation in major depression
Menke, A., Klengel, T., Rubel, J., Brückl, T., Pfister, H., Lucae, S., Uhr, M., Holsboer, F., & Binder, E. B. (2013) · Genes, Brain and Behavior · doi:10.1111/gbb.12026 · Cited by 151 · cited 1×
“In agreement with this notion, the FKBP51-encoding gene has been associated with anxiety, depression, and schizophrenia (Menke et al. 2013; Fujii et al. 2014; Szczepankiewicz et al. 2014; Stamm et al. 2016).”
Background
Modeling Signal Propagation Mechanisms and Ligand-Based Conformational Dynamics of the Hsp90 Molecular Chaperone Full-Length Dimer
Morra, G., Verkhivker, G. M., & Colombo, G. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000323 · Cited by 151
Gedunin Inactivates the Co-chaperone p23 Protein Causing Cancer Cell Death by Apoptosis
Patwardhan, C. A., Fauq, A. H., Peterson, L. B., Miller, C. A., Blagg, B. S. J., & Chadli, A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.427328 · Cited by 151
Noncatalytic Role of the FKBP52 Peptidyl-Prolyl Isomerase Domain in the Regulation of Steroid Hormone Signaling
Riggs, D. L., Cox, M. B., Tardif, H. L., Hessling, M., Buchner, J., & Smith, D. F. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00985-07 · Cited by 150 · cited 2×
“Strikingly, although the PPIase domain seems to be important for the function of PPIases, the enzymatic function seems to be dispensable for Hsp90-mediated client maturation (Riggs et al. 2003, 2007).”
Background
Anticancer Inhibitors of Hsp90 Function
Garg, G., Khandelwal, A., & Blagg, B. S. J. (2016) · Advances in cancer research · doi:10.1016/bs.acr.2015.12.001 · Cited by 150
Roles of Heat Shock Protein gp96 in the ER Quality Control: Redundant or Unique Function?
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Molecular chaperone involvement in chloroplast protein import
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ATP-competitive inhibitors block protein kinase recruitment to the Hsp90-Cdc37 system
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The Chaperone TRAP1 As a Modulator of the Mitochondrial Adaptations in Cancer Cells
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Involvement of Tumor Necrosis Factor Receptor-associated Protein 1 (TRAP1) in Apoptosis Induced by β-Hydroxyisovalerylshikonin
Masuda, Y., Shima, G., Aiuchi, T., Horie, M., Hori, K., Nakajo, S., Kajimoto, S., Shibayama‐Imazu, T., & Nakaya, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404256200 · Cited by 142
Silencing the cochaperone CDC37 destabilizes kinase clients and sensitizes cancer cells to HSP90 inhibitors
Smith, J. R., Clarke, P. A., de Billy, E., & Workman, P. (2008) · Oncogene · doi:10.1038/onc.2008.380 · Cited by 140
Spatially and kinetically resolved changes in the conformational dynamics of the Hsp90 chaperone machine
Graf, C., Stankiewicz, M., Krämer, G., & Mayer, M. P. (2009) · The EMBO Journal · doi:10.1038/emboj.2008.306 · Cited by 140
Conformational Switching of the Molecular Chaperone Hsp90 via Regulated Phosphorylation
Soroka, J., Wandinger, S. K., Mäusbacher, N., Schreiber, T., Richter, K., Daub, H., & Buchner, J. (2012) · Molecular Cell · doi:10.1016/j.molcel.2011.12.031 · Cited by 139 · cited 2×
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BackgroundInfluential
Dephosphorylation of Tau by Protein Phosphatase 5
Liu, F., Iqbal, K., Grundke, I., Rossie, S. S., & Gong, C. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m410775200 · Cited by 139
(−)-Epigallocatechin-3-gallate Is a Novel Hsp90 Inhibitor
Yin, Z., Henry, E. C., & Gasiewicz, T. A. (2008) · Biochemistry · doi:10.1021/bi801637q · Cited by 138
The Molecular Chaperone Hsp90 Modulates Intermediate Steps of Amyloid Assembly of the Parkinson-related Protein α-Synuclein
Falsone, S. F., Kungl, A. J., Rek, A., Cappai, R., & Zangger, K. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.057240 · Cited by 137
Hsp90 Chaperone Inhibitor 17-AAG Attenuates Aβ-Induced Synaptic Toxicity and Memory Impairment
Chen, Y., Wang, B., Liu, D., Li, J. J., Xue, Y.-Q., Sakata, K., Zhu, L., Heldt, S. A., Xu, H., & Liao, F. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0151-13.2014 · Cited by 137
The Plasticity of the Hsp90 Co-chaperone System
Sahasrabudhe, P., Rohrberg, J., Biebl, M. M., Rutz, D. A., & Buchner, J. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.08.004 · Cited by 136 · cited 8×
“Consistent with this idea, the deletion of Sti1 in yeast is not lethal (Chang et al. 1997) and some Hsp90 clients do not show Sti1 dependence for their activity (Sahasrabudhe et al. 2017).”
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Crystal Structure and Activity of Human p23, a Heat Shock Protein 90 Co-chaperone
Weaver, A. J., Sullivan, W. P., Felts, S. J., Owen, B. A. L., & Toft, D. O. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m003410200 · Cited by 136
Silencing of HSP90 Cochaperone AHA1 Expression Decreases Client Protein Activation and Increases Cellular Sensitivity to the HSP90 Inhibitor 17-Allylamino-17-Demethoxygeldanamycin
Holmes, J. L., Sharp, S. Y., Hobbs, S., & Workman, P. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-3268 · Cited by 135
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 132
Structural and functional coupling of Hsp90‐ and Sgt1‐centred multi‐protein complexes
Zhang, M., Botër, M., Li, K., Kadota, Y., Panaretou, B., Prodromou, C., Shirasu, K., & Pearl, L. H. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.190 · Cited by 131
Sgt1p Is a Unique Co-chaperone That Acts as a Client Adaptor to Link Hsp90 to Skp1p
Catlett, M. G., & Kaplan, K. B. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m603847200 · Cited by 131
Functional Specificity of Co-Chaperone Interactions with Hsp90 Client Proteins
Riggs, D. L., Cox, M. B., Cheung‐Flynn, J., Prapapanich, V., Carrigan, P. E., & Smith, D. F. (2004) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409230490892513 · Cited by 131
Defining the Essential Function of Yeast Hsf1 Reveals a Compact Transcriptional Program for Maintaining Eukaryotic Proteostasis
Solís, E. J., Pandey, J. P., Zheng, X., Jin, D. X., Gupta, P. B., Airoldi, E. M., Pincus, D., & Denic, V. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.01.021 · Cited by 131
Endoplasmic reticulum HSP90b1 (gp96, grp94) optimizes B-cell function via chaperoning integrin and TLR but not immunoglobulin
Liu, B., & Li, Z. (2008) · Blood · doi:10.1182/blood-2008-03-143107 · Cited by 129
Hsp90 Inhibits α-Synuclein Aggregation by Interacting with Soluble Oligomers
Daturpalli, S., Waudby, C. A., Meehan, S., & Jackson, S. (2013) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.08.006 · Cited by 129
Hsp90 activator Aha1 drives production of pathological tau aggregates
Shelton, L. B., Baker, J. D., Zheng, D., Sullivan, L. E., Solanki, P. K., Webster, J. M., Sun, Z., Sabbagh, J. J., Nordhues, B. A., Koren, J., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707039114 · Cited by 129
The client protein p53 adopts a molten globule–like state in the presence of Hsp90
Park, S. J., Borin, B. N., Martinez-Yamout, M. A., & Dyson, H. J. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2045 · Cited by 128
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×
“The solvent-exposed W300 residue in yeast Hsp82, which is located at the rim of the client-binding site, has previously been shown to affect the maturation of different Hsp90 clients (Hawle et al. 2006; Flom et al. 2012).”
Background
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
Structural Studies on the Co-chaperone Hop and Its Complexes with Hsp90
Onuoha, S. C., Coulstock, E. T., Grossmann, J. G., & Jackson, S. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.02.013 · Cited by 127
HDAC6 regulates androgen receptor hypersensitivity and nuclear localization via modulating Hsp90 acetylation in castration-resistant prostate cancer.
Ai, J., Wang, Y., Dar, J. A., Liu, J., Liu, L., Nelson, J. B., & Wang, Z. (2009) · Molecular Endocrinology · doi:10.1210/me.2009-0188 · Cited by 126 · cited 1×
“Generally, acetylation and nitrosylation are considered to weaken the interaction of Hsp90 with clients, favoring their destabilization and degradation (Scroggins et al. 2007; Ai et al. 2009; Retzlaff et al. 2009; Zhang et al. 2010).”
Background
Charged linker sequence modulates eukaryotic heat shock protein 90 (Hsp90) chaperone activity
Tsutsumi, S., Mollapour, M., Prodromou, C., Lee, C., Panaretou, B., Yoshida, S., Mayer, M. P., & Neckers, L. Μ. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114414109 · Cited by 126
Heat shock protein 90: its inhibition and function
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See all 304

Authors: Biebl, M. M., & Buchner, J.
Venue: Cold Spring Harbor Perspectives in Biology
Publisher: Cold Spring Harbor Laboratory
Published: 2019-02-11
Volume: 11
Issue: 9
Pages: a034017
ISSN: 1943-0264 (ISSN-L)
DOI: 10.1101/cshperspect.a034017
OpenAlex: W2913172834
Cited by: 304
References: 322
Type: posted content
Language: en
Open access: bronze

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Structure, Function, and Regulation of the Hsp90 Machinery

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