The DOI matches its Crossref record; 55 of the 56 references it cites were found in a registry or an index.
Diverse Cellular Functions of the Hsp90 Molecular Chaperone Uncovered Using Systems Approaches
Open accessAbstract
A comprehensive understanding of the cellular functions of the Hsp90 molecular chaperone has remained elusive. Although Hsp90 is essential, highly abundant under normal conditions, and further induced by environmental stress, only a limited number of Hsp90 "clients" have been identified. To define Hsp90 function, a panel of genome-wide chemical-genetic screens in Saccharomyces cerevisiae were combined with bioinformatic analyses. This approach identified several unanticipated functions of Hsp90 under normal conditions and in response to stress. Under normal growth conditions, Hsp90 plays a major role in various aspects of the secretory pathway and cellular transport; during environmental stress, Hsp90 is required for the cell cycle, meiosis, and cytokinesis. Importantly, biochemical and cell biological analyses validated several of these Hsp90-dependent functions, highlighting the potential of our integrated global approach to uncover chaperone functions in the cell.
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In the citing paper
“The fungal Hsp90 interactome, which includes numerous client proteins such as receptors, protein kinases and transcription factors, displays a surprisingly high degree of plasticity that depends on environmental conditions.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [92]
In the citing paper
“The fungal Hsp90 interactome, which includes numerous client proteins such as receptors, protein kinases and transcription factors, displays a surprisingly high degree of plasticity that depends on environmental conditions.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [92]
In the citing paper
“Several key cell cycle regulators have been identified as Hsp90 interactors in S. cerevisiae, including Swe1, Cdc28, Cdc50 and Cdc6061,92,123.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [92]
In the citing paper
“Hsp90 also has evolutionarily conserved roles in cell cycle progression.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [92]
In the citing paper
“Also, many features of the Hsp90 interactome are highly conserved from yeast to humans despite substantial network rewiring over evolutionary time.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [92]
In the citing paper
“These conserved features include a preponderance of protein kinases and transcription factors as client proteins67,78,91-93.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [92]
In the citing paper
“Hsp90's role in cell cycle progression appears to be conserved in the fungal kingdom. In the budding yeast Saccharomyces cerevisiae, Hsp90 is required for cell cycle progression during environmental stress, and in the fission yeast Schizosaccharomyces pombe Hsp90 interacts with cell cycle machinery (Aligue et al., 1994; Munoz and Jimenez, 1999; McClellan et al., 2007).”
From Cdc28 provides a molecular link between Hsp90, morphogenesis, and cell cycle progression in Candida albicans (2012) · cites this paper as McClellan et al., 2007
In the citing paper
“In S. cerevisiae, Cdc15 and Dbf2, two kinases in the MEN cascade, were identified in screens for Hsp90 interactors, and bub2 null mutants are hypersensitive to Hsp90 inhibitors, as are strains lacking the major MEN targets Sic1 and Cdh1 (Zhao et al., 2005; McClellan et al., 2007).”
From Cdc28 provides a molecular link between Hsp90, morphogenesis, and cell cycle progression in Candida albicans (2012) · cites this paper as McClellan et al., 2007
Citations
Cites
The Pfam Protein Families Database
Bateman, A. G. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.276 · Cited by 14,075
The Gene Ontology (GO) database and informatics resource
Gene Ontology Consortium (2003) · Nucleic Acids Research · doi:10.1093/nar/gkh036 · Cited by 4,596
Functional profiling of the Saccharomyces cerevisiae genome
Giaever, G., Chu, A. M., Ni, L., Connelly, C., Riles, L., Véronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., André, B., et al. (2002) · Nature · doi:10.1038/nature00935 · Cited by 4,316
Self-citationBioGRID: a general repository for interaction datasets
Stark, C. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkj109 · Cited by 3,960
Functional Characterization of the S. cerevisiae Genome by Gene Deletion and Parallel Analysis
Winzeler, E. A., Shoemaker, D. D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J. D., Bussey, H., et al. (1999) · Science · doi:10.1126/science.285.5429.901 · Cited by 3,953
Self-citationBrachmann, C. B., Davies, A., Cost, G. J., Caputo, E. M., Li, J., Hieter, P., & Boeke, J. D. (1998) · Yeast · doi:10.1002/(sici)1097-0061(19980130)14:2 · Cited by 3,418
The Pfam protein families database
Bateman, A. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh121 · Cited by 3,127
HSP90 and the chaperoning of cancer
Whitesell, L., & Lindquist, S. L. (2005) · Nature Reviews Cancer · doi:10.1038/nrc1716 · Cited by 2,502
Global Mapping of the Yeast Genetic Interaction Network
Tong, A. H. Y., Lesage, G., Bader, G. D., Ding, H., Xu, H., Xin, X., Young, J., Berriz, G. F., Brost, R. L., Chang, M., et al. (2004) · Science · doi:10.1126/science.1091317 · Cited by 2,089
Pratt, W. B., & Toft, D. O. (2003) · Experimental Biology and Medicine · doi:10.1177/153537020322800201 · Cited by 1,497
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Items 401–476 of 476
Aoki, S., Harada, K., Kawai, S., Abe, Y., Nagata, S., Imataki, R., & Arita, K. (2021) · Journal of Hard Tissue Biology · doi:10.2485/jhtb.30.13 · Cited by 2
Rocha, M. C., Santos, C. A., & Malavazi, I. (2018) · Current Proteomics · doi:10.2174/1570164615666180820155807 · Cited by 2
The Best for the Most Important: Maintaining a Pristine Proteome in Stem and Progenitor Cells
Aktas, B. H., Upcin, B., Henke, E., Padmasekar, M., Qin, X., & Ergün, S. (2019) · Stem Cells International · doi:10.1155/2019/1608787 · Cited by 2
Zinkevičiūtė, R., Bakūnaitė, E., Čiplys, E., Ražanskas, R., Raškevičiūtė, J., & Slibinskas, R. (2015) · New Biotechnology · doi:10.1016/j.nbt.2015.04.001 · Cited by 2
Khalili, V., Shokri, H., Khosravi, A., Akim, A. M., & Saroukolaei, S. A. (2016) · Journal de Mycologie Médicale · doi:10.1016/j.mycmed.2015.12.007 · Cited by 2
Role of Heat Shock Protein 90 in Autoimmune Inflammatory Rheumatic Diseases
Štorkánová, H., & Tomčík, M. (2019) · Heat shock proteins · doi:10.1007/978-3-030-02254-9_5 · Cited by 2
Hsp90 and Its Role in Heme-Maturation of Client Proteins: Implications for Human Diseases
Ghosh, A., & Stuehr, D. J. (2019) · Heat shock proteins · doi:10.1007/978-3-030-23158-3_12 · Cited by 2
Thermal Changes during Rheolytic Mechanical Thrombectomy
Hsu, M. C., Weber, C. N., Mohammed, M. A., Gade, T. P. F., Hunt, S. J., Nadolski, G., & Clark, T. W. I. (2016) · Journal of Vascular and Interventional Radiology · doi:10.1016/j.jvir.2016.02.008 · Cited by 1
The effect of microenvironment on Candida albicans morphological switch
Wu, C., Cui, Y., Yang, C., & Tang, J. (2014) · Reviews in Medical Microbiology · doi:10.1097/mrm.0000000000000015 · Cited by 1
Emergence and Characterization of the p23 Molecular Chaperone
Echtenkamp, F., & Freeman, B. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1130-1_9 · Cited by 1
Mackie, T. D. (2018) · D-Scholarship@Pitt (University of Pittsburgh) · Cited by 1
CORE at the boundary of stress resistance and longevity
Lippi, A., & Kriško, A. (2022) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2022.106277 · Cited by 1
The interplay between stress and nutrition during pregnancy: Influence on fetal brain development
Wankhede, N. L., Umare, M. D., Bajaj, K. K., Kale, M. B., Marde, V. S., Taksande, B. G., Umekar, M. J., & Upaganlawar, A. B. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-89834-8.00039-8 · Cited by 1
Allosteric CDC37 Inhibitor Disrupts Chaperone Complex to Block CDK4/6 Maturation
Zhang, L., Liu, W., Zheng, Z., Zhang, Q., He, Y., Gu, J., Wang, D., Shu, H., Yu, J., Liu, J., et al. (2024) · Angewandte Chemie · doi:10.1002/ange.202413618 · Cited by 1
James, K., Wipat, A., & Hallinan, J. S. (2012) · Integrative Biology · doi:10.1039/c2ib00123c · Cited by 1
Diezmann, S., & Cowen, L. E. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1130-1_8 · Cited by 1
Li, J., Sun, L.-H., Xu, C., Yu, F., Zhou, H., Tang, L., & He, J. (2012) · PROGRESS IN BIOCHEMISTRY AND BIOPHYSICS · doi:10.3724/sp.j.1206.2011.00611 · Cited by 2
The VHL short variant involves in protein quality control
Liu, Y., Yang, H., Zuo, F., & Chen, L. (2016) · Gene · doi:10.1016/j.gene.2016.05.027 · Cited by 1
Kim, M. K. (2017) · Korean Journal of Clinical Laboratory Science · doi:10.15324/kjcls.2017.49.4.460 · Cited by 1
Yusof, N. A., Wong, C., Murad, A. M. A., Bakar, F. D. A., Mahadi, N. M., Rahman, A. Y. A., Zainuddin, N., & Najimudin, M. N. M. (2019) · Polish Polar Research · doi:10.24425/ppr.2019.129674 · Cited by 1
Wang, Y. (2012) · Digital Commons-TMC (Texas Medical Center) · Cited by 1
Phosphorylation and proteome dynamics in pathogen-resistant tomato plants
Stulemeijer, I. J. E. (2008) · doi:10.18174/199874 · Cited by 1
Fernández‐Bautista, N. (2017) · doi:10.20868/upm.thesis.48105 · Cited by 1
The psychiatric referral in primary care practice.
Noori, S. S., Soldatos, C. R., & Kales, J. (1979) · PubMed · Cited by 1
Sharma, D. M., Singh, S., Verma, V., & Bairwa, N. K. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/664185 · Cited by 1
Ascertaining structural dynamics for a conformational plasticity in lncRNA-HSP90 interactionsPreprint
Thomas, L. X., Archa, P., Nair, B. G., Suravajhala, P., & Suravajhala, R. (2022) · Research Square · doi:10.21203/rs.3.rs-2043114/v1 · Cited by 1
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Yu, Y. (2011) · Deep Blue (University of Michigan) · Cited by 1
Biochemical analysis of proteins in the telomere maintenance pathway
DeZwaan, D. C. (2011) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
Liu, B., & Li, Z. (2014) · Springer eBooks · doi:10.1007/978-94-017-9421-3_12
Investigation of the role of putative chaperones in retinal degeneration
Novoselova, T. V. (2009) · UCL Discovery (University College London)
Salahuddin, P. (2015) · Journal of Biochemistry and Molecular Biology Research
A Hsp90 és az adipogenezis kapcsolatának vizsgálata
Nguyễn, M. T. (2014) · Semmelweis University Repository (Semmelweis University) · doi:10.14753/se.2014.1971
Pouland, T. (2016) · D-Scholarship@Pitt (University of Pittsburgh)
Integrins in Tumorigenesis and Cancer Cell Invasion
Högnäs, G. (2013) · UTUPub (University of Turku)
Sun, N. (2013) · DigitalGeorgetown (Georgetown University Library)
Schwock, J. (2010) · TSpace (University of Toronto)
Stress management : multilayer regulation of the heat shock response
Budzyński, M. A. (2017) · Doria (University of Helsinki) · doi:10.13140/rg.2.2.16736.48641
Mapping Genetic Interaction Networks in Yeast
Baryshnikova, A. (2013) · TSpace (University of Toronto)
The Roles of Hsp90 and Calcineurin in Antifungal Drug Resistance
Singh, S. (2012) · TSpace (University of Toronto)
Re-evaluating the conformation equilibrium of Grp94 Molecular Chaperone
Sun, M. (2016) · Brandeis Institutional Repository
Tan, S. (2017) · DR-NTU (Nanyang Technological University) · doi:10.32657/10356/72655
Armstrong, H. (2013) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r3tc7r
Translocation and function of Akt in the mitochondria
Mans, K. A. (2010)
Hogan, D. (2017) · University of New Hampshire Scholars Repository (University of New Hampshire at Manchester)
Murillo, A. (2017) · oURspace (University of Regina) · doi:10.82465/4774
The adaptive potential of the middle domain of yeast Hsp90Preprint
Cote-Hammarlof, P. A., Fragata, I., Flynn, J. M., Mavor, D., Zeldovich, K. B., Bank, C., & Bolon, D. N. A. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/832022
Complex structure of human Hsp90N and a novel small inhibitor FS5
Liu, R., Lu, X.-L., Huang, X., He, W., Duan, J., Zhang, J., & Li, J. (2020) · Nuclear Science and Techniques · doi:10.1007/s41365-020-0739-3
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Duron, D. I. (2020) · UA Campus Repository (The University of Arizona)
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Yuan, Z., Wang, L. Z., hong, S., Li, L., Tang, T., shi, C., & Yuan, B. (2021) · Research Square · doi:10.21203/rs.3.rs-181774/v1
On chaperone co-operation in temporal and spatial protein quality control
Andersson, R. (2021) · Gothenburg University Publications Electronic Archive (Gothenburg University)
Mercier, R. J. (2019) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r3-tms0-be49
Proteostasis beyond chaperones - Auxiliary systems in the management of damaged proteins
Josefson, R. (2021) · Gothenburg University Publications Electronic Archive (Gothenburg University)
Como implicar a los bancos en la proteccion de los intereses del exportador
Osorio, F. P. (2000) · El Exportador
Environmental systems biology of temperature adaptation in yeast
Paget, C. M. (2013) · Research Explorer (The University of Manchester)
Welch, M. D. (2008) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1131951.589060
Le, N.-T., Hoang, N. M., Fujiwara, K., & Abe, J. (2017) · Springer eBooks · doi:10.1007/978-3-319-67199-4_617
Le, N.-T., Hoang, N. M., Fujiwara, K., & Abe, J. (2016) · Springer eBooks · doi:10.1007/978-1-4614-6438-9_617-1
Diagnostic value of HSP90α and Related Markers in Lung CancerPreprint
Yuan, Z., Hong, S., Li, L., He, L., Xiao, P., Tang, T. F., Shi, C., Mu, Y., Sun, C., Shang, Y., et al. (2019) · Research Square · doi:10.21203/rs.2.10011/v1
Diagnostic value of HSP90α and Related Markers in Lung CancerPreprint
Yuan, Z., Hong, S., Li, L., He, L., Xiao, P., Tang, T. F., Shi, C., Mu, Y., Sun, C., Shang, Y., et al. (2019) · Research Square · doi:10.21203/rs.2.10011/v4
Mollapour, M. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.737482045.793572272
Diagnostic value of HSP90α and Related Markers in Lung CancerPreprint
Yuan, Z., Hong, S., Li, L., He, L., Xiao, P., Tang, T. F., Shi, C., Mu, Y., Sun, C., Shang, Y., et al. (2019) · Research Square · doi:10.21203/rs.2.10011/v3
Diagnostic value of HSP90α and Related Markers in Lung CancerPreprint
Yuan, Z., Hong, S., Li, L., He, L., Xiao, P., Tang, T. F., Shi, C., Mu, Y., Sun, C., Shang, Y., et al. (2019) · Research Square · doi:10.21203/rs.2.10011/v2
Selection Of Theaflavin 2B As a Potential HSP90 Antagonist Semi-rigid Ligand Docking AnalysisPreprint
Akinsehinwa, S., & Medayedupin, O. A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.24.497557
Mochizuki, K., Takimoto, Y., Nakagawa, T., & Gessei, T. (2025) · Plasmonics · doi:10.1007/s11468-025-03301-z
Molecular chaperones mediated proteostasis depletion: A cause of neurodegeneration?
Kinger, S., Choudhary, A., Kumar, P., Jagtap, Y. A., Sharma, V., Dhiman, R., Prasad, A., Verma, R., Chinnathambi, S., & Mishra, A. (2025) · Advances in protein chemistry and structural biology · doi:10.1016/bs.apcsb.2025.10.033
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Zhang, T. (2011) · Deep Blue (University of Michigan)
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Horwich, A. L., Büchner, J., Smock, R. G., Gierasch, L. M., & Saibil, H. R. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-374920-8.00313-1
Rios, E. I., & Johnson, J. L. (2026) · Cell Stress and Chaperones · doi:10.1016/j.cstres.2026.100164
Bracher, A. (2009) · MPG.PuRe (Max Planck Society)
Geer, M. A. (2015) · DukeSpace (Duke University)
Metadata
- Authors
- McClellan, A. J., Xia, Y., Deutschbauer, A. M., Davis, R. W., Gerstein, M., & Frydman, J.
- Affiliations
- Stanford University (US)
- Yale University (US)
- Corresponding author
- Frydman, Judith
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2007-10
- Volume
- 131
- Issue
- 1
- Pages
- 121-135
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2132919995
- Cited by
- 474
- References
- 56
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 21 · 2023: 9 · 2022: 20 · 2021: 26 · 2020: 32 · 2019: 33 · 2018: 27 · 2017: 33 · 2016: 23 · 2015: 29 · 2014: 32 · 2013: 31 · 2012: 41
- FWCI
- 9.66
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2116 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Jane Coffin Childs Memorial Fund for Medical Research
- National Institutes of Health
- National Institute of General Medical Sciences (GM 56433, F32GM064992, GM64992, P50GM062413)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Keywords
- HSP90, molecular chaperones, Saccharomyces cerevisiae, secretory pathway, cell transport, environmental stress response, cell cycle, meiosis, cytokinesis, chaperone activity
- MeSH terms
- Biological Transport, Cell Cycle, Saccharomyces cerevisiae, Reproducibility of Results, Genome, Fungal, Gene Deletion, HSP90 Heat-Shock Proteins, Computational Biology, Oligonucleotide Array Sequence Analysis, Secretory Vesicles, Saccharomyces cerevisiae Proteins, Gene Regulatory Networks
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