The Role of p23, Hop, Immunophilins, and Other Co-chaperones in Regulating Hsp90 Function

Methods in Molecular Biology

Volumn 787, Issue , 2011, Pages 45-66

  Cox, Marc B ^a   Johnson, Jill L ^b  

^a UNIVERSITY OF TEXAS AT EL PASO   (United States)

^b UNIVERSITY OF IDAHO   (United States)

Author keywords

Co chaperone; Hsp90; Immunophilin; p23; Protein folding

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 90; HOMEODOMAIN PROTEIN; HOP PROTEIN, MOUSE; IMMUNOPHILIN; ISOMERASE; PROSTAGLANDIN E SYNTHASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ANIMAL; ARTICLE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOUSE; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

ANIMALS; HOMEODOMAIN PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOPHILINS; INTRAMOLECULAR OXIDOREDUCTASES; MICE; MOLECULAR CHAPERONES; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EID: 80054756986     PISSN: 10643745     EISSN: 19406029     Source Type: Book Series    
DOI: 10.1007/978-1-61779-295-3_4     Document Type: Chapter

References (133)

1. Mayer MP, Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 2005;62:670–84.
2. Pearl LH, Prodromou C. Structure and mechanism of the hsp90 molecular chaperone machinery. Annu Rev Biochem 2006;75:271–94.
3. Wandinger SK, Richter K, Buchner J. The Hsp90 chaperone machinery. J Biol Chem 2008;283:18473–7.
4. Pratt WB, Toft DO. Regulation of signaling protein function and trafficking by the hsp90/ hsp70-based chaperone machinery. Exp Biol Med (Maywood) 2003;228:111–33.
5. Zhao R, Davey M, Hsu YC, et al. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 2005;120:715–27.
6. McClellan AJ, Xia Y, Deutschbauer AM, Davis RW, Gerstein M, Frydman J. Diverse cellular functions of the hsp90 molecular chaperone uncovered using systems approaches. Cell 2007;131:121–35.
7. Pearl LH, Prodromou C, Workman P. The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem J 2008;410:439–53.
8. Neckers L, Mollapour M, Tsutsumi S. The complex dance of the molecular chaperone Hsp90. Trends Biochem Sci 2009;34:223–6.
9. Southworth DR, Agard DA. Species-dependent ensembles of conserved conformational states define the Hsp90 chaperone ATPase cycle. Mol Cell 2008;32:631–40.
10. Vaughan CK, Gohlke U, Sobott F, et al. Structure of an Hsp90-Cdc37-Cdk4 complex. Mol Cell 2006;23:697–707.
11. Riggs D, Cox M, Cheung-Flynn J, Prapapanich V, Carrigan P, Smith D. Functional specificity of co-chaperone interactions with Hsp90 client proteins. Crit Rev Biochem Mol Biol 2004;39:279–95.
12. Harst A, Lin H, Obermann WM. Aha1 competes with Hop, p50 and p23 for binding to the molecular chaperone Hsp90 and contributes to kinase and hormone receptor activation. Biochem J 2005;387:789–96.
13. Siligardi G, Hu B, Panaretou B, Piper PW, Pearl LH, Prodromou C. Co-chaperone regulation of conformational switching in the Hsp90 ATPase cycle. J Biol Chem 2004;279: 51989–98.
14. McLaughlin SH, Sobott F, Yao ZP, et al. The co-chaperone p23 arrests the Hsp90 ATPase cycle to trap client proteins. J Mol Biol 2006;356:746–58.
15. Young JC, Hartl FU. Polypeptide release by Hsp90 involves ATP hydrolysis and is enhanced by the co-chaperone p23. Embo J 2000;19: 5930–40.
16. Richter K, Walter S, Buchner J. The Co-chaperone Sba1 connects the ATPase reaction of Hsp90 to the progression of the chaperone cycle. J Mol Biol 2004;342:1403–13.
17. Ali MM, Roe SM, Vaughan CK, et al. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 2006;440: 1013–7.
18. Cox MB, Miller CA, 3rd. Cooperation of heat shock protein 90 and p23 in aryl hydrocarbon receptor signaling. Cell Stress Chaperones 2004;9:4–20.
19. Weikl T, Abelmann K, Buchner J. An unstructured C-terminal region of the Hsp90 cochaperone p23 is important for its chaperone function. J Mol Biol 1999;293:685–91.
20. Freeman BC, Toft DO, Morimoto RI. Molecular chaperone machines: chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science 1996;274:1718–20.
21. Taguwa S, Kambara H, Omori H, et al. Co-chaperone activity of human butyrate-induced transcript 1 facilitates hepatitis C virus replication through an Hsp90-dependent pathway. J Virol 2009.
22. Fang Y, Fliss AE, Rao J, Caplan AJ. SBA1 encodes a yeast hsp90 cochaperone that is homologous to vertebrate p23 proteins. Mol Cell Biol 1998;18:3727–34.
23. Grad I, McKee TA, Ludwig SM, et al. The Hsp90 cochaperone p23 is essential for perinatal survival. Mol Cell Biol 2006;26:8976–83.
24. Catlett MG, Kaplan KB. Sgt1p is a unique cochaperone that acts as a client-adaptor to link Hsp90 to Skp1p. J Biol Chem 2006; 281:33739–48.
25. Zhang M, Boter M, Li K, et al. Structural and functional coupling of Hsp90-and Sgt1-centred multi-protein complexes. Embo J 2008;27:2789–98.
26. Kadota Y, Amigues B, Ducassou L, et al. Structural and functional analysis of SGT1-HSP90 core complex required for innate immunity in plants. EMBO Rep 2008;9:1209–15.
27. Picard D. A stress protein interface of innate immunity. EMBO Rep 2008;9:1193–5.
28. Caplan AJ, Mandal AK, Theodoraki MA. Molecular chaperones and protein kinase quality control. Trends Cell Biol 2007;17: 87–92.
29. Mandal AK, Lee P, Chen JA, et al. Cdc37 has distinct roles in protein kinase quality control that protect nascent chains from degradation and promote posttranslational maturation. J Cell Biol 2007;176:319–28.
30. Chadli A, Graham JD, Abel MG, et al. GCUNC-45 is a novel regulator for the progesterone receptor/hsp90 chaperoning pathway. Mol Cell Biol 2006;26:1722–30.
31. Hessling M, Richter K, Buchner J. Dissection of the ATP-induced conformational cycle of the molecular chaperone Hsp90. Nat Struct Mol Biol 2009;16:287–93.
32. Wang X, Venable J, LaPointe P, et al. Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 2006;127:803–15.
33. Scheufler C, Brinker A, Bourenkov G, et al. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 2000; 101:199–210.
34. Chen S, Smith DF. Hop as an adaptor in the heat shock protein 70 (Hsp70) and hsp90 chaperone machinery. J Biol Chem 1998;273: 35194–200.
35. Wegele H, Haslbeck M, Reinstein J, Buchner J. Sti1 is a novel activator of the Ssa proteins. J Biol Chem 2003;278:25970–6.
36. Flom G, Behal RH, Rosen L, Cole DG, Johnson JL. Definition of the minimal fragments of Sti1 required for dimerization, interaction with Hsp70 and Hsp90 and in vivo functions. Biochem J 2007;404:159–67.
37. Carrigan PE, Riggs DL, Chinkers M, Smith DF. Functional comparison of human and Drosophila Hop reveals novel role in steroid receptor maturation. J Biol Chem 2005;280: 8906–11.
38. Chang HC, Nathan DF, Lindquist S. In vivo analysis of the Hsp90 cochaperone Sti1 (p60). Mol Cell Biol 1997;17:318–25.
39. Barik S. Immunophilins: for the love of proteins. Cell Mol Life Sci 2006;63:2889–900.
40. Bose S, Weikl T, Bugl H, Buchner J. Chaperone function of Hsp90-associated proteins. Science 1996;274:1715–7.
41. Prodromou C, Siligardi G, O’Brien R, et al. Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. Embo J 1999;18:754–62.
42. Mayr C, Richter K, Lilie H, Buchner J. Cpr6 and Cpr7, two closely related Hsp90-associated immunophilins from Saccharomyces cerevisiae, differ in their functional properties. J Biol Chem 2000;275:34140–6.
43. Duina AA, Chang HC, Marsh JA, Lindquist S, Gaber RF. A cyclophilin function in Hsp90-dependent signal transduction. Science 1996;274:1713–5.
44. Duina AA, Marsh JA, Kurtz RB, Chang HC, Lindquist S, Gaber RF. The peptidyl-prolyl isomerase domain of the CyP-40 cyclophilin homolog Cpr7 is not required to support growth or glucocorticoid receptor activity in Saccharomyces cerevisiae. J Biol Chem 1998;273:10819–22.
45. Mok D, Allan RK, Carrello A, Wangoo K, Walkinshaw MD, Ratajczak T. The chaperone function of cyclophilin 40 maps to a cleft between the prolyl isomerase and tetratricopeptide repeat domains. FEBS Lett 2006;580:2761–8.
46. Riggs DL, Cox MB, Tardif HL, Hessling M, Buchner J, Smith DF. Noncatalytic role of the FKBP52 peptidyl-prolyl isomerase domain in the regulation of steroid hormone signaling. Mol Cell Biol 2007;27:8658–69.
47. Smith DF, Toft DO. The Intersection of Steroid Receptors with Molecular Chaperones: Observations and Questions. Mol Endocrinol 2008;22:2229–40.
48. Hidalgo-de-Quintana J, Evans RJ, Cheetham ME, van der Spuy J. The Leber congenital amaurosis protein AIPL1 functions as part of a chaperone heterocomplex. Invest Ophthalmol Vis Sci 2008;49:2878–87.
49. Hinds TD, Jr., Sanchez ER. Protein phosphatase 5. Int J Biochem Cell Biol 2007.
50. Wandinger SK, Suhre MH, Wegele H, Buchner J. The phosphatase Ppt1 is a dedicated regulator of the molecular chaperone Hsp90. Embo J 2006;25:367–76.
51. Vaughan CK, Mollapour M, Smith JR, et al. Hsp90-dependent activation of protein kinases is regulated by chaperone-targeted dephosphorylation of Cdc37. Mol Cell 2008;31: 886–95.
52. Millson SH, Vaughan CK, Zhai C, et al. Chaperone ligand-discrimination by the TPR-domain protein Tah1. Biochem J 2008;413: 261–8.
53. Boulon S, Marmier-Gourrier N, Pradet-Balade B, et al. The Hsp90 chaperone controls the bio-genesis of L7Ae RNPs through conserved machinery. J Cell Biol 2008;180:579–95.
54. Tesic M, Marsh JA, Cullinan SB, Gaber RF. Functional interactions between Hsp90 and the Co-chaperones Cns1 and Cpr7 in saccharomyces cerevisiae. J Biol Chem 2003;278: 32692–701.
55. Hainzl O, Wegele H, Richter K, Buchner J. Cns1 is an activator of the Ssa1 ATPase activity. J Biol Chem 2004;279:23267–73.
56. Crevel G, Bennett D, Cotterill S. The Human TPR Protein TTC4 Is a Putative Hsp90 Co-Chaperone Which Interacts with CDC6 and Shows Alterations in Transformed Cells. PLoS ONE 2008;3:e0001737.
57. Young JC, Hoogenraad NJ, Hartl FU. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 2003;112:41–50.
58. Dickey CA, Kamal A, Lundgren K, et al. The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins. J Clin Invest 2007;117: 648–58.
59. Brychzy A, Rein T, Winklhofer KF, Hartl FU, Young JC, Obermann WM. Cofactor Tpr2 combines two TPR domains and a J domain to regulate the Hsp70/Hsp90 chaperone system. EMBO J 2003;22:3613–23.
60. Moffatt NS, Bruinsma E, Uhl C, Obermann WM, Toft D. Role of the cochaperone Tpr2 in Hsp90 chaperoning. Biochemistry 2008;47: 8203–13.
61. Cziepluch C, Kordes E, Poirey R, Grewenig A, Rommelaere J, Jauniaux JC. Identification of a novel cellular TPR-containing protein, SGT, that interacts with the nonstructural protein NS1 of parvovirus H-1. J Virol 1998;72: 4149–56.
62. Callahan MA, Handley MA, Lee YH, Talbot KJ, Harper JW, Panganiban AT. Functional interaction of human immunodeficiency virus type 1 Vpu and Gag with a novel member of the tetratricopeptide repeat protein family. J Virol 1998;72:5189–97.
63. Dutta S, Tan YJ. Structural and functional characterization of human SGT and its interaction with Vpu of the human immunodeficiency virus type 1. Biochemistry 2008;47:10123–31.
64. Angeletti PC, Walker D, Panganiban AT. Small glutamine-rich protein/viral protein U-binding protein is a novel cochaperone that affects heat shock protein 70 activity. Cell Stress Chaperones 2002;7:258–68.
65. Fielding BC, Gunalan V, Tan TH, et al. Severe acute respiratory syndrome coronavirus protein 7a interacts with hSGT. Biochem Biophys Res Commun 2006;343:1201–8.
66. Fonte V, Kapulkin V, Taft A, Fluet A, Friedman D, Link CD. Interaction of intracellular beta amyloid peptide with chaperone proteins. Proc Natl Acad Sci USA 2002;99:9439–44.
67. Liou ST, Wang C. Small glutamine-rich tetratricopeptide repeat-containing protein is composed of three structural units with distinct functions. Arch Biochem Biophys 2005;435:253–63.
68. Natochin M, Campbell TN, Barren B, et al. Characterization of the G alpha(s) regulator cysteine string protein. J Biol Chem 2005;280: 30236–41.
69. Schantl JA, Roza M, De Jong AP, Strous GJ. Small glutamine-rich tetratricopeptide repeat-containing protein (SGT) interacts with the ubiquitin-dependent endocytosis (UbE) motif of the growth hormone receptor. Biochem J 2003;373:855–63.
70. Wang H, Shen H, Wang Y, et al. Overexpression of small glutamine-rich TPR-containing protein promotes apoptosis in 7721 cells. FEBS Lett 2005;579:1279–84.
71. Wang H, Zhang Q, Zhu D. hSGT interacts with the N-terminal region of myostatin. Biochem Biophys Res Commun 2003;311: 877–83.
72. Winnefeld M, Rommelaere J, Cziepluch C. The human small glutamine-rich TPR-containing protein is required for progress through cell division. Exp Cell Res 2004;293: 43–57.
73. Yin H, Wang H, Zong H, et al. SGT, a Hsp90beta binding partner, is accumulated in the nucleus during cell apoptosis. Biochem Biophys Res Commun 2006;343:1153–8.
74. Buchanan G, Ricciardelli C, Harris JM, et al. Control of androgen receptor signaling in prostate cancer by the cochaperone small glutamine rich tetratricopeptide repeat containing protein alpha. Cancer Res 2007;67:10087–96.
75. Wu SJ, Liu FH, Hu SM, Wang C. Different combinations of the heat-shock cognate protein 70 (hsc70) C-terminal functional groups are utilized to interact with distinct tetratricopeptide repeat-containing proteins. Biochem J 2001;359:419–26.
76. Kordes E, Savelyeva L, Schwab M, Rommelaere J, Jauniaux JC, Cziepluch C. Isolation and characterization of human SGT and identification of homologues in Saccharomyces cerevisiae and Caenorhabditis elegans. Genomics 1998;52:90–4.
77. de Groot PW, Ruiz C, Vazquez de Aldana CR, et al. A genomic approach for the identification and classification of genes involved in cell wall formation and its regulation in Saccharomyces cerevisiae. Comp Funct Genomics 2001;2:124–42.
78. Niu W, Li Z, Zhan W, Iyer VR, Marcotte EM. Mechanisms of cell cycle control revealed by a systematic and quantitative overexpression screen in S. cerevisiae. PLoS Genet 2008;4: e1000120.
79. Liou ST, Cheng MY, Wang C. SGT2 and MDY2 interact with molecular chaperone YDJ1 in Saccharomyces cerevisiae. Cell Stress Chaperones 2007;12:59–70.
80. Kimura Y, Yahara I, Lindquist S. Role of the protein chaperone YDJ1 in establishing Hsp90-mediated signal transduction pathways. Science 1995;268:1362–5.
81. Cyr DM. Swapping nucleotides, tuning Hsp70. Cell 2008;133:945–7.
82. Liu XD, Morano KA, Thiele DJ. The yeast Hsp110 family member, Sse1, is an Hsp90 cochaperone. J Biol Chem 1999;274:26654–60.
83. Hohfeld J, Minami Y, Hartl FU. Hip, a novel cochaperone involved in the eukaryotic Hsc70/Hsp40 reaction cycle. Cell 1995;83: 589–98.
84. Prapapanich V, Chen S, Toran EJ, Rimerman RA, Smith DF. Mutational analysis of the hsp70-interacting protein Hip. Mol Cell Biol 1996;16:6200–7.
85. Kosano H, Stensgard B, Charlesworth MC, McMahon N, Toft D. The assembly of progesterone receptor-hsp90 complexes using purified proteins. J Biol Chem 1998;273:32973–9.
86. Arlander SJ, Felts SJ, Wagner JM, Stensgard B, Toft DO, Karnitz LM. Chaperoning checkpoint kinase 1 (Chk1), an Hsp90 client, with purified chaperones. J Biol Chem 2006;281: 2989–98.
87. Chang HC, Lindquist S. Conservation of Hsp90 macromolecular complexes in Saccharomyces cerevisiae. J Biol Chem 1994; 269:24983–8.
88. Johnson JL, Craig EA. A role for the Hsp40 Ydj1 in repression of basal steroid receptor activity in yeast. Mol Cell Biol 2000;20:3027–36.
89. Mandal AK, Nillegoda N, Chen JA, Caplan AJ. Ydj1 protects nascent protein kinases from degradation and controls the rate of their maturation. Mol Cell Biol 2008;28:4434–44.
90. Hon T, Lee HC, Hach A, et al. The Hsp70-Ydj1 molecular chaperone represses the activity of the heme activator protein Hap1 in the absence of heme. Mol Cell Biol 2001; 21:7923–32.
91. Sahi C, Craig EA. Network of general and specialty J protein chaperones of the yeast cytosol. Proc Natl Acad Sci USA 2007;104:7163–8.
92. Dittmar KD, Banach M, Galigniana MD, Pratt WB. The role of DnaJ-like proteins in glucocorticoid receptor.hsp90 heterocomplex assembly by the reconstituted hsp90.p60. hsp70 foldosome complex. J Biol Chem 1998;273:7358–66.
93. Hernandez MP, Chadli A, Toft DO. HSP40 binding is the first step in the HSP90 chaperoning pathway for the progesterone receptor. J Biol Chem 2002;277:11873–81.
94. Murphy PJ, Morishima Y, Chen H, et al. Visualization and mechanism of assembly of a glucocorticoid receptor.Hsp70 complex that is primed for subsequent Hsp90-dependent opening of the steroid binding cleft. J Biol Chem 2003;278:34764–73.
95. Flom GA, Lemieszek M, Fortunato EA, Johnson JL. Farnesylation of Ydj1 is required for in vivo interaction with Hsp90 client proteins. Mol Biol Cell 2008;19:5249–58.
96. Smith DF. Dynamics of heat shock protein 90-progesterone receptor binding and the disactivation loop model for steroid receptor complexes. Molecular Endocrinology 1993;7: 1418–29.
97. Wegele H, Wandinger SK, Schmid AB, Reinstein J, Buchner J. Substrate transfer from the chaperone Hsp70 to Hsp90. J Mol Biol 2006;356:802–11.
98. Lee P, Shabbir A, Cardozo C, Caplan AJ. Sti1 and Cdc37 can stabilize Hsp90 in chaperone complexes with a protein kinase. Mol Biol Cell 2004;15:1785–92.
99. Cheung J, Smith DF. Molecular chaperone interactions with steroid receptors: an update. Mol Endocrinol 2000;14:939–46.
100. Davies TH, Ning YM, Sanchez ER. Differential control of glucocorticoid receptor hormone-binding function by tetratricopeptide repeat (TPR) proteins and the immunosuppressive ligand FK506. Biochemistry 2005;44:2030–8.
101. Riggs DL, Roberts PJ, Chirillo SC, et al. The Hsp90-binding peptidylprolyl isomerase FKBP52 potentiates glucocorticoid signaling in vivo. Embo J 2003;22:1158–67.
102. Tranguch S, Cheung-Flynn J, Daikoku T, et al. Cochaperone immunophilin FKBP52 is critical to uterine receptivity for embryo implantation. Proc Natl Acad Sci USA 2005;102:14326–31.
103. Galigniana MD, Harrell JM, Murphy PJ, et al. Binding of hsp90-associated immunophilins to cytoplasmic dynein: direct binding and in vivo evidence that the peptidylprolyl isomerase domain is a dynein interaction domain. Biochemistry 2002;41: 13602–10.
104. Galigniana MD, Radanyi C, Renoir JM, Housley PR, Pratt WB. Evidence that the peptidylprolyl isomerase domain of the hsp90-binding immunophilin FKBP52 is involved in both dynein interaction and glucocorticoid receptor movement to the nucleus. J Biol Chem 2001;276:14884–9.
105. Echeverria PC, Mazaira G, Erlejman A, Gomez-Sanchez C, Piwien Pilipuk G, Galigniana MD. Nuclear import of the glucocorticoid receptor-hsp90 complex through the nuclear pore complex is mediated by its interaction with Nup62 and importin beta. Mol Cell Biol 2009;29:4788–97.
106. Pratt WB, Galigniana MD, Harrell JM, DeFranco DB. Role of hsp90 and the hsp90-binding immunophilins in signalling protein movement. Cell Signal 2004;16: 857–72.
107. Htun H, Holth LT, Walker D, Davie JR, Hager GL. Direct visualization of the human estrogen receptor alpha reveals a role for ligand in the nuclear distribution of the receptor. Mol Biol Cell 1999;10:471–86.
108. Lim CS, Baumann CT, Htun H, et al. Differential localization and activity of the A-and B-forms of the human progesterone receptor using green fluorescent protein chimeras. Mol Endocrinol 1999;13: 366–75.
109. Freeman BC, Yamamoto KR. Disassembly of transcriptional regulatory complexes by molecular chaperones. Science 2002;296: 2232–5.
110. Silverstein AM, Galigniana MD, Kanelakis KC, Radanyi C, Renoir JM, Pratt WB. Different regions of the immunophilin FKBP52 determine its association with the glucocorticoid receptor, hsp90, and cytoplasmic dynein. J Biol Chem 1999;274: 36980–6.
111. Hu J, Toft DO, Seeger C. Hepadnavirus assembly and reverse transcription require a multi-component chaperone complex which is incorporated into nucleocapsids. Embo J 1997;16:59–68.
112. Koga F, Kihara K, Neckers L. Inhibition of cancer invasion and metastasis by targeting the molecular chaperone heat-shock protein 90. Anticancer Res 2009;29:797–807.
113. Sawai A, Chandarlapaty S, Greulich H, et al. Inhibition of Hsp90 down-regulates mutant epidermal growth factor receptor (EGFR) expression and sensitizes EGFR mutant tumors to paclitaxel. Cancer Res 2008;68: 589–96.
114. McDowell CL, Bryan Sutton R, Obermann WM. Expression of Hsp90 chaperome proteins in human tumor tissue. Int J Biol Macromol 2009;45:310–4.
115. Periyasamy S, Warrier M, Tillekeratne MP, Shou W, Sanchez ER. The immunophilin ligands cyclosporin A and FK506 suppress prostate cancer cell growth by androgen receptor-dependent and-independent mechanisms. Endocrinology 2007;148:4716–26.
116. Bredemeyer AJ, Carrigan PE, Fehniger TA, Smith DF, Ley TJ. Hop cleavage and function in granzyme B-induced apoptosis. J Biol Chem 2006;281:37130–41.
117. Radanyi C, Le Bras G, Bouclier C, et al. Tosylcyclonovobiocic acids promote cleavage of the hsp90-associated cochaperone p23. Biochem Biophys Res Commun 2009;379: 514–8.
118. Mollerup J, Berchtold MW. The co-chaperone p23 is degraded by caspases and the proteasome during apoptosis. FEBS Lett 2005; 579:4187–92.
119. Johnson JL, Brown C. Plasticity of the Hsp90 chaperone machine in divergent eukaryotic organisms. Cell Stress Chaperones 2009;14: 83–94.
120. Zhang L, Hach A, Wang C. Molecular mechanism governing heme signaling in yeast: a higher-order complex mediates heme regulation of the transcriptional activator HAP1. Mol Cell Biol 1998;18:3819–28.
121. Nair SC, Toran EJ, Rimerman RA, Hjermstad S, Smithgall TE, Smith DF. A pathway of multi-chaperone interactions common to diverse regulatory proteins: estrogen receptor, Fes tyrosine kinase, heat shock transcription factor Hsf1, and the aryl hydrocarbon receptor. Cell Stress Chaperones 1996;1: 237–50.
122. Blagosklonny MV, Toretsky J, Bohen S, Neckers L. Mutant conformation of p53 translated in vitro or in vivo requires functional HSP90. Proc Natl Acad Sci USA 1996;93:8379–83.
123. Minet E, Ernest I, Michel G, et al. HIF1A gene transcription is dependent on a core promoter sequence encompassing activating and inhibiting sequences located upstream from the transcription initiation site and cis elements located within the 5¢UTR. Biochem Biophys Res Commun 1999;261:534–40.
124. Xu Y, Lindquist S. Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc Natl Acad Sci 1993;90:7074–8.
125. Louvion JF, Abbas-Terki T, Picard D. Hsp90 is required for pheromone signaling in yeast. Mol Biol Cell 1998;9:3071–83.
126. Donze O, Abbas-Terki T, Picard D. The Hsp90 chaperone complex is both a facilitator and a repressor of the dsRNA-dependent kinase PKR. Embo J 2001;20:3771–80.
127. Aligue R, Akhavan-Niak H, Russell P. A role for Hsp90 in cell cycle control: Wee1 tyrosine kinase activity requires interaction with Hsp90. EMBO J 1994;13:6099–106.
128. Xu W, Mimnaugh E, Rosser MF, et al. Sensitivity of mature Erbb2 to geldanamycin is conferred by its kinase domain and is mediated by the chaperone protein Hsp90. The Journal of biological chemistry 2001; 276(5):3702–8.
129. Sato S, Fujita N, Tsuruo T. Modulation of Akt kinase activity by binding to Hsp90. Proc Natl Acad Sci USA 2000;97:10832–7.
130. Eustace BK, Sakurai T, Stewart JK, et al. Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nat Cell Biol 2004;6: 507–14.
131. Siligardi G, Panaretou B, Meyer P, et al. Regulation of Hsp90 ATPase activity by the co-chaperone Cdc37p/p50cdc37. J Biol Chem 2002;277:20151–9.
132. Panaretou B, Siligardi G, Meyer P, et al. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol Cell 2002;10:1307–18.
133. Murata S, Minami Y, Minami M, Chiba T, Tanaka K. CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep 2001;2:1133–8.