Hsp90 inhibitors deplete key anti-apoptotic proteins in pediatric solid tumor cells and demonstrate synergistic anticancer activity with cisplatin

International Journal of Cancer

Volumn 113, Issue 2, 2005, Pages 179-188

  Bagatell, Rochelle ^a,b   Beliakoff, Jason ^a   David, Cynthia L ^a   Marron, Marilyn T ^a   Whitesell, Luke ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Geldanamycin; Heat shock protein; Neuroblastoma; Osteosarcoma

Indexed keywords

CISPLATIN; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; PROTEIN INHIBITOR; PROTEIN KINASE B; SOMATOMEDIN C RECEPTOR;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER SURVIVAL; CELL PROLIFERATION; CELL PROTECTION; CHILDHOOD CANCER; CONTROLLED STUDY; DRUG EXPOSURE; DRUG INHIBITION; HEAT SHOCK RESPONSE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NEUROBLASTOMA; NEUROBLASTOMA CELL; NICK END LABELING; OSTEOSARCOMA; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; SOLID TUMOR; WILD TYPE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZOQUINONES; BONE NEOPLASMS; CELL PROLIFERATION; CELL SURVIVAL; CHILD; CISPLATIN; DNA DAMAGE; ENZYME INHIBITORS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOBLOTTING; IN SITU NICK-END LABELING; LACTAMS, MACROCYCLIC; NEUROBLASTOMA; OSTEOSARCOMA; QUINONES; TUMOR CELLS, CULTURED;

EID: 10344225631     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.20611     Document Type: Article

References (50)

1. Bagatell R, Khan O, Paine-Murrieta G, Taylor CW, Akinaga S, Whitesell L. Destabilization of steroid receptors by Hsp90-binding drugs: a ligand independent approach to hormonal therapy of breast cancer. Clin Cancer Res 2001;7:2076-84.
2. Banerji U, O'Donnell A, Scurr M, Benson C, Hanwell J, Clark S, Raynaud S, Turner A, Walton M, Workman P, Judson I. Phase I trial of the heat shock protein 90 (HSP90) inhibitor 17-allylamino 17-demethoxygeldanamycin (17AAG). Pharmacokinetic (PK) profile and pharmacodynamic (PD) endpoints. Proc Am Soc Clin Oncol 2001;20:326.
3. Goetz MP, Toft DO, Ames MM, Erlichman C. The Hsp90 chaperone complex as a novel target for cancer therapy. Ann Oncol 2003;14:1169-76.
4. Maloney A, Workman P. Hsp90 as a new therapeutic target for cancer therapy: the story unfolds. Expert Opin Biol Ther 2002; 2: 3-24.
5. Ivy SP, Lugo TG, Bernstein ML, Smith MA. Evolving molecular and targeted strategies. In: Pizzo PA, Poplack DG, eds. Principles and practice of pediatric oncology, 4th ed. Philadelphia: Lippincott Williams and Wilkins, 2002. 309-49.
6. 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 2003;9:4961-71.
7. Whitesell L, Shifrin SD, Schwab G, Neckers LM. Benzoquinonoid ansamycins possess selective tumoricidal activity unrelated to src kinase inhibition. Cancer Res 1992;52:1721-8.
8. Chou T-C, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. In: Weber G, ed. Advances in enzyme regulation. vol 22. New York: Pergamon Press, 1983. 27-55.
9. Liu X, Turbyville T, Fritz A, Whitesell L. Inhibition of insulin-like growth factor I receptor expression in neuroblastoma cells induces the regression of established tumors in mice. Cancer Res 1998;58:5432-8.
10. Egorin MJ, Zuhowski EG, Rosen DM, Sentz DL, Covey JM, Eiseman JL. Plasma pharmacokinetics and tissue distribution of 17-(Allylamino)-17- demethoxygeldanamycin (NSC 330507) in CD2F1 micel. Cancer Chemother Pharmacol 2001;47:291-302.
11. Sausville EA, Tomaszewski JE, Ivy P. Clinical development of 17-allylamino, 17-demethoxygeldanamycin. Cur Cancer Drug Targets 2003;3:377-83.
12. Bagatell R, Paine-Murrieta G, Taylor C, Pulcini E, Akinaga S, Benjamin I, Whitesell L. Induction of a heat shock factor 1-dependent stress response alters the cytotoxic activity of Hsp90 binding agents. Clin Cancer Res 2000;6:3312-8.
13. Wilson RH, Takimoto CH, Agnew EB, Morrison G, Grollman F, Thomas RR, Saif MW, Allegra C, Grochow L, Szabo E, Hamilton JM, Monahan BP, et al. Phase I pharmacologic study of 17-(Allylamino)-17-demethoxygeldanamycin (AAG) in adult patients with advanced solid tumors. Proc Am Soc Clin Oncol 2001;20:325.
14. Banerji U, O'Donnell A, Scurr M, Benson C, Stapleton S, Raynaud F, Clarke S, Turner A, Workman P, Judson I, Block E. A pharmacokinetically (PK)-pharmacodynamically (PD) guided phase I trial of the heat shock protein 90 (HSP90) inhibitor 17-allylamino, 17-demethoxygeldanamycin (17AAG) Am Soc Clin Oncol Meeting Proceedings 2003;22:199.
15. Munster PN, Srethapakdi M, Moasser MM, Rosen N. Inhibition of heat shock protein 90 function by ansamycins causes the morphological and functional differentiation of breast cancer cells. Cancer Res 2001;7:2945-52.
16. Munster PN, Basso A, Solit D, Norton L, Rosen N. Modulation of Hsp90 function by ansamycins sensitizes breast cancer cells to chemotherapy-induced apoptosis in an RB- and schedule-dependent manner. Clin Cancer Res 2001;7:2228-36.
17. Shew JY, Lin BT, Chen PL, Tseng BY, Yang-Feng TL, Lee WH. C-terminal truncation of the retinoblastoma gene product leads to functional inactivation. Proc Natl Acad Sci USA 1990;87:6-10.
18. Itoh H, Ogura M, Komatsuda A, Wakui H, Miura A, Tashima Y. A novel chaperone-activity-reducing mechanism of the 90-kDa molecular chaperone HSP90. Biochem J 1999;343:697-703.
19. Soti C, Racz A, Csermely P. A nucleotide-dependent molecular switch controls ATP binding at the C-terminal domain of Hsp90. J Biol Chem 2002;277:7066-75.
20. Nardai G, Sass B, Eber J, Orosz G, Csermely P. Reactive cysteines of the 90-kDa heat shock protein, Hsp90. Arch Biochem Biophys 2000;384:59-67.
21. Csermely P, Schnaider T, Soti C, Prohaskka Z, Nardai G. The 90-kDa molecular chaperone family: Structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 1998;79:129-68.
22. Pratt WB. The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proc Soc Exp Biol Med 1998;217:420-31.
23. Stebbins CE, Russo AA, Schneider C, Rosen N, Hartl FU, Pavletich NP. Crystal structure of an hsp90-geldanamycin complex: Targeting of a protein chaperone by an anti-tumor agent. Cell 1997;89:239-50.
24. Roe SM, Prodromou C, O'Brien R, Ladbury JE, Piper PW, Pearl LH. Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicola and geldanamycin. J Med Chem 1999;42:260-6.
25. Grenert JP, Sullivan WP, Fadden P, Haystead TAJ, Clark J, Mimnaugh E, Krutzsch H, Ochel H-J, Schulte TW, Sausville E, Neckers LM, Toft DO. The ammo-terminal domain of heat shock protein 90 (hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates hsp90 conformation. J Biol Chem 1997;272:23843-50.
26. Schulte TW, Akinaga S, Soga S, Sullivan W, Stensgard B, Toft D, Neckers L. Antibiotic radicicola binds to the N-terminal domain of Hsp90 and shares important biologic activities with geldanamycin. Cell Stress Chaperones 1998;3:100-8.
27. Whitesell L, Sutphin P, An WG, Schulte T, Blagosklonny MV, Neckers L. Geldanamycin-stimulated destabilization of mutated p53 is mediated by the proteasome in vivo. Oncogene 1997;14:2809-6.
28. Neckers L, Schulte T, Mimnaugh E. Geldanamycin as a potential anti-cancer agent: its molecular target and biochemical activity. Invest New Drugs 1999;17:361-73.
29. Kamal A, Thao L, Sensintaffar J, Zhang L, Boehm MF, Fritz LC, Burrows FJ. A high affinity conformation of Hsp90 confers tumor selectivity on Hsp90 inhibitors. Nature 2003;425:407-10.
30. Kim HR, Kang HS, Kim HD. Geldanamycin induces heat shock protein expression through activation of HSF1 in K562 erythroleukemic cells. IUBMB Life 1999;48:429-33.
31. van Golen CM, Castle VP, Feldman EL. IGF-1 receptor activation and BCL-2 overexpression prevent early apoptotic events in human neuroblastoma. Cell Death Differ 2000;7:654-65.
32. Singleton JR, Randolph AE, Feldman EL. Insulin-like growth factor I receptor prevents apoptosis and enhances neuroblastoma tumorigenesis. Cancer Res 1996;56:4522-9.
33. Zumkeller W, Schwab M. Insulin-like growth factor system in neuroblastoma tumorigenesis and apoptosis: potential diagnostic and therapeutic perspectives. Horm Metab Res 1999;31:138-41.
34. Teitz T, Wei T, Valentine MB, Vanin EF, Grenet J, Valentine VA, Behm FG, Look AT, Lahti JM, Kidd VJ. Caspase 8 is deleted or silenced preferentially in childhood neuroblastomas with amplification of MYCN. Nat Med 2000;6:529-35.
35. Sollars V, Lu X, Xiao L, Wang X, Garfinkel MD, Ruden DM. Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nat Genet 2003;33:70-4.
36. Siddick ZH. Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene 2003;22:7265-79.
37. Vasilevskaya IA, Rakitina TV, O'Dwyer PJ. Geldanamycin and its 17-allylamino-17-demethoxy analogue antagonize the action of Cisplatin in human colon adenocarcinoma cells: differential caspase activation as a basis for interaction. Cancer Res 2003;63:3241-6.
38. McCollum A, Toft DO, Erlichman C. Geldanamycin enhances cisplatin cytotoxicity through loss of Akt activation in A549 cells. Clin Cancer Res 2003;9:6178s.
39. Sato S, Fujita N, Tsuruo T. Modulation of Akt kinase activity by binding to Hsp90. Proc Natl Acad Sci USA 2000;97:10832-7.
40. Meyer P, Prodromou C, Hu B, Vaughan C, Roe SM, Panaretou B, Piper PW, Peal LH. Structural and functional analysis of the middle segment of hsp90: implications for ATP hydrolysis and client protein and cochaperone interactions. Mol Cell 2003;11:647-58.
41. Scheibel T, Weikl T, Buchner J. Two chaperone sites in Hsp90 differing in substrate specificity and ATP dependence. Proc Natl Acad Sci USA 1998;95:1495-9.
42. Young JC, Schneider C, Hartl FU. In vitro evidence that Hsp90 contains two independent chaperone sites. FEBS Lett 1997;418:139-43.
43. Zou J, Guo Y, Guettouche T, Smith DF, Voellmy R. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 1998;94:471-80.
44. Obermann WM, Sondermann H, Russo AA, Pavletich NP, Hartl FU. In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J Cell Biol 1998;143:901-10.
45. 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 1997;272:4013-20.
46. Solit DB, Zheng FF, Drobnjak M, Munster PN, Higgins B, Verbel D, Heller G, Tong W, Cordon-Cardo C, Agus DB, Scher HI, Rosen N. 17-Allylamino-17- demethoxygeldanamycin induces the degradation of androgen receptor and HER-2/neu and inhibits the growth of prostate cancer xenografts. Clin Cancer Res 2002;8:986-93.
47. Schulte TW, Blagosklonny MV, Romanova L, Mushinski JF, Monia BP, Johnston JF, Nguyen P, Trepel J, Neckers LM. Destabilization of Raf-1 by geldanamycin leads to disruption of the Raf-1-MEK-mitogen-activated protein kinase signaling pathway. Mol Cell Biol 1996;16:5839-45.
48. 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 2003;63:2139-44.
49. Cianfarani S, Rossi P. Neuroblastoma and insulin-like growth factor system. New insights and clinical perspectives. Eur J Pediatr 1997;156:256-61.
50. Kim S, Kang J, Hu W, Evers BM, Chung DH. Geldanamycin decreases Raf-1 and Akt levels and induces apoptosis in neuroblastomas. Int J Cancer 2003;103:352-9.