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Mutation of essential Hsp90 co-chaperones SGT1 or CNS1 renders yeast hypersensitive to overexpression of other co-chaperones

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Abstract

The essential molecular chaperone Hsp90 functions with over ten co-chaperones in Saccharomyces cerevisiae, but the in vivo roles of many of these co-chaperones are poorly understood. Two of these co-chaperones, Cdc37 and Sgt1, target specific types of clients to Hsp90 for folding. Other co-chaperones have general roles in supporting Hsp90 function, but the degree of overlapping or competing functions is unclear. None of the chaperones, when overexpressed, were able to rescue the lethality of an SGT1 disruption strain. However, overexpression of SBA1, PPT1, AHA1 or HCH1 caused varying levels of growth defects in an sgt1-K360E strain. Negative effects of CPR6 overexpression were similarly observed in cells expressing the temperature-sensitive mutation cns1-G90D. In all cases, alterations within co-chaperones designed to disrupt Hsp90 interaction relieved the negative growth defects. Sgt1-K360E and Cns1-G90D were previously shown to exhibit reduced Hsp90 interaction. Our results indicate that overexpression of other co-chaperones further disrupts the essential functions of Cns1 and Sgt1. However, the specificity of the negative effects indicates that only a subset of co-chaperones competes with Sgt1 or Cns1 for binding to Hsp90. This provides new evidence that co-chaperones selectively compete for binding to subpopulations of cellular Hsp90 and suggest that changes in the relative levels of co-chaperones may have dramatic effects on Hsp90 function.

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References

  • Ali MM, Roe SM, Vaughan CK, Meyer P, Panaretou B, Piper PW, Prodromou C, Pearl LH (2006) Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440(7087):1013–1017

    Article  PubMed  CAS  Google Scholar 

  • Armstrong H, Wolmarans A, Mercier R, Mai B, LaPointe P (2012) The co-chaperone Hch1 regulates Hsp90 function differently than its homologue Aha1 and confers sensitivity to yeast to the Hsp90 inhibitor NVP-AUY922. PLoS One 7(11):e49322

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bansal PK, Abdulle R, Kitagawa K (2004) Sgt1 associates with Hsp90: an initial step of assembly of the core kinetochore complex. Mol Cell Biol 24(18):8069–8079

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bansal PK, Mishra A, High AA, Abdulle R, Kitagawa K (2009) Sgt1 dimerization is negatively regulated by protein kinase CK2-mediated phosphorylation at Ser361. J Biol Chem 284(28):18692–18698

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Boter M, Amigues B, Peart J, Breuer C, Kadota Y, Casais C, Moore G, Kleanthous C, Ochsenbein F, Shirasu K, Guerois R (2007) Structural and functional analysis of SGT1 reveals that its interaction with HSP90 is required for the accumulation of Rx, an R protein involved in plant immunity. Plant Cell 19(11):3791–3804

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Burke D, Dawson D, Stearns T (2000) Methods in yeast genetics: a cold spring harbor laboratory course manual. Cold Spring Harbor Laboratory Press, Plainview, NY

    Google Scholar 

  • Catlett MG, Kaplan KB (2006) Sgt1p is a unique co-chaperone that acts as a client-adaptor to link Hsp90 to Skp1p. J Biol Chem 281(44):33739–33748

    Article  PubMed  CAS  Google Scholar 

  • Crevel G, Bennett D, Cotterill S (2008) The human TPR protein TTC4 is a putative Hsp90 co-chaperone which interacts with CDC6 and shows alterations in transformed cells. PLoS One 3(3):e0001737

    Article  PubMed  Google Scholar 

  • Das AK, Cohen PW, Barford D (1998) The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein–protein interactions. EMBO J 17(5):1192–1199

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dolinski KJ, Cardenas ME, Heitman J (1998) CNS1 encodes an essential p60/Sti1 homolog in Saccharomyces cerevisiae that suppresses cyclophilin 40 mutations and interacts with Hsp90. Mol Cell Biol 18(12):7344–7352

    PubMed  CAS  PubMed Central  Google Scholar 

  • Duina AA, Chang HC, Marsh JA, Lindquist S, Gaber RF (1996) A cyclophilin function in Hsp90-dependent signal transduction. Science 274(5293):1713–1715

    Article  PubMed  CAS  Google Scholar 

  • Fang Y, Fliss AE, Rao J, Caplan AJ (1998) SBA1 encodes a yeast hsp90 cochaperone that is homologous to vertebrate p23 proteins. Mol Cell Biol 18(7):3727–3734

    PubMed  CAS  PubMed Central  Google Scholar 

  • Flom G, Weekes J, Johnson JL (2005) Novel interaction of the Hsp90 chaperone machine with Ssl2, an essential DNA helicase in Saccharomyces cerevisiae. Curr Genet 47(6):368–380

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Flom GA, Langner E, Johnson JL (2012) Identification of an Hsp90 mutation that selectively disrupts cAMP/PKA signaling in Saccharomyces cerevisiae. Curr Genet 58:149–163

    Article  PubMed  CAS  Google Scholar 

  • Forafonov F, Toogun OA, Grad I, Suslova E, Freeman BC, Picard D (2008) p23/Sba1p protects against Hsp90 inhibitors independently of its intrinsic chaperone activity. Mol Cell Biol 28(10):3446–3456

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gelperin DM, White MA, Wilkinson ML, Kon Y, Kung LA, Wise KJ, Lopez-Hoyo N, Jiang L, Piccirillo S, Yu H, Gerstein M, Dumont ME, Phizicky EM, Snyder M, Grayhack EJ (2005) Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev 19(23):2816–2826

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Genest O, Reidy M, Street TO, Hoskins JR, Camberg JL, Agard DA, Masison DC, Wickner S (2013) Uncovering a region of heat shock protein 90 important for client binding in E. coli and chaperone function in yeast. Mol Cell 49(3):464–473

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425(6959):737–741

    Article  PubMed  CAS  Google Scholar 

  • Harst A, Lin H, Obermann WM (2005) Aha1 competes with Hop, p50 and p23 for binding to the molecular chaperone Hsp90 and contributes to kinase and hormone receptor activation. Biochem J 387(Pt 3):789–796

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hessling M, Richter K, Buchner J (2009) Dissection of the ATP-induced conformational cycle of the molecular chaperone Hsp90. Nat Struct Mol Biol 16(3):287–293

    Article  PubMed  CAS  Google Scholar 

  • Horibe T, Kohno M, Haramoto M, Ohara K, Kawakami K (2011) Designed hybrid TPR peptide targeting Hsp90 as a novel anticancer agent. J Transl Med 9:8

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Johnson JL, Brown C (2009) Plasticity of the Hsp90 chaperone machine in divergent eukaryotic organisms. Cell Stress Chaperones 14(1):83–94

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Johnson JL, Halas A, Flom G (2007) Nucleotide-dependent interaction of Saccharomyces cerevisiae Hsp90 with the cochaperone proteins Sti1, Cpr6, and Sba1. Mol Cell Biol 27(2):768–776

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kadota Y, Amigues B, Ducassou L, Madaoui H, Ochsenbein F, Guerois R, Shirasu K (2008) Structural and functional analysis of SGT1-HSP90 core complex required for innate immunity in plants. EMBO Rep 9(12):1209–1215

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Koulov AV, Lapointe P, Lu B, Razvi A, Coppinger J, Dong MQ, Matteson J, Laister R, Arrowsmith C, Yates JR 3rd, Balch WE (2010) Biological and structural basis for Aha1 regulation of Hsp90 ATPase activity in maintaining proteostasis in the human disease cystic fibrosis. Mol Biol Cell 21(6):871–884

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lee P, Shabbir A, Cardozo C, Caplan AJ (2004) Sti1 and Cdc37 can stabilize Hsp90 in chaperone complexes with a protein kinase. Mol Biol Cell 15(4):1785–1792

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Li J, Richter K, Buchner J (2011) Mixed Hsp90-cochaperone complexes are important for the progression of the reaction cycle. Nat Struct Mol Biol 18(1):61–66

    Article  PubMed  Google Scholar 

  • Li J, Soroka J, Buchner J (2012) The Hsp90 chaperone machinery: conformational dynamics and regulation by co-chaperones. Biochim Biophys Acta 1823(3):624–635

    Article  PubMed  CAS  Google Scholar 

  • Li J, Richter K, Reinstein J, Buchner J (2013) Integration of the accelerator Aha1 in the Hsp90 co-chaperone cycle. Nat Struct Mol Biol 20(3):326–331

    Article  PubMed  Google Scholar 

  • Lin JY, Nagy PD (2013) Identification of novel host factors via conserved domain search: Cns1 cochaperone is a novel restriction factor of tombusvirus replication in yeast. J Virol 87(23):12600–12610

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lorenz OR, Freiburger L, Rutz DA, Krause M, Zierer BK, Alvira S, Cuellar J, Valpuesta JM, Madl T, Sattler M, Buchner J (2014) Modulation of the hsp90 chaperone cycle by a stringent client protein. Mol Cell 53(6):941–953

    Article  PubMed  CAS  Google Scholar 

  • Louvion JF, Warth R, Picard D (1996) Two eukaryote-specific regions of Hsp82 are dispensable for its viability and signal transduction functions in yeast. Proc Natl Acad Sci USA 93(24):13937–13942

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mandal AK, Lee P, Chen JA, Nillegoda N, Heller A, DiStasio S, Oen H, Victor J, Nair DM, Brodsky JL, Caplan AJ (2007) Cdc37 has distinct roles in protein kinase quality control that protect nascent chains from degradation and promote posttranslational maturation. J Cell Biol 176(3):319–328

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Marsh JA, Kalton HM, Gaber RF (1998) Cns1 is an essential protein associated with the hsp90 chaperone complex in Saccharomyces cerevisiae that can restore cyclophilin 40-dependent functions in cpr7Delta cells. Mol Cell Biol 18(12):7353–7359

    PubMed  CAS  PubMed Central  Google Scholar 

  • Mayor A, Martinon F, De Smedt T, Petrilli V, Tschopp J (2007) A crucial function of SGT1 and HSP90 in inflammasome activity links mammalian and plant innate immune responses. Nat Immunol 8(5):497–503

    Article  PubMed  CAS  Google Scholar 

  • Mayr C, Richter K, Lilie H, Buchner J (2000) Cpr6 and Cpr7, two closely related Hsp90-associated immunophilins from Saccharomyces cerevisiae, differ in their functional properties. J Biol Chem 275(44):34140–34146

    Article  PubMed  CAS  Google Scholar 

  • McDowell CL, Sutton RB, Obermann WM (2009) Expression of Hsp90 chaperome proteins in human tumor tissue. Int J Biol Macromol 45(3):310–314

    Article  PubMed  CAS  Google Scholar 

  • Meyer P, Prodromou C, Hu B, Vaughan C, Roe SM, Panaretou B, Piper PW, Pearl LH (2003) Structural and functional analysis of the middle segment of hsp90. Implications for ATP hydrolysis and client protein and cochaperone interactions. Mol Cell 11(3):647–658

    Article  PubMed  CAS  Google Scholar 

  • Meyer P, Prodromou C, Liao C, Hu B, Roe SM, Vaughan CK, Vlasic I, Panaretou B, Piper PW, Pearl LH (2004) Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery. EMBO J 23(3):511–519

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mollapour M, Neckers L (2012) Post-translational modifications of Hsp90 and their contributions to chaperone regulation. Biochim Biophys Acta 1823(3):648–655

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mollapour M, Bourboulia D, Beebe K, Woodford MR, Polier S, Hoang A, Chelluri R, Li Y, Guo A, Lee MJ, Fotooh-Abadi E, Khan S, Prince T, Miyajima N, Yoshida S, Tsutsumi S, Xu W, Panaretou B, Stetler-Stevenson WG, Bratslavsky G, Trepel JB, Prodromou C, Neckers L (2014) Asymmetric Hsp90 N domain SUMOylation recruits Aha1 and ATP-competitive inhibitors. Mol Cell 53(2):317–329

    Article  PubMed  CAS  Google Scholar 

  • Mumberg D, Muller R, Funk M (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156:119–122

    Article  PubMed  CAS  Google Scholar 

  • Neckers L, Mollapour M, Tsutsumi S (2009) The complex dance of the molecular chaperone Hsp90. Trends Biochem Sci 34(5):223–226

    Article  PubMed  CAS  Google Scholar 

  • Okayama S, Kopelovich L, Balmus G, Weiss RS, Herbert BS, Dannenberg AJ, Subbaramaiah K (2014) p53 regulates Hsp90 ATPase activity and thereby Wnt signaling by modulating Aha1 expression. J Biol Chem 289:6513–6525

    PubMed  CAS  Google Scholar 

  • Owens-Grillo JK, Stancato LF, Hoffmann K, Pratt WB, Krishna P (1996) Binding of immunophilins to the 90 kDa heat shock protein (hsp90) via a tetratricopeptide repeat domain is a conserved protein interaction in plants. Biochemistry 35(48):15249–15255

    Article  PubMed  CAS  Google Scholar 

  • Panaretou B, Siligardi G, Meyer P, Maloney A, Sullivan JK, Singh S, Millson SH, Clarke PA, Naaby-Hansen S, Stein R, Cramer R, Mollapour M, Workman P, Piper PW, Pearl LH, Prodromou C (2002) Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol Cell 10(6):1307–1318

    Article  PubMed  CAS  Google Scholar 

  • Patwardhan CA, Fauq A, Peterson LB, Miller C, Blagg BS, Chadli A (2013) Gedunin inactivates the co-chaperone p23 protein causing cancer cell death by apoptosis. J Biol Chem 288(10):7313–7325

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Picard D (2006) Intracellular dynamics of the Hsp90 co-chaperone p23 is dictated by Hsp90. Exp Cell Res 312(2):198–204

    Article  PubMed  CAS  Google Scholar 

  • Prodromou C (2012) The ‘active life’ of Hsp90 complexes. Biochim Biophys Acta 1823(3):614–623

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pullen L, Bolon DN (2011) Enforced N-domain proximity stimulates Hsp90 ATPase activity and is compatible with function in vivo. J Biol Chem 286(13):11091–11098

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Retzlaff M, Hagn F, Mitschke L, Hessling M, Gugel F, Kessler H, Richter K, Buchner J (2010) Asymmetric activation of the hsp90 dimer by its cochaperone aha1. Mol Cell 37(3):344–354

    Article  PubMed  CAS  Google Scholar 

  • Russell LC, Whitt SR, Chen MS, Chinkers M (1999) Identification of conserved residues required for the binding of a tetratricopeptide repeat domain to heat shock protein 90. J Biol Chem 274(29):20060–20063

    Article  PubMed  CAS  Google Scholar 

  • Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, Hartl FU, Moarefi I (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101(2):199–210

    Article  PubMed  CAS  Google Scholar 

  • Siligardi G, Hu B, Panaretou B, Piper PW, Pearl LH, Prodromou C (2004) Co-chaperone regulation of conformational switching in the Hsp90 ATPase cycle. J Biol Chem 279(50):51989–51998

    Article  PubMed  CAS  Google Scholar 

  • Smith DF (1993) Dynamics of heat shock protein 90- progesterone receptor binding and the disactivation loop model for steroid receptor complexes. Mol Endocrinol 7:1418–1429

    PubMed  CAS  Google Scholar 

  • Street TO, Lavery LA, Agard DA (2011) Substrate binding drives large-scale conformational changes in the Hsp90 molecular chaperone. Mol Cell 42(1):96–105

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Stuttmann J, Parker JE, Noel LD (2008) Staying in the fold: the SGT1/chaperone machinery in maintenance and evolution of leucine-rich repeat proteins. Plant Signal Behav 3(5):283–285

    Article  PubMed  PubMed Central  Google Scholar 

  • Taipale M, Krykbaeva I, Koeva M, Kayatekin C, Westover KD, Karras GI, Lindquist S (2012) Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 150(5):987–1001

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Taylor P, Dornan J, Carrello A, Minchin RF, Ratajczak T, Walkinshaw MD (2001) Two structures of cyclophilin 40: folding and fidelity in the TPR domains. Structure 9(5):431–438

    Article  PubMed  CAS  Google Scholar 

  • Tesic M, Marsh JA, Cullinan SB, Gaber RF (2003) Functional interactions between Hsp90 and the Co-chaperones Cns1 and Cpr7 in Saccharomyces cerevisiae. J Biol Chem 278(35):32692–32701

    Article  PubMed  CAS  Google Scholar 

  • Vaughan CK, Mollapour M, Smith JR, Truman A, Hu B, Good VM, Panaretou B, Neckers L, Clarke PA, Workman P, Piper PW, Prodromou C, Pearl LH (2008) Hsp90-dependent activation of protein kinases is regulated by chaperone-targeted dephosphorylation of Cdc37. Mol Cell 31(6):886–895

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wandinger SK, Suhre MH, Wegele H, Buchner J (2006) The phosphatase Ppt1 is a dedicated regulator of the molecular chaperone Hsp90. EMBO J 25(2):367–376

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ward BK, Allan RK, Mok D, Temple SE, Taylor P, Dornan J, Mark PJ, Shaw DJ, Kumar P, Walkinshaw MD, Ratajczak T (2002) A structure-based mutational analysis of cyclophilin 40 identifies key residues in the core tetratricopeptide repeat domain that mediate binding to Hsp90. J Biol Chem 277(43):40799–40809

    Article  PubMed  CAS  Google Scholar 

  • Wegele H, Muller L, Buchner J (2004) Hsp70 and Hsp90—a relay team for protein folding. Rev Physiol Biochem Pharmacol 151:1–44

    Article  PubMed  CAS  Google Scholar 

  • Whitesell L, Lindquist SL (2005) HSP90 and the chaperoning of cancer. Nat Rev Cancer 5(10):761–772

    Article  PubMed  CAS  Google Scholar 

  • Wu Z, Gholami AM, Kuster B (2012) Systematic identification of the HSP90 candidate regulated proteome. Mol Cell Proteomics 11(6):M111 016675

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu W, Mollapour M, Prodromou C, Wang S, Scroggins BT, Palchick Z, Beebe K, Siderius M, Lee MJ, Couvillon A, Trepel JB, Miyata Y, Matts R, Neckers L (2012) Dynamic tyrosine phosphorylation modulates cycling of the HSP90-P50(CDC37)-AHA1 chaperone machine. Mol Cell 47(3):434–443

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yang J, Roe SM, Cliff MJ, Williams MA, Ladbury JE, Cohen PT, Barford D (2005) Molecular basis for TPR domain-mediated regulation of protein phosphatase 5. EMBO J 24(1):1–10

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Boter M, Li K, Kadota Y, Panaretou B, Prodromou C, Shirasu K, Pearl LH (2008) Structural and functional coupling of Hsp90- and Sgt1-centred multi-protein complexes. EMBO J 27(20):2789–2798

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhao R, Davey M, Hsu YC, Kaplanek P, Tong A, Parsons AB, Krogan N, Cagney G, Mai D, Greenblatt J, Boone C, Emili A, Houry WA (2005) Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 120(5):715–727

    Article  PubMed  CAS  Google Scholar 

  • Zuehlke AD, Johnson JL (2012) Chaperoning the chaperone: a role for the co-chaperone Cpr7 in modulating Hsp90 function in Saccharomyces cerevisiae. Genetics 191:805–814

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zuehlke AD, Wren N, Tenge V, Johnson JL (2013) Interaction of heat shock protein 90 and the co-chaperone Cpr6 with Ura2, a bifunctional enzyme required for pyrimidine biosynthesis. J Biol Chem 288(38):27406–27414

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

The authors wish to thank Gary Flom, Nick Wren, Steven Heid and Sam Hatfield for construction of wild-type and mutant co-chaperone plasmids. They also thank Rick Gaber (Northwestern University) for reagents. This work was funded by a grant from the National Science Foundation MCB-0744522.

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  1. Abbey D. Zuehlke

    Present address: Urologic Oncology Branch, Center for Cancer Research, National Cancer Institute, 9000 Rockville Pike, Bethesda, MD, 20892, USA

Authors and Affiliations

  1. Department of Biological Sciences, University of Idaho, P.O. Box 443051, Moscow, ID, 83844-3051, USA

    Jill L. Johnson, Victoria R. Tenge & Jordan C. Langworthy

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  1. Jill L. Johnson
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  2. Abbey D. Zuehlke
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Correspondence to Jill L. Johnson.

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Johnson, J.L., Zuehlke, A.D., Tenge, V.R. et al. Mutation of essential Hsp90 co-chaperones SGT1 or CNS1 renders yeast hypersensitive to overexpression of other co-chaperones. Curr Genet 60, 265–276 (2014). https://doi.org/10.1007/s00294-014-0432-3

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