The network interaction of the human cytosolic 90kDa heat shock protein Hsp90: A target for cancer therapeutics

Journal of Proteomics

Volumn 75, Issue 10, 2012, Pages 2790-2802

  da Silva, Viviane C H ^a   Ramos, Carlos H I ^a,b  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b Instituto Nacional de Ciencia e Tecnologia em Biologia Estrutural e Bioimagem   (Brazil)

Author keywords

Cancer; Heat shock protein; Hsp90; Molecular chaperone; Protein folding

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ATR PROTEIN; CALMODULIN; CHAPERONE; DJ 1 PROTEIN; DOCETAXEL; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR; HEAT SHOCK PROTEIN 90; INSULIN RECEPTOR SUBSTRATE 2; PHOSPHOTRANSFERASE; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN KINASE C DELTA; RAB7 PROTEIN; RADICICOL; SIRTUIN 2; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNC 51 LIKE KINASE 1; UNCLASSIFIED DRUG;

ACETYLATION; APOPTOSIS; BINDING SITE; BREAST CANCER; CANCER GROWTH; CANCER INVASION; CELL CYCLE ARREST; CELL PROLIFERATION; CELL VIABILITY; CYTOSOL; DNA DAMAGE; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME INACTIVATION; GENE SILENCING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; MYELOID LEUKEMIA; NEOPLASM; NONHUMAN; OVARY CARCINOMA; OXIDATION; OXIDATIVE STRESS; PANCREAS CANCER; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW;

AMINO ACID SEQUENCE; CYTOSOL; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MOLECULAR TARGETED THERAPY; NEOPLASMS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; SEQUENCE HOMOLOGY, AMINO ACID;

EUKARYOTA;

EID: 84860339862     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.12.028     Document Type: Review

References (191)

1. Dyson H.J., Wright P.E. Unfolded proteins and protein folding studied by NMR. Chem Rev 2004, 104:3607-3622.
2. Tompa P. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett 2005, 579:3346-3354.
3. Hartl F.U. Chaperone-assisted protein folding: the path to discovery from a personal perspective. Nat Med 2011, 17:1206-1210.
4. Horwich A.L. Protein folding in the cell: an inside story. Nat Med 2011, 17:1211-1216.
5. Bukau B., Weissman J., Horwich A. Molecular chaperones and protein quality control. Cell 2006, 125:443-451.
6. Hartl F.U., Bracher A., Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011, 475:324-332.
7. Tiroli-Cepeda A., Ramos C.H.I. An overview of the role of molecular chaperones in protein homeostasis. Protein Pept Lett 2011, 18:101-109.
8. Ramos C.H.I., Ferreira S.T. Protein folding, misfolding and aggregation: evolving concepts and conformational diseases. Protein Pept Lett 2005, 12:213-222.
9. Luheshi L.M., Crowther D.C., Dobson C.M. Protein misfolding and disease: from the test tube to the organism. Curr Opin Chem Biol 2008, 12:25-31.
10. Kikis E.A., Gidalevitz T., Morimoto R.I. Protein homeostasis in models of aging and age-related conformational disease. Adv Exp Med Biol 2010, 694:138-159.
11. Anderson J.F., Siller E., Barral J.M. Disorders of protein biogenesis and stability. Protein Pept Lett 2011, 18:110-121.
12. Mollapour M, Neckers L. Post-translational modifications of Hsp90 and their contributions to chaperone regulation. Biochim Biophys Acta 2011, doi:. doi:10.1016/j.bbamcr.2011.07.018.
13. Jakob U., Lilie H., Meyer I., Buchner J. Transient interaction of Hsp90 with early unfolding intermediates of citrate synthase. Implications for heat shock in vivo. J Biol Chem 1995, 270:7288-7294.
14. Prodromou C., Pearl L.H. Structure and functional relationships of Hsp90. Curr Cancer Drug Targets 2003, 3:301-323.
15. Taipale M., Jarosz D.F., Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 2010, 11:515-528.
16. Makhnevych T, Houry WA. The role of Hsp90 in protein complex assembly. Biochim Biophys Acta 2011, doi:. doi:10.1016/j.bbamcr.2011.09.001.
17. Sreedhar A.S., Kalmár E., Csermely P., Shen Y.F. Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett 2004, 562:11-15.
18. Chen B., Piel W.H., Gui L., Bruford E., Monteiro A. The HSP90 family of genes in the human genome: insights into their divergence and evolution. Genomics 2005, 86:627-637.
19. Hoffmann T., Hovemann B. Heat-shock proteins, Hsp84 and Hsp86, of mice and men: two related genes encode formerly identified tumour-specific transplantation antigens. Gene 1988, 74:491-501.
20. Chen B., Piel W.H., Gui L., Bruford E., Monteiro A. The HSP90 family of genes in the human genome: insights into their divergence and evolution. Genomics 2005, 86:627-637.
21. Eustace B.K., Sakurai T., Stewart J.K., Yimlamai D., Unger C., Zehetmeier C., et al. Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nat Cell Biol 2004, 6:507-514.
22. Richter K., Buchner J. Hsp90: twist and fold. Cell 2006, 127:251-253.
23. Pearl L.H., Prodromou C. Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 2006, 75:271-294.
24. Ali M.M., Roe S.M., Vaughan C.K., Meyer P., Panaretou B., Piper P.W., et al. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 2006, 440:1013-1017.
25. Mayer M.P. Gymnastics of Molecular Chaperones, Mol. Cell 2010, 39:321-331.
26. Krukenberg K.A., Street T.O., Lavery L.A., Agard D.A. Conformational dynamics of the molecular chaperone Hsp90. Q Rev Biophys 2011, 44:229-255.
27. Chiosis G., Vilenchik M., Kim J., Solit D. Hsp90: the vulnerable chaperone. Drug Discov Today 2004, 9:881-888.
28. Johnson J.L., Brown C. Plasticity of the Hsp90 chaperone machine in divergent eukaryotic organisms. Cell Stress Chaperones 2009, 14:83-94.
29. Russell L.C., Whitt S.R., Chen M.S., Chinkers M. Identification of conserved residues required for the binding of a tetratricopeptide repeat domain to heat shock protein 90. J Biol Chem 1999, 274:20060-20063.
30. Odunuga O.O., Longshaw V.M., Blatch G.L. Hop: more than an Hsp70/Hsp90 adaptor protein. Bioessays 2004, 26:1058-1068.
31. Murata S., Chiba T., Tanaka K. CHIP: a quality-control E3 ligase collaborating with molecular chaperones. Int J Biochem Cell Biol 2003, 35:572-578.
32. Yang J., Roe S.M., Cliff M.J., Williams M.A., Ladbury J.E., Cohen P.T., et al. Molecular basis for TPR domain-mediated regulation of protein phosphatase 5. EMBO J 2005, 24:1-10.
33. Fan A.C., Young J.C. Function of cytosolic chaperones in Tom70-mediated mitochondrial import. Protein Pept Lett 2011, 18:122-131.
34. Miyata Y., Chambraud B., Radanyi C., Leclerc J., Lebeau M.C., Renoir J.M., et al. Phosphorylation of the immunosuppressant FK506-binding protein FKBP52 by casein kinase II: regulation of HSP90-binding activity of FKBP52. Proc Natl Acad Sci U S A 1997, 94:14500-14505.
35. Longshaw V.M., Dirr H.W., Blatch G.L., Lässle M. The in vitro phosphorylation of the co-chaperone mSTI1 by cell cycle kinases substantiates a predicted casein kinase II-p34cdc2-NLS (CcN) motif. Biol Chem 2000, 381:1133-1138.
36. Kobayashi T., Nakatani Y., Tanioka T., Tsujimoto M., Nakajo S., Nakaya K., et al. Regulation of cytosolic prostaglandin E synthase by phosphorylation. Biochem J 2004, 381:59-69.
37. Johnson B.D., Schumacher R.J., Ross E.D., Toft D.O. Hop modulates Hsp70/Hsp90 interactions in protein folding. J Biol Chem 1998, 273:3679-3686.
38. Grenert J.P., Johnson B.D., Toft D.O. The importance of ATP binding and hydrolysis by hsp90 in formation and function of protein heterocomplexes. J Biol Chem 1999, 274:17525-17533.
39. Wegele H., Wandinger S.K., Schmid A.B., Reinstein J., Buchner J. Substrate transfer from the chaperone Hsp70 to Hsp90. J Mol Biol 2006, 356:802-811.
40. Scheufler C., Brinker A., Bourenkov G., Pegoraro S., Moroder L., Bartunik H., et al. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 2000, 101:199-210.
41. Onuoha S.C., Coulstock E.T., Grossmann J.G., Jackson S.E. Structural studies on the co-chaperone Hop and its complexes with Hsp90. J Mol Biol 2008, 379:732-744.
42. Gonçalves D.C., Gava L.M., Ramos C.H.I. Human Hsp70/Hsp90 organizing protein (Hop) D456G is a mixture of monomeric and dimeric species. Protein Pept Lett 2010, 17:492-498.
43. Yi F., Doudevski I., Regan L. HOP is a monomer: investigation of the oligomeric state of the co-chaperone HOP. Protein Sci 2010, 19:19-25.
44. Ebong I.O., Morgner N., Zhou M., Saraiva M.A., Daturpalli S., Jackson S.E., et al. Heterogeneity and dynamics in the assembly of the Heat Shock Protein 90 chaperone complexes. Proc Natl Acad Sci U S A 2011, 108:17939-17944.
45. Gava L.M., Gonçalves D.C., Borges J.C., Ramos C.H.I. Stoichiometry and thermodynamics of the interaction between the C-terminus of human 90kDa heat shock protein Hsp90 and the mitochondrial translocase of outer membrane Tom70. Arch Biochem Biophys 2011, 513:119-125.
46. Cortajarena A.L., Yi F., Regan L. Designed TPR modules as novel anticancer agents. ACS Chem Biol 2008, 3:161-166.
47. Yi F., Regan L. A novel class of small molecule inhibitors of Hsp90. ACS Chem Biol 2008, 3:645-654.
48. Pimienta G., Herbert K.M., Regan L. A compound that inhibits the HOP-Hsp90 complex formation and has unique killing effects in breast cancer cell lines. Mol Pharmacol 2011, 8:2252-2261.
49. Walsh N., Larkin A.M., Swan N., Conlon K., Dowling P., McDermott R., et al. RNAi knockdown of Hop (Hsp70/Hsp90 organising protein) decreases invasion via MMP-2 down regulation. Cancer Lett 2011, 306:180-189.
50. Connell P., Ballinger C.A., Jiang J., Wu Y., Thompson L.J., Hohfeld J., et al. The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat Cell Biol 2001, 3:93-96.
51. Zhou P., Fernandes N., Dodge I.L., Reddi A.L., Rao N., Safran H., et al. ErbB2 degradation mediated by the co-chaperone protein CHIP. J Biol Chem 2003, 278:13829-13837.
52. Zhang L., Nephew K.P., Gallagher P.J. Regulation of death-associated protein kinase. Stabilization by HSP90 heterocomplexes. J Biol Chem 2007, 282:11795-11804.
53. Kajiro M., Hirota R., Nakajima Y., Kawanowa K., So-ma K., Ito I., et al. The ubiquitin ligase CHIP acts as an upstream regulator of oncogenic pathways. Nat Cell Biol 2009, 11:312-319.
54. Yan S., Sun X., Xiang B., Cang H., Kang X., Chen Y., et al. Redox regulation of the stability of the SUMO protease SENP3 via interactions with CHIP and Hsp90. EMBO J 2010, 29:3773-3786.
55. Mclaughlin S.H., Sobott F., Yao Z.P., Zhang W., Nielsen P.R., Grossmann J.G., et al. The co- chaperone p23 arrests the Hsp90 ATPase cycle to trap client proteins. J Mol Biol 2006, 356:746-758.
56. Panaretou B., Siligardi G., Meyer P., Maloney A., Sullivan J.K., Singh S., et al. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone Aha1. Mol Cell 2002, 10:1307-1318.
57. Meyer P., Prodromou C., Liao C., Hu B., Roe S.M., Vaughan C.K., et al. Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery. EMBO J 2004, 23:511-519.
58. Harst A., Lin H., Obermann W.M. 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, 387:789-796.
59. Retzlaff M., Hagn F., Mitschke L., Hessling M., Gugel F., Kessler H., et al. Asymmetric activation of the hsp90 dimer by its cochaperone Aha1. Mol Cell 2010, 37:344-354.
60. Holmes J.L., Sharp S.Y., Hobbs S., Workman P. Silencing of HSP90 cochaperone AHA1 expression decreases client protein activation and increases cellular sensitivity to the HSP90inhibitor 17-allylamino-17-demethoxygeldanamycin. Cancer Res 2008, 68:1188-1197.
61. Mandal A.K., Lee P., Chen J.A., Nillegoda N., Heller A., DiStasio S., 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, 176:319-328.
62. Smith J.R., Workman P. Targeting CDC37: an alternative, kinase-directed strategy for disruption of oncogenic chaperoning. Cell Cycle 2009, 8:362-372.
63. Zhang T., Hamza A., Cao X., Wang B., Yu S., Zhan C.G., et al. A novel Hsp90 inhibitor to disrupt Hsp90/Cdc37 complex against pancreatic cancer cells. Mol Cancer Ther 2008, 7:162-170.
64. Wandinger S.K., Suhre M.H., Wegele H., Buchner J. The phosphatase Ppt1 is a dedicated regulator of the molecular chaperone Hsp90. EMBO J 2006, 25:367-376.
65. Vaughan C.K., Mollapour M., Smith J.R., Truman A., Hu B., Good V.M., et al. Hsp90-dependent activation of protein kinases is regulated by chaperone-targeted dephosphorylation of Cdc37. Mol Cell 2008, 31:886-895.
66. Jeong H., Mason S.P., Barabasi A.L., Oltvai Z.N. Lethality and centrality in protein networks. Nature 2001, 411:41-42.
67. Higurashi M., Ishida T., Kinoshita K. Identification of transient hub proteins and the possible structural basis for their multiple interactions. Protein Sci 2008, 17:72-78.
68. Ekman D., Light S., Björklund A.K., Elofsson A. What properties characterize the hub proteins of the protein-protein interaction network of Saccharomyces cerevisiae?. Genome Biol 2006, 7:R45.
69. Zhao R., Davey M., Hsu Y.C., Kaplanek P., Tong A., Parsons A.B., et al. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 2005, 120:715-727.
70. Batada N.N., Hurst L.D., Tyers M. Evolutionary and physiological importance of hub proteins. PLoS Comput Biol 2006, 2:e88.
71. Patil A., Nakamura H. Disordered domains and high surface charge confer hubs with the ability to interact with multiple proteins in interaction networks. FEBS Lett 2006, 580:2041-2045.
72. McClellan A.J., Xia Y., Deutschbauer A.M., Davis R.W., Gerstein M., Frydman J. Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell 2007, 13:1121-1135.
73. Workman P. Combinatorial attack on multistep oncogenesis by inhibiting the Hsp90 molecular chaperone. Cancer Lett 2004, 206:149-157.
74. Sharp S., Workman P. Inhibitors of the HSP90 molecular chaperone: current status. Adv Cancer Res 2006, 95:323-348.
75. Neckers L. Heat shock protein 90: the cancer chaperone. J Biosci 2007, 32:517-530.
76. Pearl L.H., Prodromou C., Workman P. The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem J 2008, 410:439-453.
77. Gava L., Ramos C.H.I. Human 90kDa heat shock protein Hsp90 as a target for cancer therapeutics. Curr Chem Biol 2009, 3:330-341.
78. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
79. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
80. Whitesell L., Bagatell R., Falsey R. The stress response: implications for the clinical development of hsp90 inhibitors. Curr Cancer Drug Targets 2003, 3:349-358.
81. Kamal A., Thao L., Sensintaffar J., Zhang L., Boehm M.F., Fritz L.C., et al. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 2003, 425:407-410.
82. Taldone T., Chiosis G. Purine-scaffold Hsp90 inhibitors. Curr Top Med Chem 2009, 9:1436-1446.
83. Salminen A., Ojala J., Kaarniranta K., Hiltunen M., Soininen H. Hsp90 regulates tau pathology through co-chaperone complexes in Alzheimer's disease. Prog Neurobiol 2011, 93:99-110.
84. Shonhai A., Maier A.G., Przyborski J.M., Blatch G.L. Intracellular protozoan parasites of humans: the role of molecular chaperones in development and pathogenesis. Protein Pept Lett 2011, 18:143-157.
85. Cowen L.E., Singh S.D., Köhler J.R., Collins C., Zaas A.K., Schell W.A., et al. Harnessing Hsp90 function as a powerful, broadly effective therapeutic strategy for fungal infectious disease. Proc Natl Acad Sci U S A 2009, 106:2818-2823.
86. Chase G., Deng T., Fodor E., Leung B.W., Mayer D., Schwemmle M., et al. Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 2008, 377:431-439.
87. Brugge J.S. Interaction of the Rous sarcoma virus protein pp 60v-src with the cellular proteins pp50 and pp90. Curr Top Microbiol Immunol 1986, 123:1-22.
88. Xu Y., Lindquist S. Heat-shock protein Hsp90 governs the activity of pp 60v-src kinase. Proc Natl Acad Sci U S A 1993, 90:7074-7078.
89. Di Cosimo S., Baselga J. Targeted therapies in breast cancer: where are we now?. Eur J Cancer 2008, 44:2781-2790.
90. Yarden Y., Kuang W.J., Yang-Feng T., Coussens L., Munemitsu S., Dull T.J., et al. Human proto-oncogene c-kit: a new cell surface receptor tyrosine kinase for an unidentified ligand. EMBO J 1987, 6:3341-3351.
91. Matthews W., Jordan C.T., Wiegand G.W., Pardoll D., Lemischka I.R. A receptor tyrosine kinase specific to hematopoietic stem and progenitor cell-enriched populations. Cell 1991, 65:1143-1152.
92. Furitsu T., Tsujimura T., Tono T., Ikeda H., Kitayama H., Koshimizu U., et al. Identification of mutations in the coding sequence of the proto-oncogene c-kit in a human mast cell leukemia cell line causing ligand-independent activation of c-kit product. J Clin Invest 1993, 92:1736-1744.
93. Hirota S., Isozaki K., Moriyama Y., Hashimoto K., Nishida T., Ishiguro S., et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 1998, 279:577-580.
94. Fumo G., Akin C., Metcalfe D.D., Neckers L. 17-Allylamino-17-demethoxygeldanamycin (17-AAG) is effective in downregulating mutated, constitutively activated KIT protein in human mast cells. Blood 2004, 103:1078-1084.
95. Banerji U., O'Donnell A., Scurr M., Pacey S., Stapleton S., Asad Y., et al. Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advanced malignancies. J Clin Oncol 2005, 23:4152-4161.
96. Dias S.R., Friedlos F., Light Y., Springer C., Workman P., Marais R. Activated B-RAF is an Hsp90 client protein that is targeted by the anticancer drug 17-allylamino-17-demethoxygeldanamycin. Cancer Res 2005, 65:10686-10691.
97. Grbovic O.M., Basso A.D., Sawai A., Ye Q., Friedlander P., Solit D., et al. V600E BRaf requires the Hsp90 chaperone for stability and is degraded in response to Hsp90 inhibitors. Proc Natl Acad Sci U S A 2006, 103:57-62.
98. Fukuyo Y., Inoue M., Nakajima T., Higashikubo R., Horikoshi N.T., Hunt C., et al. Oxidative stress plays a critical role in inactivating mutant BRAF by geldanamycin derivatives. Cancer Res 2008, 68:6324-6330.
99. Mehta P.P., Kung P., Yamazaki S., Walls M., Shen A., Nguyen L., et al. A novel class of specific Hsp90 small molecule inhibitors demonstrate in vitro and in vivo anti-tumor activity in human melanoma cells. Cancer Lett 2011, 300:30-39.
100. Lewis J., Devin A., Miller A., Lin Y., Rodriguez Y., Neckers L., et al. Disruption of hsp90 function results in degradation of the death domain kinase, receptor-interacting protein (RIP), and blockage of tumor necrosis factor-induced nuclear factor-kappaB activation. J Biol Chem 2000, 275:10519-10526.
101. Georgakis G.V., Li Y., Younes A. The heat shock protein 90 inhibitor 17-AAG induces cell cycle arrest and apoptosis in mantle cell lymphomacell lines by depleting cyclin D1, Akt, Bid and activating caspase 9. Br J Haematol 2006, 135:68-71.
102. Ahmad N., Kumar R. Steroid hormone receptors in cancer development: a target for cancer therapeutics. Cancer Lett 2011, 300:1-9.
103. Echeverría P.C., Picard D. Molecular chaperones, essential partners of steroid hormone receptors for activity and mobility. Biochim Biophys Acta 2010, 1803:641-649.
104. Soussi T., Legros Y., Lubin R., Ory K., Schlichtholz B. Multifactorial analysis of p53 alteration in human cancer: a review. Int J Cancer 1994, 57:1-9.
105. Vogelstein B., Lane D., Levine A.J. Surfing the p53 network. Nature 2000, 408:307-310.
106. Römer L., Klein C., Dehner A., Kessler H., Buchner J. p53-a natural cancer killer: structural insights and therapeutic concepts. Angew Chem Int Ed Eng 2006, 45:6440-6460.
107. Maki C.G., Huibregtse J.M., Howley P.M. In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res 1996, 56:2649-2654.
108. Soussi T. The p53 tumor suppressor gene: from molecular biology to clinical investigation. Ann N Y Acad Sci 2000, 910:121-139.
109. Lin K., Rockliffe N., Johnson G.G., Sherrington P.D., Pettitt A.R. Hsp90 inhibition has opposing effects on wild-type and mutant p53 and induces p21 expression and cytotoxicity irrespective of p53/ATM status in chronic lymphocytic leukaemia cellsHsp90 inhibition and p53/ATM status in CLL. Oncogene 2008, 27:2445-2455.
110. Fukumoto R., Kiang J.G. Geldanamycin analog 17-DMAG limits apoptosis in human peripheral blood cells by inhibition of p53 activation and its interaction with heat-shock protein 90kDa after exposure to ionizing radiation. Radiat Res 2011, 176:333-345.
111. DeZwaan D.C., Freeman B.C. HSP90 manages the ends. Trends Biochem Sci 2010, 35:384-391.
112. Lydall D. Taming the tiger by the tail: modulation of DNA damage responses by telomeres. EMBO J 2009, 28:2174-2187.
113. Holt S.E., Aisner D.L., Baur J., Tesmer V.M., Dy M., Ouellette M., et al. Functional requirement of p23 and Hsp90 in telomerase complexes. Genes Dev 1999, 13:817-826.
114. Forsythe H.L., Jarvis J.L., Turner J.W., Elmore L.W., Holt S.E. Stable association of HSP90 and p23, but not Hsp70, with active human telomerase. J Biol Sci 2001, 276:15571-15574.
115. DeZwaan D.C., Toogun O.A., Echtenkamp F.J., Freeman B.C. The Hsp82 molecular chaperone promotes a switch between unextendable and extendable telomere states. Nat Struct Mol Biol 2009, 16:711-716.
116. Laskar S., Bhattacharyya M.K., Shankar R., Bhattacharyya S. HSP90 controls SIR2 mediated gene silencing. PLoS One 2011, 6:e23406.
117. Barral J.M., Hutagalung A.H., Brinker A., Hartl F.U., Epstein H.F. Role of the myosin assembly protein UNC-45 as a molecular chaperone for myosin. Science 2002, 295:669-671.
118. Willis M.S., Schisler J.C., Portbury A.L., Patterson C. Build it up-tear it down: protein quality control in the cardiac sarcomere. Cardiovasc Res 2009, 81:439-448.
119. Gaiser A.M., Kaiser C.J.O., Haslbeck V., Richter K. Downregulation of the Hsp90 system causes defects in muscle cells of Caenorhabditis elegans. PLoS One 2011, 6:e25485.
120. Voellmy R., Boellmann F. Chaperone regulation of the heat shock protein response. Adv Exp Med Biol 2007, 594:89-99.
121. Francis B.R., Thorsness P.E. Hsp90 and mitochondrial proteases Yme1 and Yta10/12 participate in ATP synthase assembly in Saccharomyces cerevisiae. Mitochondrion 2011, 1:587-600.
122. Lees-Miller S.P., Anderson C.W. The human double-stranded DNA-activated protein kinase phosphorylates the 90-kDa heat-shock protein, Hsp90α at two NH2-terminal threonine residues. J Biol Chem 1989, 264:17275-17280.
123. Lees-Miller S.P., Anderson C.W. Two human 90-kDa heat shock proteins are phosphorylated in vivo at conserved. J Biol Chem 1989, 264:2431-2437.
124. Brouet A., Sonveaux P., Dessy C., Moniotte S., Balligand J.L., Feron O. Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins. Circ Res 2001, 89:866-873.
125. Ogiso H., Kagi N., Matsumoto E., Nishimoto M., Arai R., Shirouzu M., et al. Phosphorylation analysis of 90kDa heat shock protein within the cytosolic aryl-hydrocarbon receptor complex. Biochemistry 2004, 43:15510-15519.
126. Duval M., Le Boeuf F., Huot J., Gratton J.P. Src-mediated phosphorylation of Hsp90 in response to vascular endothelial growth factor (VEGF) is required for VEGF receptor-2 signaling to endothelial NO synthase. Mol Biol Cell 2007, 18:4659-4668.
127. Kurokawa M., Zhao C., Reya T., Kornbluth S. Inhibition of apoptosome formation by suppression of Hsp90β phosphorylation in tyrosine kinase-induced leukemias. Mol Cell Biol 2008, 28:5494-5506.
128. Deb T.B., Zuo A.H., Wang Y., Barndt R.J., Cheema A.K., Sengupta S., et al. Pnck induces ligand-independent EGFR degradation by probable perturbation of the Hsp90 chaperone complex. Am J Physiol Cell Physiol 2011, 300:1139-1154.
129. Mollapour M., Tsutsumi S., Truman A.W., Xu W., Vaughan C.K., Beebe K., et al. Threonine 22 phosphorylation attenuates Hsp90 interaction with cochaperones and affects its chaperone activity. Mol Cell 2011, 41:672-681.
130. Scroggins B.T., Robzyk K., Wang D., Marcu M.G., Tsutsumi S., Beebe K., et al. An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol Cell 2007, 25:151-159.
131. Yang Y., Rao R., Shen J., Tang Y., Fiskus W., Nechtman J., et al. Role of acetylation and extracellular location of heat shock protein 90α in tumor cell invasion. Cancer Res 2008, 68:4833-4842.
132. Zhang Y., Kwon S., Yamaguchi T., Cubizolles F., Rousseaux S., Kneissel M., et al. Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally. Mol Cell Biol 2008, 28:1688-1701.
133. Zhou Q., Agoston A.T., Atadja P., Nelson W.G., Davidson N.E. Inhibition of histone deacetylases promotes ubiquitin-dependent proteasomal degradation of DNA methyltransferase 1 in human breast cancer cells. Mol Cancer Res 2008, 6:873-883.
134. Gao C., Guo H., Wei J., Mi Z., Wai P.Y., Kuo P.C. Identification of S-nitrosylated proteins in endotoxin-stimulated RAW264.7 murine macrophages. Nitric Oxide 2005, 12:121-126.
135. Martinez-Ruiz A., Villanueva L., Gonzalez De Orduna C., Lopez-Ferrer D., Higueras M.A., Tarin C., et al. S-nitrosylation of Hsp90 promotes the inhibition of its ATPase and endothelial nitric oxide synthase regulatory activities. Proc Natl Acad Sci U S A 2005, 102:8525-8530.
136. Zhang Y., Keszler A., Broniowska K.A., Hogg N. Characterization and application of the biotin-switch assay for the identification of S-nitrosated proteins. Free Radic Biol Med 2005, 38:874-881.
137. Retzlaff M., Stahl M., Eberl H.C., Lagleder S., Beck J., Kessler H., et al. Hsp90 is regulated by a switch point in the C-terminal domain. EMBO Rep 2009, 10:1147-1153.
138. Zhao Y.G., Gilmore R., Leone G., Coffey M.C., Weber B., Lee P.W. Hsp90 phosphorylation is linked to its chaperoning function. Assembly of the reovirus cell attachment protein. J Biol Chem 2001, 276:32822-32827.
139. Mollapour M., Tsutsumi S., Neckers L. Hsp90 phosphorylation, Wee1 and the cell cycle. Cell Cycle 2010, 9:2310-2316.
140. Murtagh J., Lu H., Schwartz E.L. Taxotere-induced inhibition of human endothelial cell migration is a result of heat shock protein 90 degradation. Cancer Res 2006, 66:8192-8199.
141. Prodromou C., Siligardi G., O'Brien R., Woolfson D.N., Regan L., Panaretou B., et al. Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. EMBO J 1999, 18:754-762.
142. Southworth D.R., Agard D.A. Client-loading conformation of the Hsp90 molecular chaperone revealed in the cryo-EM structure of the human Hsp90:Hop complex. Mol Cell 2011, 42:771-781.
143. Das A.K., Cohen P.W., Barford D. The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J 1998, 17:1192-1199.
144. Cliff M.J., Williams M.A., Brooke-Smith J., Barford D., Ladbury J.E. Molecular recognition via coupled folding and binding in a TPR domain. J Mol Biol 2005, 346:717-732.
145. Cliff M.J., Harris R., Barford D., Ladbury J.E., Williams M.A. Conformational diversity in the TPR domain-mediated interaction of protein phosphatase 5 with Hsp90. Structure 2006, 14:415-426.
146. Zhang M., Windheim M., Roe S.M., Peggie M., Cohen P., Prodromou C., et al. Chaperoned ubiquitylation-crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIPUbc13-Uev1a complex. Mol Cell 2005, 20:525-538.
147. Cheung-Flynn J., Roberts P.J., Riggs D.L., Smith D.F. C-terminal sequences outside the tetratricopeptide repeat domain of FKBP51 and FKBP52 cause differential binding to Hsp90. J Biol Chem 2003, 278:17388-17394.
148. Young J.C., Hoogenraad N.J., Hartl F.U. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 2003, 112:41-50.
149. Li J., Qian X., Hu J., Sha B. Molecular chaperone Hsp70/Hsp90 prepares the mitochondrial outer membrane translocon receptor Tom71 for preprotein loading. J Biol Chem 2009, 284:23852-23859.
150. Jascur T., Brickner H., Salles-Passador I., Barbier V., El Khissiin A., Smith B., et al. Regulation of p21(WAF1/CIP1) stability by WISp39, a Hsp90 binding TPR protein. Mol Cell 2005, 17:237-249.
151. Carrello A., Ingley E., Minchin R.F., Tsai S., Ratajczak T. The common tetratricopeptide repeat acceptor site for steroid receptor- associated immunophilins and Hop is located in the dimerization domain of Hsp90. J Biol Chem 1999, 274:2682-2689.
152. 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, 275:34140-34146.
153. Meyer B.K., Perdew G.H. Characterization of the AhR-hsp90-XAP2 core complex and the role of the immunophilin-related protein XAP2 in AhR stabilization. Biochemistry 1999, 38:8907-8917.
154. Boulon S., Marmier-Gourrier N., Pradet-Balade B., Wurth L., Verheggen C., Jady B.E., et al. The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J Cell Biol 2008, 180:579-595.
155. Millson S.H., Vaughan C.K., Zhai C., Ali M.M., Panaretou B., Piper P.W., et al. Chaperone ligand-discrimination by the TPR-domain protein Tah1. Biochem J 2008, 413:261-268.
156. Chadli A., Graham J.D., Abel M.G., Jackson T.A., Gordon D.F., Wood W.M., et al. GCUNC-45 is a novel regulator for the progesterone receptor/hsp90 chaperoning pathway. Mol Cell Biol 2006, 26:1722-1730.
157. Millson S.H., Truman A.W., King V., Prodromou C., Pearl L.H., Piper P.W. A two-hibrid screen of the yeast proteome for Hsp90 interactors uncovers a novel Hsp90 chaperone requirement in the activity of a stress-activated mitogen-activated protein kinase, Slt2p (Mpk1p). Eukaryot Cell 2005, 4:849-860.
158. Roe S.M., Ali M.M., Meyer P., Vaughan C.K., Panaretou B., Piper P.W., et al. The mechanism of Hsp90 regulation by the protein kinase-specific cochaperone p50cdc37. Cell 2004, 116:87-98.
159. Zhao R., Davey M., Hsu Y.C., Kaplanek P., Tong A., Parsons A.B., et al. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 2005, 120:715-727.
160. Johnson J.L., Toft D.O. Binding of p23 and hsp90 during assembly with the progesterone receptor. Mol Endocrinol 1995, 9:670-678.
161. Koulov A.V., Lapointe P., Lu B., Razvi A., Coppinger J., Dong M.Q., et al. Biological and structural basis for Aha1 regulation of Hsp90 ATPase activity in maintaining proteostasis in the human disease cystic fibrosis. Mol Biol Cell 2010, 21:871-884.
162. Adwan T.S., Ohm A.M., Jones D.M.N., Humphries M.J., Reyland M.E. Regulated binding of importin-α to PKCδ in response to apoptotic signals facilitates nuclear import. JBC 2011, 286:35716-35724.
163. Ha K., Fiskus W., Rao R., Balusu R., Venkannagari S., Nalabothula N.R., et al. Hsp90 inhibitor-mediated disruption of chaperone association of ATR with Hsp90 sensitizes cancer cells to DNA damage. Mol Cancer Ther 2011, 10:1194-1206.
164. Kim Y.M., Pyo H. Cooperative enhancement of radiosensitivity after combined treatment of 17-(allylamino)-17-demethoxygeldanamycin and celecoxib in human lung and colon cancer cell lines. DNA Cell Biol 2012, 31:15-29.
165. Joo J.H., Dorsey F.C., Joshi A., Hennessy-Walters K.M., Rose K.L., McCastlain K., et al. Hsp90-Cdc37 chaperone complex regulates Ulk1- and Atg13-mediated mitophagy. Mol Cell 2011, 43:572-585.
166. Fukushima T., Okajima H., Yamanaka D., Ariga M., Nagata S., Ito A., et al. HSP90 interacting with IRS-2 is involved in cAMP-dependent potentiation of IGF-I signals in FRTL-5 cells. Mol Cell Endocrinol 2011, 344:81-89.
167. Knobbe C., Revett T., Bai Y., Chow V., Jeon A.H.W., Bohm C., et al. Choice of bioloical source material supersedes oxidative stress in its influence on DJ-1 in vivo interactions with Hsp90. J Proteome Res 2011, 10:4388-4404.
168. Jin Y., Zhen Y., Haugsten E.M., Wiedlocha A. The driver of malignancy in KG-1a leukemic cells, FGFR1OP2-FGFR1, encodes an HSP90 addicted oncoprotein. Cell Signal 2011, 23:1758-1766.
169. Wang T, Zhang M, Ma Z, Guo K, Tergaonkar V, Zeng Q, Hong W. A role of Rab7 in stabilizing EGFR-Her2 and in sustaining Akt survival signal. J Cell Physiol 2011, doi:. doi:10.1002/jcp.23023.
170. Kim Y.J., Lee S.A., Myung S.C., Kim W., Lee C.S. Radicicol, an inhibitor of Hsp90, enhances TRAIL-induced apoptosis in human epithelial ovarian carcinoma cells by promoting activation of apoptosis-related proteins. Mol Cell Biochem 2012, 359:33-43.
171. Kekatpure V.D., Dannenberg A.J., Subbaramaiah K. HDAC6 modulates Hsp90 chaperone activity and regulates activation of aryl hydrocarbon receptor signaling. J Biol Chem 2009, 284:7436-7445.
172. Carbone D.L., Doorn J.A., Kiebler Z., Ickes B.R., Petersen D.R. Modification of heat shock protein 90 by 4-hydroxynonenal in a rat model of chronic alcoholic liver disease. J Pharmacol Exp Ther 2005, 315:8-15.
173. Kundrat L., Regan L. Identification of residues on Hsp70 and Hsp90 ubiquitinated by the cochaperone CHIP. J Mol Biol 2010, 395:587-594.
174. Mollapour M., Tsutsumi S., Donnelly A.C., Beebe K., Tokita M.J., Lee M.J., et al. Swe1Wee1-dependent tyrosine phosphorylation of Hsp90 regulates distinct facets of chaperone function. Mol Cell 2010, 37:333-343.
175. Bennetzen M.V., Larsen D.H., Bunkenborg J., Bartek J., Lukas J., Andersen J.S. Site-specific phosphorylation dynamics of the nuclear proteome during the DNA damage response. Mol Cell Proteomics 2010, 9:1314-1323.
176. Wang Z., Gucek M., Hart G.W. Cross-talk between GlcNAcylation and phosphorylation: site-specific phosphorylation dynamics in response to globally elevated O-GlcNAc. Proc Natl Acad Sci U S A 2008, 105:13793-13798.
177. Jorgensen C., Sherman A., Chen G.I., Pasculescu A., Poliakov A., Hsiung M., et al. Cell-specific information processing in segregating populations of Eph receptor ephrin-expressing cells. Science 2009, 326:1502-1509.
178. Choudhary C., Olsen J.V., Brandts C., Cox J., Reddy P.N., Bohmer F.D., et al. Mislocalized activation of oncogenic RTKs switches downstream signaling outcomes. Mol Cell 2009, 36:326-339.
179. Olsen J.V., Blagoev B., Gnad F., Macek B., Kumar C., Mortensen P., et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127:635-648.
180. Guo A., Villen J., Kornhauser J., Lee K.A., Stokes M.P., Rikova K., et al. Signaling networks assembled by oncogenic EGFR and c-Met. Proc Natl Acad Sci U S A 2008, 105:692-697.
181. Rikova K., Guo A., Zeng Q., Possemato A., Yu J., Haack H., et al. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007, 131:1190-1203.
182. Huttlin E.L., Jedrychowski M.P., Elias J.E., Goswami T., Rad R., Beausoleil S.A., et al. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 2010, 143:1174-1189.
183. Rose D.W., Wettenhall R.E., Kudlicki W., Kramer G., Hardesty B. The 90-kilodalton peptide of the heme-regulated eIF-2 alpha kinase has sequence similarity with the 90-kilodalton heat shock protein. Biochemistry 1987, 26:6583-6587.
184. Lei H., Venkatakrishnan A., Yu S., Kazlauskas A. Protein kinase A-dependent translocation of Hsp90 alpha impairs endothelial nitric-oxide synthase activity in high glucose and diabetes. J Biol Chem 2007, 282:9364-9371.
185. Molina H., Horn D.M., Tang N., Mathivanan S., Pandey A. Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. Proc Natl Acad Sci U S A 2007, 104:2199-2204.
186. 90 phosphorylation of Hsp90α by protein kinase A regulates its chaperone machinery. Biochem J 2012, 441:387-397.
187. Moritz A., Li Y., Guo A., Villen J., Wang Y., MacNeill J., et al. Akt-RSK-S6 kinase signaling networks activated by oncogenic receptor tyrosine kinases. Sci Signal 2010, 3:ra64.
188. Mayya V., Lundgren D.H., Hwang S.I., Rezaul K., Wu L., Eng J.K., et al. Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions. Sci Signal 2009, 2:ra46.
189. Olsen J.V., Vermeulen M., Santamaria A., Kumar C., Miller M.L., Jensen L.J., et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 2010, 3:ra3.
190. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
191. Dephoure N., Zhou C., Villen J., Beausoleil S.A., Bakalarski C.E., Elledge S.J., et al. A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci U S A 2008, 105:10762-10767.