Hsp110 Chaperones Control Client Fate Determination in the Hsp70–Hsp90 Chaperone System
Open accessAbstract
Heat shock protein 70 (Hsp70) plays a central role in protein homeostasis and quality control in conjunction with other chaperone machines, including Hsp90. The Hsp110 chaperone Sse1 promotes Hsp90 activity in yeast, and functions as a nucleotide exchange factor (NEF) for cytosolic Hsp70, but the precise roles Sse1 plays in client maturation through the Hsp70–Hsp90 chaperone system are not fully understood. We find that upon pharmacological inhibition of Hsp90, a model protein kinase, Ste11ΔN, is rapidly degraded, whereas heterologously expressed glucocorticoid receptor (GR) remains stable. Hsp70 binding and nucleotide exchange by Sse1 was required for GR maturation and signaling through endogenous Ste11, as well as to promote Ste11ΔN degradation. Overexpression of another functional NEF partially compensated for loss of Sse1, whereas the paralog Sse2 fully restored GR maturation and Ste11ΔN degradation. Sse1 was required for ubiquitinylation of Ste11ΔN upon Hsp90 inhibition, providing a mechanistic explanation for its role in substrate degradation. Sse1/2 copurified with Hsp70 and other proteins comprising the “early-stage” Hsp90 complex, and was absent from “late-stage” Hsp90 complexes characterized by the presence of Sba1/p23. These findings support a model in which Hsp110 chaperones contribute significantly to the decision made by Hsp70 to fold or degrade a client protein.
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The canonical NEF-binding sites on Hsp70NBD-IIB remain available in the loading complex, explaining how the NEF Bag-1 can accelerate GR maturation and how the NEF Hsp110 can participate in GR maturation.
“The canonical nucleotide exchange factor (NEF)-binding sites10,14 on Hsp70NBD-IIB remain available, explaining how the NEF Bag-1 can accelerate GR maturation30 (Supplementary Fig. 4a, b) and also how the NEF Hsp110 can be involved in GR maturation31 (Supplementary Fig. 4c, d).”
From Structure of Hsp90–Hsp70–Hop–GR reveals the Hsp90 client-loading mechanism (2022) · cites this paper as [31]
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BackgroundAll in the family: atypical Hsp70 chaperones are conserved modulators of Hsp70 activity
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“exclusively uses this transporter (Andreasson et al., 2004; Garrett, 2008).”
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“Slt2 is an Hsp90 client; thus the observed growth defect of sse1 cells at 39°C is a direct consequence of Sse1’s participation in Hsp90 chaperoning (Piper et al., 2006; Truman et al., 2007).”
BackgroundFarnesylation of Ydj1 Is Required for In Vivo Interaction with Hsp90 Client Proteins
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“Growth assays were carried out by replica pronging as described (Shaner et al., 2008).”
BackgroundMethodSelf-citationYdj1 Protects Nascent Protein Kinases from Degradation and Controls the Rate of Their Maturation
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“Identification of the Hsp70 activator Ydj1 as an important regulator of protein kinase stability when forward progress through the Hsp90 system is compromised suggests that Hsp70 is a major nexus of client fate evaluation and that other Hsp70-regulating partners may likewise influence this decision (Mandal et al., 200…”
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“exclusively uses this transporter (Andreasson et al., 2004; Garrett, 2008).”
MethodAkt shows variable sensitivity to an Hsp90 inhibitor depending on cell context
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“…from animal cells treated with the drug demonstrate that Hsp90 is still bound to protein kinase or steroid hormone receptor clients, along with Hop (Sti1) and Hsp70, but that cochaperones such as Cdc37 or p23 are dissociated (Smith et al., 1995; An et al., 2000; Theodoraki et al., 2007).”
BackgroundSelf-citationPiper, P. W., Truman, A. W., Millson, S. H., & Nuttall, J. M. (2006) · Biochemical Society Transactions · doi:10.1042/bst0340783 · Cited by 20 · cited 1× · see citing works
“Slt2 is an Hsp90 client; thus the observed growth defect of sse1 cells at 39°C is a direct consequence of Sse1’s participation in Hsp90 chaperoning (Piper et al., 2006; Truman et al., 2007).”
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Verghese, J., Abrams, J., Wang, Y., & Morano, K. A. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05018-11 · Cited by 575 · see citing works
“Sse1 is also strongly implicated in protein degradation and appears to be required for ubiquitination and the subsequent proteasomal degradation of Hsp70-bound substrates (181, 276).”
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“Numerous natural and synthetic Hsp90 inhibitors have been developed in recent years, some of which exhibit excellent antitumor activities and have entered clinical trials.([141,144,147,148]) Geldanamycin (GA), a benzoquinone ansamycin anti‐ biotic, is the first discovered Hsp90 inhibitor.”
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“Hsp90 function is regulated by a cohort of co-chaperones that modulate its ATPase cycle, enable client acquisition and selection, and provide a link to other chaperone systems as well as the ubiquitin-proteasome system [11-13].”
BackgroundStructure of Hsp90–Hsp70–Hop–GR reveals the Hsp90 client-loading mechanism
Wang, R. Y.-R., Noddings, C. M., Kirschke, E., Myasnikov, A. G., Johnson, J. L., & Agard, D. A. (2022) · Nature · doi:10.1038/s41586-021-04252-1 · Cited by 213 · see citing works
Fries, G. R., Gassen, N. C., & Rein, T. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18122614 · Cited by 167 · see citing works
“[63,64] HSPBP1 (Hsp70 binding protein 1) Nucleotide exchange factor of Hsp70.”
BackgroundQuality control and fate determination of Hsp90 client proteins
Theodoraki, M. A., & Caplan, A. J. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.08.006 · Cited by 108 · see citing works
“Sse1, the Hsp110 chaperone that acts as a nucleotide exchange factor for Hsp70 [32] is required for degradation of client protein kinases in cells treated with geldanamycin [33].”
Self-citationXu, X., Sarbeng, E. B., Vorvis, C., Kumar, D. P., Zhou, L., & Liu, Q. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.275057 · Cited by 105 · see citing works
Hsp70 Targets a Cytoplasmic Quality Control Substrate to the San1p Ubiquitin Ligase
Guerriero, C. J., Weiberth, K. F., & Brodsky, J. L. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.475905 · Cited by 87 · see citing works
Wang, Y., Gibney, P. A., West, J. D., & Morano, K. A. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-06-0447 · Cited by 69 · see citing works
“The proline analogue azetidine 2-carboxylic acid (AZC) is incorporated into nascent chains, in which it leads to misfolding and ubiquitination of newly synthesized proteins (Trotter et al., 2002; Mandal et al., 2010).”
BackgroundSelf-citationAbrams, J. L., Verghese, J., Gibney, P. A., & Morano, K. A. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.530014 · Cited by 63 · see citing works
“To test this hypothesis, we challenged cells with AZC, a proline analog that incorporates into nascent chains causing protein misfolding (41, 64, 65).”
BackgroundSelf-citationBracher, A., & Verghese, J. (2014) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-3-319-11731-7_1 · Cited by 62 · see citing works
Hsp70-mediated quality control: should I stay or should I go?
Kohler, V., & Andréasson, C. (2020) · Biological Chemistry · doi:10.1515/hsz-2020-0187 · Cited by 57 · see citing works
Kandasamy, G., & Andréasson, C. (2018) · Journal of Cell Science · doi:10.1242/jcs.210948 · Cited by 54 · see citing works
“Hsp110 (Sse1) has previously been proposed to be involved specifically at the ubiquitylation step of proteasomal degradation of misfolded proteins (Heck et al., 2010; Mandal et al., 2010).”
BackgroundA Bidirectional System for the Dynamic Small Molecule Control of Intracellular Fusion Proteins
Neklesa, T. K., Noblin, D. J., Kuzin, A., Lew, S., Seetharaman, J., Acton, T., Kornhaber, G. J., Xiao, R., Montelione, G. T., Tong, L., et al. (2013) · ACS Chemical Biology · doi:10.1021/cb400569k · Cited by 52 · see citing works
Saxena, A., Banasavadi‐Siddegowda, Y., Fan, Y., Bhattacharya, S., Roy, G., Giovannucci, D. R., Frizzell, R. A., & Wang, X. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.297580 · Cited by 51 · see citing works
“Yeast Hsp105 homologue Sse1 is an Hsp90 cochaperone (7) and plays an important role in the regulation of client protein maturation and degradation in the cytosol in an NEF-dependent manner (56).”
BackgroundZininga, T., Achilonu, I., Hoppe, H. C., Prinsloo, E., Dirr, H. W., & Shonhai, A. (2016) · Cell Stress and Chaperones · doi:10.1007/s12192-016-0678-4 · Cited by 50 · see citing works
“Nucleotide exchange indirectly determines the substrate dwell time on the Hsp70SBD thereby influencing substrate fate (Mandal et al. 2010) as the premature release of substrates from Hsp70 could result in their aggregation, leading to their degradation (Mayer and Bukau 2005).”
Kimura, A., Ogata, K., Altan, B., Yokobori, T., Ide, M., Mochiki, E., Toyomasu, Y., Kogure, N., Yanoma, T., Suzuki, M., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.7821 · Cited by 50 · see citing works
“HSP110ΔE9 lacks a substratebinding domain, and it is unable to play a role of a molecular chaperone for other HSPs (HSP70 or HSP27).”
InfluentialZininga, T., & Shonhai, A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20235930 · Cited by 41 · see citing works
“Nucleotide exchange function of Hsp70 defines substrate dwell time on the chaperone, and this in turn influences the fate of substrates, as those proteins that are not folded are channeled towards degradation [200].”
BackgroundWang, X., & Subjeck, J. R. (2013) · International Journal of Hyperthermia · doi:10.3109/02656736.2013.803607 · Cited by 47 · see citing works
“It is possible that these large HSPs serve dual roles as chaperones of their own and as co-chaperones or NEFs for Hsp70s to assist protein folding in a cooperative process [64].”
Co-Chaperones in Targeting and Delivery of Misfolded Proteins to the 26S Proteasome
Abildgaard, A. B., Gersing, S. K., Larsen-Ledet, S., Nielsen, S. V., Stein, A., Lindorff‐Larsen, K., & Hartmann‐Petersen, R. (2020) · Biomolecules · doi:10.3390/biom10081141 · Cited by 44 · see citing works
“To this end, ubiquitination of HSP70-bound substrates has been found to depend on Sse1, and upon inhibition of HSP90, Sse1 seems to stimulate degradation [234].”
BackgroundZininga, T., Achilonu, I., Hoppe, H., Prinsloo, E., Dirr, H., & Shonhai, A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129445 · Cited by 47 · see citing works
“Hsp110 and canonical Hsp70s both possess a highly conserved NBD and a less well conserved C-terminal SBD. Hsp110 differs from canonical Hsp70s as the former possess an extended lid segment [16].”
BackgroundInfluentialGarcía, V. M. G., Nillegoda, N. B., Bukau, B., & Morano, K. A. (2017) · Molecular Biology of the Cell · doi:10.1091/mbc.e17-01-0070 · Cited by 41 · see citing works
“However, overexpression of either Fes1 or a soluble, truncated mutant form of the normally endoplasmic reticulum-associated NEF Snl1, both of which lack demonstrated holdase activities, partially suppresses these phenotypes (Raviol et al., 2006; Mandal et al., 2010).”
BackgroundInfluentialSelf-citationFalse start: Cotranslational protein ubiquitination and cytosolic protein quality control
Comyn, S. A., Chan, G. T., & Mayor, T. (2013) · Journal of Proteomics · doi:10.1016/j.jprot.2013.08.005 · Cited by 40 · see citing works
“[31] Mandal AK, Gibney PA, Nillegoda NB, Theodoraki MA, Caplan AJ, Morano KA.”
BackgroundMechanisms and regulation of the Hsp70 chaperone network
Wentink, A. S., Rosenzweig, R., Kampinga, H. H., & Bukau, B. (2025) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-025-00890-9 · Cited by 39 · see citing works
“BAG-and Hsp110-type NEFs have both been implicated in this process 125,175 .”
The Endoplasmic Reticulum Chaperone GRP170: From Immunobiology to Cancer Therapeutics
Wang, H., Pezeshki, A. M., Yu, X., Guo, C., Subjeck, J. R., & Wang, X. (2015) · Frontiers in Oncology · doi:10.3389/fonc.2014.00377 · Cited by 39 · see citing works
“More studies are necessary to address the question as to why GRP170 in the ER possess the dual ability to bind to substrates or client proteins and to have NEF activity (54).”
BackgroundChaperone-assisted protein aggregate reactivation: Different solutions for the same problem
Aguado, A., Fernández-Higuero, J. Á., Moro, F., & Muga, A. (2015) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2015.07.006 · Cited by 31 · see citing works
Contribution of chaperones to STAT pathway signaling.
Bocchini, C., Kasembeli, M., Roh, S., & Tweardy, D. (2014) · JAK-STAT · doi:10.4161/21623988.2014.970459 · Cited by 30 · see citing works
Nagao, J.-I., Cho, T., Uno, J., Ueno, K., Imayoshi, R., Nakayama, H., Chibana, H., & Kaminishi, H. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2012.00822.x · Cited by 25 · see citing works
“Saccharomyces cerevisiae Sse1p functions as a nucleotide exchange factor (NEF) for Hsp70 chaperones during protein folding (Yam et al., 2005; Dragovic et al., 2006; Raviol et al., 2006) and as an NEF for Hsp70 in Hsp90 chaperone complexes to promote client protein maturation (Mandal et al., 2010).”
BackgroundInfluentialA first-in-class inhibitor of Hsp110 molecular chaperones of pathogenic fungi
Hu, L., Sun, C., Kidd, J. M., Han, J., Fang, X., Li, H., Liu, Q., May, A. E., Li, Q., Zhou, L., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38220-2 · Cited by 24 · see citing works
Gao, L., Yuan, Z., Yu, S., Yang, Y., Li, Y., & He, C. (2018) · Comparative Biochemistry and Physiology Part D Genomics and Proteomics · doi:10.1016/j.cbd.2018.07.005 · Cited by 22 · see citing works
Bracher, A., & Verghese, J. (2023) · Sub-cellular biochemistry · doi:10.1007/978-3-031-14740-1_1 · Cited by 21 · 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
Requirement of Hsp105 in CoCl 2 -induced HIF-1α accumulation and transcriptional activation
Mikami, H., Saito, Y., Okamoto, N., Kakihana, A., Kuga, T., & Nakayama, Y. (2017) · Experimental Cell Research · doi:10.1016/j.yexcr.2017.02.004 · Cited by 17 · see citing works
Mapping the degradation pathway of a disease-linked aspartoacylase variant
Gersing, S. K., Wang, Y., Grønbæk-Thygesen, M., Kampmeyer, C., Clausen, L., Willemoës, M., Andréasson, C., Stein, A., Lindorff‐Larsen, K., & Hartmann‐Petersen, R. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009539 · Cited by 16 · see citing works
The Role of Hsp70s in the Development and Pathogenicity of Plasmodium Species
Shonhai, A. (2013) · Springer eBooks · doi:10.1007/978-94-007-7438-4_3 · Cited by 17 · see citing works
Interdomain interactions dictate the function of the Candida albicans Hsp110 protein Msi3
Li, H., Hu, L., Cuffee, C. W., Mohamed, M., Li, Q., Liu, Q., Zhou, L., & Liu, Q. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.101082 · Cited by 16 · see citing works
Zuehlke, 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
Hsp70 clears misfolded kinases that partitioned into distinct quality-control compartments
Roy, J., Mitra, S., Sengupta, K., & Mandal, A. K. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-08-1262 · Cited by 12 · see citing works
“SSA1 promotes ubiquitylation of kinases for degradation via the proteasome We have seen that Hsp70 mediates degradation of Ste11ΔNK444R kinase by the proteasome when its folding is interrupted by the Hsp90 inhibitor GA (Mandal et al., 2010).”
BackgroundMethodInfluentialSelf-citationUntangling the complexity of heat shock protein 27 in cancer and metastasis
Rizvi, S. F., Hasan, A., Parveen, S., & Mir, S. S. (2023) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2023.109537 · Cited by 12 · see citing works
Wang, Y., Li, H., Sun, C., Liu, Q., Zhou, L., & Liu, Q. (2021) · Cell Stress and Chaperones · doi:10.1007/s12192-021-01213-5 · Cited by 12 · see citing works
Zhao, C., Wu, Y., Li, M., Tan, W., Hu, Y., Wang, Y., Gao, R., Hu, L., & Li, Q. (2024) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2024.116855 · Cited by 11 · see citing works
Tenge, V. R., Jared, K., & Johnson, J. L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092569 · Cited by 9 · see citing works
“This hypothesis is consistent with earlier reports that suggest that components of early, but not late, Hsp90 complexes participate in client degradation [15,29].”
BackgroundResultInfluentialHsp110 expression changes in rat primary myocardial cells exposed to heat stress in vitro
Liu, Z. J., Lv, Y., Zhang, M., Yue, Z. H., Tang, S., Islam, A., Rehana, B., Bao, E., & Hartung, J. (2012) · Genetics and Molecular Research · doi:10.4238/2012.november.29.1 · Cited by 9 · see citing works
“, 2008a,b) including the coupled effects of the nucleotides and interactions on the open-closed isomerization of the nucleotide binding domains (Mandal et al., 2010).”
BackgroundVCP controls KCC2 degradation through FAF1 recruitment and accelerates emergence from anesthesia
Chen, P., Hu, J.-J., Liu, Y., Cao, B., & Song, X. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2414016122 · Cited by 5 · see citing works
“HSP70 is crucial for effectively enlisting HSP110; it carries the substrate and then binds to HSP110 on the 19S particle to complete substrate transport ( 30 , 31 ).”
Bhattacharjee, P., Roy, J., & Mandal, A. K. (2025) · Journal of Biosciences · doi:10.1007/s12038-025-00506-6 · Cited by 7 · see citing works
“…the degradation of various substrates including the r 32 transcription factor in bacteria and protein kinases and cytosolic misfolded proteins in the yeast S. cerevisiae (Guisbert et al. 2004; Rodriguez et al. 2008; Mandal et al. 2010; Nillegoda et al. 2010; Gowda et al. 2013; Roy et al. 2015).”
Self-citationLi, M., Zhao, C., Xiang, H., Wang, Y., Gao, R., Cai, Q., Chen, Z., Chen, Z., Hu, L., & Li, Q. (2024) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2024.107888 · Cited by 5 · see citing works
Pradhan, A. K., Kandasamy, G., Chatterjee, U., Bharadwaj, A., Mathew, S. J., Dohmen, R. J., & Palanimurugan, R. (2021) · FEBS Letters · doi:10.1002/1873-3468.14147 · Cited by 5 · see citing works
Liu, S., Ou, Y., Li, Y., Sulaiman, K., Tao, M., Shawky, E. M., Tian, J., & Zhu, W. (2022) · Physiologia Plantarum · doi:10.1111/ppl.13667 · Cited by 5 · see citing works
Heat shock protein 110: A novel candidate for disease diagnosis and targeted therapy
Zhao, C., Xiang, H., Li, M., Gao, R., Zhang, Y., Li, Q., & Hu, L. (2024) · Drug Discovery Today · doi:10.1016/j.drudis.2024.104199 · Cited by 4 · see citing works
Co-evolutionary analysis implies auxiliary functions of HSP110 inPlasmodium falciparum
Bhartiya, D., Chandramouli, B., & Kumar, N. (2015) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.24842 · Cited by 4 · see citing works
Characterization of a New Hsp110 Inhibitor as a Potential Antifungal
Sun, C., Li, Y., Kidd, J. M., Han, J., Ding, L., May, A. E., Zhou, L., & Liu, Q. (2024) · Journal of Fungi · doi:10.3390/jof10110732 · Cited by 3 · see citing works
Farley, F. W., McCully, R. R., Maslo, P. B., Yu, L., Sheff, M. A., Sadeghi, H., & Elion, E. A. (2023) · PLoS ONE · doi:10.1371/journal.pone.0289339 · Cited by 3 · see citing works
Quality Control of Protein Folding in the Cytosol
McClellan, A. J. (2012) · Encyclopedia of Life Sciences · doi:10.1002/9780470015902.a0020886.pub2 · Cited by 3 · see citing works
“Recent studies also consistently reveal a role in cytosolic quality control for the Hsp70 cochaperone Sse1p, a yeast Hsp110 homologue which acts as a nucleotide-exchange factor for Hsp70 (McClellan et al., 2005a; Heck et al., 2010; Mandal et al., 2010; Prasad et al., 2010).”
BackgroundInfluentialBhattacharjee, P., & Mandal, A. K. (2025) · FEBS Letters · doi:10.1002/1873-3468.70174 · Cited by 2 · see citing works
“Previous studies show that Hsp90 inhibition promotes degradation of Ste11 D N K444R aided by Hsp70 and its nucleotide exchange factor Sse1 (Hsp110) [27].”
Self-citationGaur, D., Kumar, N., Ghosh, A., Singh, P. R., Kumar, P., Guleria, J., Kaur, S., Malik, N., Saha, S., Nyström, T., et al. (2022) · PLoS Genetics · doi:10.1371/journal.pgen.1010442 · Cited by 2 · see citing works
“Indeed, the mutant Hsp70s binds with relatively higher affinities with Ydj1, which in turn could affect their interaction with other co-chaperones such as Sse1 and Fes1, known to facilitate Hsp70 degradation activity [61,62].”
BackgroundChan, S. N., Prasad, R., & Matsudaira, P. T. (2020) · G3 Genes Genomes Genetics · doi:10.1534/g3.120.401186 · Cited by 2 · see citing works
Biochemical and biophysical characterization of Plasmodium falciparum glucose regulated protein 170
Muzenda, F. L., Stofberg, M. L., Mthembu, W., Strauss, E., & Zininga, T. (2025) · Scientific Reports · doi:10.1038/s41598-025-98317-0 · Cited by 1 · see citing works
“Thus, NEFs dictate substrate dwell time and ensure that adequately folding competent substrates are released, as those that are prematurely released will misfold and are channelled for degradation 22 .”
Cellular Strategies to Combat Protein Misfolding: Intricate Role of Hsp70 in Stress Management
Roy, J., & Mandal, A. K. (2015) · Current Chemical Biology · doi:10.2174/221279680803150420094608 · Cited by 1 · see citing works
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Atypical Domain Communication and Domain Functions of a Hsp110 ChaperonePreprint
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Characterisation of novel mutations within Heat Shock Protein 27 causing motor neuropathies
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Role of Hsp105 in CFTR biogenesis
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Exploration of small-molecule inhibitors targeting Hsp110 as novel therapeutics
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ROR2 Drives Right Ventricular Heart Failure Through Disruption of Proteostasis
Hartman, H., Uy, G., Uchida, K., Scarborough, E. A., Yang, Y., Barr, E. W., Williams, S., Santilli, R. T., Kavari, S. L., Brandimarto, J., et al. (2026) · Circulation · doi:10.1161/circulationaha.125.078798
- Authors
- Mandal, A. K., Gibney, P. A., Nillegoda, N. B., Theodoraki, M. A., Caplan, A. J., & Morano, K. A.
- Affiliations
- City College of New York (US)
- The University of Texas Health Science Center at Houston (US)
- Corresponding author
- Caplan, Avrom J.
- Morano, Kevin A.
- Venue
- Molecular Biology of the Cell
- Published
- 2010-05
- Volume
- 21
- Issue
- 9
- Pages
- 1439-1448
- ISSN
- 1059-1524 (ISSN-L)
- 1939-4586
- PMC
- PMC2861604
- OpenAlex
- W2044546088
- Cited by
- 66
- References
- 61
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 5 · 2023: 3 · 2022: 3 · 2021: 5 · 2020: 3 · 2019: 1 · 2018: 3 · 2017: 6 · 2016: 2 · 2015: 6 · 2014: 4 · 2013: 8 · 2012: 7
- FWCI
- 2.47
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular Biology of the Cell (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CUNY Academic Works (City University of New York) (submittedVersion)
- Digital Commons-TMC (Texas Medical Center) (submittedVersion)
- Funders
- Carnegie Corporation of New York
- University of Texas Health Science Center at Houston
- National Institutes of Health (RR-03060)
- National Cancer Institute (U54CA132378)
- National Institute of General Medical Sciences (GM 074696, R01GM070596, R01GM074696, R01GM70596)
- National Center for Research Resources (RR-03060, 5G12-RR03060, G12RR003060)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- SSE2, HSP70, HSP90, nucleotide exchange factor, ubiquitination, HSP90 inhibition, Saccharomyces cerevisiae
- MeSH terms
- Genetic Complementation Test, Mutation, Receptors, Glucocorticoid, Saccharomyces cerevisiae, Immunoblotting, Molecular Chaperones, HSP70 Heat-Shock Proteins, HSP90 Heat-Shock Proteins, Ubiquitin, Saccharomyces cerevisiae Proteins
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