Hormone-Refractory Breast Cancer Remains Sensitive to the Antitumor Activity of Heat Shock Protein 90 Inhibitors

Clinical Cancer Research

Volumn 9, Issue 13, 2003, Pages 4961-4971

  Beliakoff, Jason ^a   Bagatell, Rochelle ^a   Paine Murrieta, Gillian ^b   Taylor, Charles W ^b   Lykkesfeldt, Anne E ^c   Whitesell, Luke ^a,d  

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

^b UNIVERSITY OF ARIZONA   (United States)

^c DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^d UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

17 ALLYLAMINO 17 DEMETHOXYGELDANAMYCIN; ANTIESTROGEN; CHAPERONE; ESTROGEN RECEPTOR; FULVESTRANT; GELDANAMYCIN; GLUCOCORTICOID RECEPTOR; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; N BUTYL 11 (3,17BETA DIHYDROXYESTRA 1,3,5(10) TRIEN 7ALPHA YL) N METHYLUNDECANAMIDE; PROTEIN KINASE B; RAF PROTEIN; TAMOXIFEN; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER HORMONE THERAPY; CANCER PATIENT; CELL STRAIN MCF 7; GROWTH INHIBITION; HORMONE RESPONSE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LASER MICROSCOPY; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR XENOGRAFT;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BENZOQUINONES; BREAST NEOPLASMS; CELL LINE, TUMOR; COLLAGEN; DRUG COMBINATIONS; ESTROGENS; GENES, REPORTER; HORMONES; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOBLOTTING; LACTAMS, MACROCYCLIC; LAMININ; LASERS; LIGANDS; MICE; MICE, SCID; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; NEOPLASM TRANSPLANTATION; PRECIPITIN TESTS; PROTEOGLYCANS; QUINONES; RECEPTORS, ESTROGEN; RIFABUTIN; SIGNAL TRANSDUCTION; TIME FACTORS; TRANS-ACTIVATION (GENETICS);

EID: 0142188139     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

1. Johnston, S. R. Acquired tamoxifen resistance in human breast cancer: potential mechanisms and clinical implications. Anti-Cancer Drugs, 8: 911-930, 1997.
2. Graham, J. D., Bain, D. L., Richer, J. K., Jackson, T. A., Tung, L., and Horwitz, K. B. Nuclear receptor conformation, coregulators, and tamoxifen-resistant breast cancer. Steroids, 65: 579-584, 2000.
3. Osborne, C. K., and Fuqua, S. A. Mechanisms of tamoxifen resistance. Breast Cancer Res. Treat., 32: 49-55, 1994.
4. Johnston, S. R. Endocrine manipulation in advanced breast cancer: recent advances with SERM therapies. Clin. Cancer Res., 7 (Suppl.): 4376s-4387s, 2001.
5. Lykkesfeldt, A. E., Madsen, M. W., and Briand, P. Altered expression of estrogen-regulated genes in a tamoxifen-resistant and ICI 164,384- and ICI 182,780-sensitive human breast cancer cell line, MCF-7/TAMR-1. Cancer Res., 54: 1587-1595, 1994.
6. Wakeling, A. E. Are breast tumours resistant to tamoxifen also resistant to pure antioestrogens?. J. Steroid Biochem. Mol. Biol., 47: 107-114, 1993.
7. Lykkesfeldt, A. E., Larsen, S. S., and Briand, P. Human breast cancer cell lines resistant to pure anti-estrogens are sensitive to tamoxifen treatment. Int. J. Cancer, 61: 529-534, 1995.
8. Bagatell, R., Khan, O., Paine-Murrieta, G., Taylor, C. W., Akinaga, S., and Whitesell, L. Destabilization of steroid receptors by Hsp90-binding drugs: a ligand independent approach to hormonal therapy of breast cancer. Clin. Cancer Res., 7: 2076-2084, 2001.
9. Pratt, W. B., and Toft, D. O. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev., 18: 306-360, 1997.
10. Pratt, W. B. The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proc. Soc. Exp. Biol. Med., 217: 420-434, 1998.
11. Smith, D. F. Dynamics of heat shock protein 90-progesterone receptor binding and the disactivation loop model for steroid receptor complexes. Mol. Endocrinol., 7: 1418-1429, 1993.
12. Osborne, C. K., Schiff, R., Fuqua, S. A., and Shou, J. Estrogen receptor: current understanding of its activation and modulation. Clin. Cancer Res., 7 (Suppl.): 4338s-4342s; discussion 4411s-4412s, 2001.
13. Segnitz, B., and Gehring, U. The function of steroid hormone receptors is inhibited by the hsp90-specific compound geldanamycin. J. Biol. Chem., 272: 18694-18701, 1997.
14. Maloney, A., and Workman, P. Hsp90 as a new therapeutic target for cancer therapy: the story unfolds. Exp. Opin. Biol. Ther., 2: 3-24, 2002.
15. Neckers, L. Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol. Med., 8: S55-S61, 2002.
16. Banerji, U., O'Donnell, A., Scurr, M., Benson, C., Hanwell, J., Clark, S., Raynaud, F., Turner, A., Walton, M., Workman, P., and 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., 20: 326, 2001.
17. Erlichman, C., Toft, D. O., Reid, J., Sloan, J., Atherton, P., Adjei, A., Ames, M., and Croghan, G. A Phase I trial of 17-allyl-amino-geldanamycin in patients with advanced cancer. Proc. Am. Assoc. Cancer Res., 42: 4474, 2001.
18. Munster, P. N., Tong, W., Schwartz, L., Larson, S., Kenneson, K., De La Cruz, A., Rosen, N., and Scher, H. Phase 1 trial of 17-(allylamino)-17-demethoxygeldanamycin (17-AAG) in patients with advanced malignancies. Proc. Am. Soc. Clin. Oncol., 20: 327, 2001.
19. Wilson, R. H., Takimoto, C. H., Agnew, E. B., Morrison, G., Grollman, F., Thomas, R. R., Saif, M. W., Allegra, C., Grochow, L., Szabo, E., Hamilton, J. M., Monahan, B. P., Neckers, L., and Grem, J. L. Phase I pharmacologic study of 17-(allylamino)-17-demethoxygeldanamycin (AAG) in adult patients with advanced solid tumors. Proc. Am. Soc. Clin. Oncol., 20: 325, 2001.
20. Smith, D. F., Whitesell, L., Nair, S. C., Chen, S., Prapapanich, V., and Rimerman, R. A. Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent. Mol. Cell. Biol., 15: 6804-6812, 1995.
21. Solit, D. B., Zheng, F. F., Drobnjak, M., Munster, P. N., Higgins, B., Verbel, D., Heller, G., Tong, W., Cordon-Cardo, C., Agus, D. B., Scher, H. I., and 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., 8: 986-993, 2002.
22. Vanaja, D. K., Mitchell, S. H., Toft, D. O., and Young, C. Y. Effect of geldanamycin on androgen receptor function and stability. Cell Stress Chaperones, 7: 55-64, 2002.
23. Whitesell, L., and Cook, P. Stable and specific binding of heat shock protein 90 by geldanamycin disrupts glucocorticoid receptor function in intact cells. Mol. Endocrinol., 10: 705-712, 1996.
24. Anderson, I., Bartley, C. R., Lerch, R. A., Gray, W. G. N., Friesen, P. D., and Gorski, J. Estrogen receptor α requires no accessory factors for high affinity binding to a consensus response element. Biochemistry, 37: 17287-17298, 1998.
25. Fliss, A. E., Benzeno, S., Rao, J., and Caplan, A. J. Control of estrogen receptor ligand binding by Hsp90. J. Steroid Biochem. Mol. Biol., 72: 223-230, 2000.
26. Lee, M. O., Kim, E. O., Kwon, H. J., Kim, Y. M., Kang, H. J., Kang, H., and Lee, J. E. Radicicol represses the transcriptional function of the estrogen receptor by suppressing the stabilization of the receptor by heat shock protein 90. Mol. Cell. Endocrinol., 188: 47-54, 2002.
27. Madsen, M. W., Reiter, B. E., Larsen. S. S., Briand, P., and Lykkesfeldt, A. E. Estrogen receptor messenger RNA splice variants are not involved in antiestrogen resistance in sublines of MCF-7 human breast cancer cells. Cancer Res., 57: 585-589, 1997.
28. Tzukerman, M. T., Esty, A., Santiso-Mere, D., Danielian, P., Parker, M. G., Stein, R. B., Pike, J. W., and McDonnell, D. P. Human estrogen receptor transactivational capacity is determined by both cellular and promoter context and mediated by two functionally distinct intramolecular regions. Mol. Endocrinol., 8: 21-30, 1994.
29. Whitesell, L., Sutphin, P. D., Pulcini, E. J., Martinez, J. D., and Cook, P. H. The physical association of multiple molecular chaperone proteins with mutant p53 is altered by geldanamycin, an hsp90-binding agent. Mol. Cell. Biol., 18: 1517-1524, 1998.
30. Darzynkiewicz, Z., Bedner, E., Li, X., Gorczyca, W., and Melamed, M. Laser-scanning cytometry: a new instrumentation with many applications. Exp. Cell Res., 249: 1-12, 1999.
31. Kamentsky, L., Burger, D., Gershman, R., Kamentsky, L., and Luther, E. Slide-based laser scanning cytometry. Acta Cytol., 41: 124-143, 1997.
32. Madsen, M. W., Reiter, B. E., and Lykkesfeldt, A. E. Differential expression of estrogen receptor mRNA splice variants in the tamoxifen resistant human breast cancer cell line, MCF-7/TAMR-1 compared to the parental MCF-7 cell line. Mol. Cell. Endocrinol., 109: 197-207, 1995.
33. Horwitz, K. B., and McGuire, W. L. Nuclear mechanisms of estrogen action. Effects of estradiol and anti-estrogens on estrogen receptors and nuclear receptor processing. J. Biol. Chem., 253: 8185-8191, 1978.
34. Borras, M., Laios, I., el Khissiin, A., Seo, H. S., Lempereur, F., Legros, N., and Leclercq, G. Estrogenic and antiestrogenic regulation of the half-life of covalently labeled estrogen receptor in MCF-7 breast cancer cells. J. Steroid Biochem. Mol. Biol., 57: 203-213, 1996.
35. Saceda, M., Lippman, M. E., Chambon, P., Lindsey, R. L., Ponglikitmongkol, M., Puente, M., and Martin, M. B. Regulation of the estrogen receptor in MCF-7 cells by estradiol. Mol. Endocrinol., 2: 1157-1162, 1988.
36. Jensen, B. L., Skouv, J., Lundholt, B. K., and Lykkesfeldt, A. E. Differential regulation of specific genes in MCF-7 and the ICI 182780-resistant cell line MCF-7/182R-6. Br. J. Cancer, 79: 386-392, 1999.
37. McDonnell, D. P., Clemm, D. L., Hermann, T., Goldman, M. E., and Pike, J. W. Analysis of estrogen receptor function in vitro reveals three distinct classes of antiestrogens. Mol. Endocrinol., 9: 659-669, 1995,
38. Schiff, R., Massarweh, S., Shou, J., and Osborne, C. K. Breast cancer endocrine resistance: how growth factor signaling and estrogen receptor coregulators modulate response. Clin. Cancer Res., 9 (Suppl.): 447s-454s, 2003.
39. Bachleitner-Hofmann, T., Pichler-Gebhard, B., Rudas, M., Gnant, M., Taucher, S., Kandioler, D., Janschek, E., Dubsky, P., Roka, S., Sporn, E., and Jakesz, R. Pattern of hormone receptor status of secondary contralateral breast cancers in patients receiving adjuvant tamoxifen. Clin. Cancer Res., 8: 3427-3432, 2002.
40. Howell, A., DeFriend, D., Robertson, J., Blamey, R., and Walton, P. Response to a specific antioestrogen (ICI 182780) in tamoxifen-resistant breast cancer. Lancet. 345: 29-30, 1995.
41. Buzdar, A. U., Come, S. E., Brodie, A., Ellis, M., Goss, P. E., Ingle, J. N., Johnston, S. R., Lee, A. V., Osborne, C. K., Vogel, V. G., and Hart, C. S. Proceedings of the First International Conference on Recent Advances and Future Directions in Endocrine Therapy for Breast Cancer: summary consensus statement. Clin. Cancer Res., 7 (Suppl.): 4335s-4337s, 2001.
42. Johnston, S. R. D., Head, J., Pancholi, S., Detre, S., Martin, L-A., Smith, I. E., and Dowsett, M. Integration of signal transduction inhibitors with endocrine therapy: an approach to overcoming hormone resitance in breast cancer. Clin. Cancer Res., 9 (Suppl.): 524s-532s, 2003.
43. Smith, D. F., Whitesell, L., and Katsanis, E. Molecular chaperones: biology and prospects for pharmacological intervention. Pharmacol. Rev., 50: 493-513, 1998.
44. Clarke, P. A., Hostein, I., Banerji, U., Stefano, F. D., Maloney, A., Walton, M., Judson, I., and Workman, P. Gene expression profiling of human colon cancer cells following inhibition of signal transduction by 17-allylamino-17-demethoxygeldanamycin, an inhibitor of the hsp90 molecular chaperone. Oncogene, 19: 4125-4133, 2000.
45. El-Ashry, D., Miller, D. L., Kharbanda, S., Lippman, M. E., and Kern, F. G. Constitutive Raf-1 kinase activity in breast cancer cells induces both estrogen-independent growth and apoptosis. Oncogene, 15: 423-435, 1997.
46. Ahmad, S., Singh, N., and Glazer, R. I. Role of AKT1 in 17β-estradiol- and insulin-like growth factor I (IGF-I)-dependent proliferation and prevention of apoptosis in MCF-7 breast carcinoma cells. Biochem. Pharmacol., 58: 425-430, 1999.
47. Schulte, T. W., Blagosklonny, M. V., Ingui, C., and 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.
48. Sato, S., Fujita, N., and Tsuruo, T. Modulation of Akt kinase activity by binding to Hsp90. Proc. Natl. Acad. Sci. USA, 97: 10832-10837, 2000.
49. Dardes, R. C., O'Regan R. M., Gajdos, C., Robinson, S. P., Bentrem, D., De Los Reyes, A., and Jordan V. C. Effects of a new clinically relevant antiestrogen (GW5638) related to tamoxifen on breast and endometrial cancer growth in vivo. Clin. Cancer Res., 8: 1995-2001, 2002.
50. Shiau, A. K., Barstad, D., Loria, P. M., Cheng, L., Kushner, P. J., Agard, D. A., and Greene, G. L. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell. 95: 927-937, 1998.
51. Pearce, S. T., Liu, H., and Jordan, V. C. Modulation of estrogen receptor α function and stability by tamoxifen and a critical amino acid (Asp-538) in helix 12. J. Biol. Chem., 278: 7630-7638, 2003.
52. Wijayaratne, A. L., and McDonnell, D. P. The human estrogen receptor-α is a ubiquitinated protein whose stability is affected differentially by agonists, antagonists, and selective estrogen receptor modulators. J. Biol. Chem., 276: 35684-35692, 2001.
53. Munster, P. N., Marchion, D. C., Basso, A. D., and Rosen, N. Degradation of HER2 by ansamycins induces growth arrest and apoptosis in cells with HER2 overexpression via a HER3, phosphatidylinositol 3′-kinase-AKT-dependent pathway. Cancer Res., 62: 3132-3137, 2002.
54. Howell, A., Robertson, J. F., Quaresma Albano, J., Aschermannova, A., Mauriac, L., Kleeberg, U. R., Vergote, I., Erikstein, B., Webster, A., and Morris, C. Fulvestrant, formerly ICI 182,780, is as effective as anastrozole in postmenopausal women with advanced breast cancer progressing after prior endocrine treatment. J. Clin. Oncol., 20: 3396-3403, 2002.
55. Osborne, C. K., Pippen, J., Jones, S. E., Parker, L. M., Ellis, M., Come, S., Gertler, S. Z., May, J. T., Burton, G., Dimery, I., Webster, A., Morris, C., Elledge, R., and Buzdar, A. Double-blind, randomized trial comparing the efficacy and tolerability of fulvestrant versus anastrozole in postmenopausal women with advanced breast cancer progressing on prior endocrine therapy: results of a North American trial. J. Clin. Oncol., 20: 3386-3395, 2002.