Heat-shock protein 90 inhibitors in cancer therapy: 17AAG and beyond

Future Oncology

Volumn 1, Issue 2, 2005, Pages 273-281

  Younes, Anas ^a   Georgakis, Georgios V ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

17 AAG; apoptosis; cancer; geldanamycin; heat shock protein (HSP)70; HSP90; lymphoma

Indexed keywords

17 ALLYLAMINO 17 DEMETHOXYGELDANAMYCIN; 17-(ALLYLAMINO)-17-DEMETHOXYGELDANAMYCIN; ANTINEOPLASTIC AGENT; BENZOQUINONE DERIVATIVE; CHAPERONE; DRUG DERIVATIVE; HEAT SHOCK PROTEIN 90; MACROCYCLIC LACTAM; PROTEIN SERINE THREONINE KINASE; RIFABUTIN;

APOPTOSIS; CELL CYCLE; DRUG ANTAGONISM; DRUG EFFECT; HUMAN; METABOLISM; NEOPLASM; REVIEW; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZOQUINONES; CELL CYCLE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; MOLECULAR CHAPERONES; NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; RIFABUTIN; SIGNAL TRANSDUCTION;

EID: 31544471974     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.1517/14796694.1.2.273     Document Type: Review

References (103)

1. Ritossa F: A new puffing pattern induced by temperature shock and DNP in Drosphila. Experientia 18, 571-573 (1962)
2. Ritossa F: Discovery of the heat shock response. Cell Stress Chaperones 1, 97-98 (1996)
3. Rutherford SL: Between genotype and phenotype: protein chaperones and evolvability. Nature Rev. Genet. 4, 263-274 (2003)
4. Sorger PK, Pelham HR: The glucose-regulated protein grp94 is related to heat shock protein hsp90. J. Mol. Biol. 194, 341-344 (1987)
5. Argon Y, Simen BB: GRP94, an ER chaperone with protein and peptide binding properties. Semin. Cell. Dev. Biol. 10, 495-505 (1999)
6. Felts SJ, Owen BA, Nguyen P, Trepel J, Donner DB, Toft DO: The hsp90-related protein TRAP1 is a mitochondrial protein with distinct functional properties. J. Biol. Chem. 275, 3305-3312 (2000)
7. Nelson GM, Huffman H, Smith DF: Comparison of the carboxy-terminal DPrepeat region in the co-chaperones Hop and Hip. Cell Stress Chaperones 8, 125-133 (2003)
8. Pearl LH (2005) Hsp90 and Cdc37 - a chaperone cancer conspiracy. Curr. Opin. Genet. Dev. 15, 55-61 (2003)
9. Meyer P: Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery. Embo. J. 23, 1402-1410 (2004)
10. Morishima Y, Kanelakis KC, Murphy PJ et al.: The hsp90 co-chaperone p23 is the limiting component of the multiprotein hsp90/hsp70- based chaperone system in vivo where it acts to stabilize the client protein: hsp90 complex. J. Biol. Chem. 278, 48754-48763 (2003)
11. Christians ES, Zhou Q, Renard J, Benjamin IJ: Heat shock proteins in mammalian development. Semin. Cell. Dev. Biol. 14, 283-290 (2003)
12. Sreedhar AS, Csermely P: Heat shock proteins in the regulation of apoptosis: new strategies in tumor therapy: a comprehensive review. Pharmacol. Ther. 101, 227-257 (2004)
13. Garrido C, Schmitt E, Cande C, Vahsen N, Parcellier A, Kroemer G: HSP27 and HSP70: potentially oncogenic apoptosis inhibitors. Cell Cycle 2, 579-584 (2003)
14. Basso AD, Solit DB, Chiosis G, Giri B, Tsichlis P, Rosen N: Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. J. Biol. Chem. 277, 39858-39866 (2002)
15. Tolson JK, Roberts SM: Manipulating heat shock protein expression in laboratory animals. Methods 35, 149-157 (2005)
16. Pirkkala L, Nykanen P, Sistonen L: Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 15, 1118-1131 (2001)
17. Kamal A, Thao L, Sensintaffar J et al.: A highaffinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425, 407-410 (2003)
18. Hoang AT, Huang J, Rudra-Ganguly N et al.: A Novel Association between the Human Heat Shock Transcription Factor 1 (HSF1) and Prostate Adenocarcinoma. Am. J. Pathol. 156, 857-864 (2000)
19. Pieper M, Rupprecht HD, Bruch KM, De Heer E, Schocklmann HO: Requirement of heat shock protein 90 in mesangial cell mitogenesis. Kidney Int. 58, 2377-2389 (2000)
20. Kamal A, Boehm MF, Burrows FJ: Therapeutic and diagnostic implications of Hsp90 activation. Trends Mol. Med. 10, 283-290 (2004)
21. Sreedhar AS, Kalmar E, Csermely P, Shen YF: Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett. 562, 11-15 (2004)
22. Grammatikakis N, Vultur A, Ramana CV et al.: The role of Hsp90N, a new member of the Hsp90 family, in signal transduction and neoplastic transformation. J. Biol. Chem. 277, 8312-8320 (2002)
23. Scheibel T, Siegmund HI, Jaenicke R, Ganz P, Lilie H, Buchner J: The charged region of Hsp90 modulates the function of the Nterminal domain. Proc. Natl Acad. Sci. USA 96, 1297-1302 (1999)
24. Matsumoto S, Tanaka E, Nemoto TK et al.: Interaction between the N-terminal and middle regions is essential for the in vivo function of HSP90 molecular chaperone. J. Biol. Chem. 277, 34959-34966 (2002)
25. Yamada S, Ono T, Mizuno A, Nemoto TK: A hydrophobic segment within the C-terminal domain is essential for both client-binding and dimer formation of the HSP90-family molecular chaperone. Eur. J. Biochem. 270, 146-154 (2003)
26. Passinen S, Valkila J, Manninen T, Syvala H, Ylikomi T: The C-terminal half of Hsp90 is responsible for its cytoplasmic localization. Eur. J. Biochem. 268, 5337-5342 (2001)
27. Minami Y, Kimura Y, Kawasaki H, Suzuki K, Yahara I: The carboxy-terminal region of mammalian HSP90 is required for its dimerization and function in vivo. Mol. Cell. Biol. 14, 1459-1464 (1994)
28. Johnson BD, Schumacher RJ, Ross ED, Toft DO: Hop modulates Hsp70/Hsp90 interactions in protein folding. J. Biol. Chem. 273, 3679-6386 (1998)
29. Odunuga OO, Longshaw VM, Blatch GL: Hop: more than an Hsp70/Hsp90 adaptor protein. Bioessays 26, 1058-1068 (2004)
30. Radanyi C, Chambraud B, Baulieu EE: The ability of the immunophilin FKBP59-HBI to interact with the 90-kDa heat shock protein is encoded by its tetratricopeptide repeat domain. Proc. Natl Acad. Sci. USA 91, 11197-11201 (1994)
31. Pratt WB, Toft DO: Regulation of Signaling Protein Function and Trafficking by the hsp90/hsp70-Based Chaperone Machinery. Exper. Biol. Medi. 228, 111-133 (2003)
32. Chiosis G, Vilenchik M, Kim J, Solit D: Hsp90: The vulnerable chaperone. Drug Discov. Today 9, 881-888 (2004)
33. Nathan DF, Lindquist S: Mutational analysis of Hsp90 function: interactions with a steroid receptor and a protein kinase. Mol. Cell. Biol. 15, 3917-3925 (1995)
34. Picard D, Khursheed B, Garabedian MJ, Fortin MG, Lindquist S, Yamamoto KR: Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348, 166 (1990)
35. Burrows F, Zhang H, Kamal A: Hsp90 Activation and Cell Cycle Regulation. Cell Cycle 3, 1530-1536 (2004)
36. Jackson SE, Queitsch C, Toft D: Hsp90: from structure to phenotype. Nature Struct. Mol. Biol. 11, 1152-1155 (2004)
37. Xu Y, Singer MA, Lindquist S: Maturation of the tyrosine kinase c-src as a kinase and as a substrate depends on the molecular chaperone Hsp90. Proc. Natl Acad. Sci. USA 96, 109-114 (1999)
38. Holt SE, Aisner DL, Baur J et al.: Functional requirement of p23 and Hsp90 in telomerase complexes. Genes Dev. 13, 817-826 (1999)
39. Rowlands MG, Newbatt YM, Prodromou C, Pearl LH, Workman P, Aherne W: Highthroughput screening assay for inhibitors of heat-shock protein 90 ATPase activity. Anal. Biochem. 327, 176-183 (2004)
40. Workman P: Altered states: selectively drugging the Hsp90 cancer chaperone. Trends Mol. Med. 10, 47-51 (2004)
41. Workman P: Overview: translating Hsp90 biology into Hsp90 drugs. Curr. Cancer Drug Targets 3, 297-300 (2003)
42. Uehara Y: Natural product origins of Hsp90 inhibitors. Curr. Cancer Drug Targets 3, 325-330 (2003)
43. Neckers L: Development of small molecule Hsp90 inhibitors: utilizing both forward and reverse chemical genomics for drug identification. Curr. Med. Chem. 10, 733-739 (2003)
44. Isaacs JS, Xu W, Neckers L: Heat shock protein 90 as a molecular target for cancer therapeutics. Cancer Cell 3, 213-217 (2003)
45. Whitesell L, Mimnaugh EG, De Costa B, Myers CE, Neckers LM: Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl Acad. Sci. USA 91, 8324-8328 (1994)
46. DeBoer C, Meulman PA, Wnuk RJ, Peterson DH: Geldanamycin, a new antibiotic. J. Antibiot. 23, 442-447 (1970)
47. Goetz MP, Toft DO, Ames MM, Erlichman C: The Hsp90 chaperone complex as a novel target for cancer therapy. Ann. Oncol. 14, 1169-1176 (2003)
48. Neckers L: Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol. Med. 8, S55-S61 (2002)
49. Ochel HJ, Eichhorn K, Gademann G: Geldanamycin: the prototype of a class of antitumor drugs targeting the heat shock protein 90 family of molecular chaperones. Cell Stress Chaperones 6, 105-112 (2001)
50. Neckers L, Ivy SP: Heat shock protein 90. Curr. Opin. Oncol. 15, 419-424 (2003)
51. Ivy PS, Schoenfeldt M: Clinical trials referral resource. Current clinical trials of 17-AG and 17-DMAG. Oncology 18, 610-620 (2004)
52. Jez JM, Chen JC, Rastelli G, Stroud RM, Santi DV: Crystal structure and molecular modeling of 17-DMAG in complex with human Hsp90. Chem. Biol. 10, 361-368 (2003)
53. Hostein I, Robertson D, DiStefano F, Workman P, Clarke PA: Inhibition of signal transduction by the Hsp90 inhibitor 17- allylamino-17- demethoxygeldanamycin results in cytostasis and apoptosis. Cancer Res. 61, 4003-4009 (2001)
54. Nimmanapalli R, OBryan E, Bhalla K: Geldanamycin and its analogue 17- allylamino-17-demethoxygeldanamycin lowers Bcr-Abl levels and induces apoptosis and differentiation of Bcr-Abl-positive human leukemic blasts. Cancer Res. 61, 1799-1804 (2001)
55. Schulte TW, Neckers LM: The benzoquinone ansamycin 17-allylamino-17- demethoxygeldanamycin binds to HSP90 and shares important biologic activities with geldanamycin. Cancer Chemother. Pharmacol. 42, 273-279 (1998)
56. Garbaccio RM, Stachel SJ, Baeschlin DK, Danishefsky SJ: Concise asymmetric syntheses of radicicol and monocillin I. J. Am. Chem. Soc. 123, 10903-10908 (2001)
57. Shiotsu Y, Neckers LM, Wortman I et al.: Novel oxime derivatives of radicicol induce erythroid differentiation associated with preferential G(1) phase accumulation against chronic myelogenous leukemia cells through destabilization of Bcr-Abl with Hsp90 complex. Blood 96, 2284-2291 (2000)
58. Soga S, Neckers LM, Schulte TW et al.: KF25706, a novel oxime derivative of radicicol, exhibits in vivo antitumor activity via selective depletion of Hsp90 binding signaling molecules. Cancer Res. 59, 2931-2938 (1999)
59. Chiosis G, Lucas B, Huezo H, Solit D, Basso A, Rosen N: Development of purine-scaffold small molecule inhibitors of Hsp90. Curr. Cancer Drug Targets 3, 371-376 (2003)
60. Dymock B, Barril X, Beswick M et al.: Adenine derived inhibitors of the molecular chaperone HSP90-SAR explained through multiple X-ray structures. Bioorg. Med. Chem. Lett. 14, 325-328 (2004)
61. Marcu MG, Neckers LM: The C-terminal half of heat shock protein 90 represents a second site for pharmacologic intervention in chaperone function. Curr. Cancer Drug Targets 3, 343-347 (2003)
62. Beliakoff J, Bagatell R, Paine-Murrieta G, Taylor CW, Lykkesfeldt AE, Whitesell L: Hormone-refractory breast cancer remains sensitive to the antitumor activity of heat shock protein 90 inhibitors. Clin. Cancer Res. 9, 4961-4971 (2003)
63. Solit DB, Scher HI, Rosen N: Hsp90 as a therapeutic target in prostate cancer. Semin. Oncol. 30, 709-716 (2003)
64. Altieri DC: Coupling apoptosis resistance to the cellular stress response: the IAP-Hsp90 connection in cancer. Cell Cycle 3, 255-256 (2004)
65. Zhang H, Burrows F: Targeting multiple signal transduction pathways through inhibition of Hsp90. J. Mol. Med. 82, 488-496 (2004)
66. Fortugno P, Beltrami E, Plescia J et al.: Regulation of survivin function by Hsp90. Proc. Natl Acad. Sci. USA 100, 13791-13796 (2003)
67. Takayama S, Reed JC, Homma S: Heatshock proteins as regulators of apoptosis. Oncogene 22, 9041-9047 (2003)
68. Thompson JE, Thompson CB: Putting the Rap on Akt. J. Clin. Oncol. 22, 4217-4226 (2004)
69. Basso AD, Solit DB, Munster PN, Rosen N: Ansamycin antibiotics inhibit Akt activation and cyclin D expression in breast cancer cells that overexpress HER2. Oncogene 21, 1159-1166 (2002)
70. Solit DB, Basso AD, Olshen AB, Scher HI, Rosen N: Inhibition of heat shock protein 90 function down-regulates Akt kinase and sensitizes tumors to Taxol. Cancer Res. 63, 2139-2144 (2003)
71. Sato S, Fujita N, Tsuruo T: Modulation of Akt kinase activity by binding to Hsp90. Proc. Natl Acad. Sci. USA 97, 10832-10837 (2000)
72. Muise-Helmericks RC, Grimes HL, Bellacosa A, Malstrom SE, Tsichlis PN, Rosen N: Cyclin D expression is controlled posttranscriptionally via a phosphatidylinositol 3- kinase/Akt-dependent pathway. J. Biol. Chem. 273, 29864-29872 (1998)
73. Schulte TW, Blagosklonny MV, Ingui C, Neckers L: Disruption of the Raf-1-Hsp90 molecular complex results in destabilization of Raf-1 and loss of Raf-1-Ras association. J. Biol. Chem. 270, 24585-24588 (1995)
74. Stancato LF, Chow YH, Hutchison KA, Perdew GH, Jove R, Pratt WB: Raf exists in a native heterocomplex with hsp90 and p50 that can be reconstituted in a cell-free system. J. Biol. Chem. 268, 21711-21716 (1993)
75. Stancato LF, Silverstein AM, Owens-Grillo JK, Chow YH, Jove R, Pratt WB: The hsp90- binding antibiotic geldanamycin decreases Raf levels and epidermal growth factor signaling without disrupting formation of signaling complexes or reducing the specific enzymatic activity of Raf kinase. J. Biol. Chem. 272, 4013-4020 (1997)
76. Schulte TW, An WG, Neckers LM: Geldanamycin-induced destabilization of Raf-1 involves the proteasome. Biochem. Biophys. Res. Commun. 239, 655-659 (1997)
77. Chen G, Cao P, Goeddel DV: TNF-induced recruitment and activation of the IKK complex require Cdc37 and Hsp90. Mol. Cell. 9, 401-410 (2002)
78. Broemer M, Krappmann D, Scheidereit C: Requirement of Hsp90 activity for IB kinase (IKK) biosynthesis and for constitutive and inducible IKK and NF-B activation. Oncogene 23, 5378 (2004)
79. Lewis J, Devin A, Miller A 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-B activation. J. Biol. Chem. 275, 10519-10526 (2000)
80. Bagatell R, Beliakoff J, David CL, Marron MT, Whitesell L: Hsp90 inhibitors deplete key anti-apoptotic proteins in pediatric solid tumor cells and demonstrate synergistic anticancer activity with cisplatin. Int. J. Cancer 113, 179-188 (2005)
81. Workman P: Combinatorial attack on multistep oncogenesis by inhibiting the Hsp90 molecular chaperone. Cancer Lett. 206,149-157 (2004)
82. Calabrese C, Frank A, Maclean K, Gilbertson R: Medulloblastoma sensitivity to 17- allylamino-17-demethoxygeldanamycin requires MEK/ERKM. J. Biol. Chem. 278, 24951-24959 (2003)
83. Nomura M, Nomura N, Newcomb EW, Lukyanov Y, Tamasdan C, Zagzag D: Geldanamycin induces mitotic catastrophe and subsequent apoptosis in human glioma cells. J. Cell. Physiol. 201, 374-384 (2004)
84. Bisht KS, Bradbury CM, Mattson D et al.: Geldanamycin and 17-allylamino-17- demethoxygeldanamycin potentiate the in vitro and in vivo radiation response of cervical tumor cells via the heat shock protein 90-mediated intracellular signaling and cytotoxicity. Cancer Res. 63, 8984-8995 (2003)
85. Mitsiades N, Mitsiades CS, Poulaki V et al.: Molecular sequelae of proteasome inhibition in human multiple myeloma cells. Proc. Natl Acad. Sci. USA 99, 14374-14379 (2002)
86. Rahmani M, Yu C, Dai Y et al.: Coadministration of the heat shock protein 90 antagonist 17-allylamino- 17- demethoxygeldanamycin with suberoylanilide hydroxamic acid or sodium butyrate synergistically induces apoptosis in human leukemia cells. Cancer Res. 63, 8420-8427 (2003)
87. George P, Bali P, Annavarapu S et al.: Combination of histone deacetylase inhibitor LBH589 and the hsp90 inhibitor 17-AAG is highly active against human CML-BC cells and AML cells with activating mutation of FLT-3. Blood 105(4), 1768-1776 (2004)
88. Nimmanapalli R, OBryan E, Kuhn D, Yamaguchi H, Wang HG, Bhalla KN: Regulation of 17-AAG-induced apoptosis: role of Bcl-2, Bcl-XL, and Bax downstream of 17- AAG-mediated down-regulation of Akt, Raf- 1, and Src kinases. Blood 102, 269-275 (2003)
89. Le Boeuf F, Houle F, Huot J: Regulation of vascular endothelial growth factor receptor 2- mediated phosphorylation of focal adhesion kinase by heat shock protein 90 and Src kinase activities. J. Biol. Chem. 279, 39175-39185 (2004)
90. Selkirk JK, Merrick BA, Stackhouse BL, He C: Multiple p53 protein isoforms and formation of oligomeric complexes with heat shock proteins Hsp70 and Hsp90 in the human mammary tumor, T47D, cell line. Appl. Theor. Electrophor. 4, 11-18 (1994)
91. Pandey P, Saleh A, Nakazawa A et al.: Negative regulation of cytochrome c-mediated oligomerization of Apaf-1 and activation of procaspase-9 by heat shock protein 90. Embo. J. 19, 4310-4322 (2000)
92. Wartmann M, Davis RJ: The native structure of the activated Raf protein kinase is a membrane-bound multi-subunit complex. J. Biol. Chem. 269, 6695-6701(1994)
93. Ali A, Bharadwaj S, OCarroll R, Ovsenek N: HSP90 interacts with and regulates the activity of heat shock factor 1 in Xenopus oocytes. Mol. Cell Biol. 18, 4949-4960 (1998)
94. Munoz MJ, Jimenez J: Genetic interactions between Hsp90 and the Cdc2 mitotic machinery in the fission yeast Schizosaccharomyces pombe. Mol. Gen. Genet. 261, 242-250 (1999)
95. Dai K, Kobayashi R, Beach D: Physical interaction of mammalian CDC37 with CDK4. J. Biol. Chem. 271, 22030-22034 (1996)
96. Stepanova L, Leng X, Parker SB, Harper JW: Mammalian p50Cdc37 is a protein kinasetargeting subunit of Hsp90 that binds and stabilizes Cdk4. Genes Dev. 10, 1491-1502 (1996)
97. Mahony D, Parry DA, Lees E: Active cdk6 complexes are predominantly nuclear and represent only a minority of the cdk6 in T cells. Oncogene 16, 603-611 (1998)
98. OKeeffe B, Fong Y, Chen D, Zhou S, Zhou Q: Requirement for a kinase-specific chaperone pathway in the production of a Cdk9/cyclin T1 heterodimer responsible for PTEFb- mediated tat stimulation of HIV-1 transcription. J. Biol. Chem. 275, 279-287 (2000)
99. Zheng FF, Kuduk SD, Chiosis G et al.: Identification of a geldanamycin dimer that induces the selective degradation of HERfamily tyrosine kinases. Cancer Res. 60, 2090-2094 (2000)
100. Minet E, Mottet D, Michel G et al.: Hypoxiainduced activation of HIF-1: role of HIF- 1alpha-Hsp90 interaction. FEBS Lett. 460, 251-256 (1999)
101. Gradin K, McGuire J, Wenger RH et al.: Functional interference between hypoxia and dioxin signal transduction pathways: competition for recruitment of the Arnt transcription factor. Mol. Cell Biol. 16, 5221-5231 (1996)
102. 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. J. Biol. Chem. 276, 3702-3708 (2001)
103. Itoh H, Ogura M, Komatsuda A, Wakui H, Miura AB, Tashima Y: A novel chaperoneactivity- reducing mechanism of the 90-kDa molecular chaperone HSP90. Biochem. J. 343 (Pt 3), 697-703 (1999).