Inhibition of heat shock protein 90 (HSP90) as a therapeutic strategy for the treatment of myeloma and other cancers

British Journal of Haematology

Volumn 152, Issue 4, 2011, Pages 367-379

  Richardson, Paul G ^a   Mitsiades, Constantine S ^a   Laubach, Jacob P ^a   Lonial, Sagar ^b   Chanan Khan, Asher A ^c   Anderson, Kenneth C ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b EMORY UNIVERSITY   (United States)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Cancer; Heat shock protein 90; Myeloma; Peripheral neuropathy; Tanespimycin

Indexed keywords

ANTINEOPLASTIC AGENT; ASPARTATE AMINOTRANSFERASE; AUY 922; BORTEZOMIB; CARMUSTINE; CHAPERONE; CYCLOPHOSPHAMIDE; CYTOTOXIC AGENT; DEXAMETHASONE; DOXORUBICIN; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; HSP 990; IMATINIB; INTERLEUKIN 6; IRINOTECAN; MELPHALAN; PHOSPHATIDYLINOSITOL 3 KINASE; PREDNISONE; PROTEIN KINASE B; RADICICOL; SOMATOMEDIN C RECEPTOR; SORAFENIB; STA 9090; STAT3 PROTEIN; TANESPIMYCIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; VINCRISTINE; XL 888;

ADVANCED CANCER; AMINO TERMINAL SEQUENCE; ANEMIA; ANOREXIA; APOPTOSIS; AUTOLOGOUS STEM CELL TRANSPLANTATION; BLADDER CANCER; BONE MARROW CELL; BREAST CANCER; CANCER CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER RELAPSE; CANCER RESISTANCE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL SURVIVAL; CHEMOTHERAPY INDUCED EMESIS; COLON TUMOR; COLORECTAL CANCER; CONSTIPATION; DIARRHEA; DIZZINESS; DRUG BIOAVAILABILITY; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG ELIMINATION; DRUG ERUPTION; DRUG HALF LIFE; DRUG POTENTIATION; ENDOPLASMIC RETICULUM STRESS; FATIGUE; GASTROINTESTINAL STROMAL TUMOR; HUMAN; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CANCER; LEUKEMIA; MALIGNANT NEOPLASTIC DISEASE; MASTOCYTOMA; MELANOMA; MONOTHERAPY; MULTIPLE CYCLE TREATMENT; MULTIPLE MYELOMA; MYALGIA; MYELODYSPLASTIC SYNDROME; MYELOMA CELL; NAUSEA; NEUTROPENIA; NONHUMAN; OVARY CANCER; PANCREAS CANCER; PATHOPHYSIOLOGY; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; REVIEW; SIDE EFFECT; SIGNAL TRANSDUCTION; SOLID TUMOR; STOMACH TUMOR; STROMA CELL; THROMBOCYTOPENIA; THYROID CANCER;

ANTINEOPLASTIC AGENTS; BENZOQUINONES; DRUG SCREENING ASSAYS, ANTITUMOR; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; MULTIPLE MYELOMA;

EID: 78851472038     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2010.08360.x     Document Type: Review

References (77)

1. Alexanian, R., Barlogie, B. & Ventura, G. (1989) Chemotherapy for resistant and relapsing multiple myeloma. European Journal of Haematology Supplementum, 51, 140-144.
2. Alexanian, R., Barlogie, B. & Tucker, S. (1990) VAD-based regimens as primary treatment for multiple myeloma. American Journal of Hematology, 33, 86-89.
3. Attal, M., Harousseau, J.L., Facon, T., Guilhot, F., Doyen, C., Fuzibet, J.G., Monconduit, M., Hulin, C., Caillot, D., Bouabdallah, R., Voillat, L., Sotto, J.J., Grosbois, B., Bataille, R. & InterGroupe Francophone du Myélome. (2003) Single versus double autologous stem-cell transplantation for multiple myeloma. New England Journal of Medicine, 349, 2495-2502.
4. Banerji, U., O'Donnell, A., Scurr, M., Pacey, S., Stapleton, S., Asad, Y., Simmons, L., Maloney, A., Raynaud, F., Campbell, M., Walton, M., Lakhani, S., Kaye, S., Workman, P. & Judson, I. (2005) Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advanced malignancies. Journal of Clinical Oncology, 23, 4152-4161.
5. Basso, A.D., Solit, D.B., Chiosis, G., Giri, B., Tsichlis, P. & Rosen, N. (2002) Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. Journal of Biological Chemistry, 277, 39858-39866.
6. Biamonte, M.A., Van de Water, R., Arndt, J.W., Scannevin, R.H., Perret, D. & Lee, W.-C. (2010) Heat shock protein 90: inhibitors in clinical trials. Journal of Medicinal Chemistry, 53, 3-17.
7. Blagosklonny, M.V., Fojo, T., Bhalla, K.N., Kim, J.S., Trepel, J.B., Figg, W.D., Rivera, Y. & Neckers, L.M. (2001) The Hsp90 inhibitor geldanamycin selectively sensitizes Bcr-Abl-expressing leukemia cells to cytotoxic chemotherapy. Leukemia, 15, 1537-1543.
8. Boelens, J., Lust, S., Offner, F., Bracke, M.E. & Vanhoecke, B.W. (2007) Review. The endoplasmic reticulum: a target for new anticancer drugs. In Vivo, 21, 215-226.
9. Breckenridge, D.G., Germain, M., Mathai, J.P., Nguyen, M. & Shore, G.C. (2003) Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene, 22, 8608-8618.
10. Chant, I.D., Rose, P.E. & Morris, A.G. (1995) Analysis of heat-shock protein expression in myeloid leukaemia cells by flow cytometry. British Journal Haematology, 90, 163-168.
11. Chatterjee, M., Jain, S., Stühmer, T., Andrulis, M., Ungethüm, U., Kuban, R.J., Lorentz, H., Bommert, K., Topp, M., Krämer, D., Müller-Hermelink, H.K., Einsele, H., Greiner, A. & Bargou, R.C. (2007) STAT3 and MAPK signaling maintain overexpression of heat shock proteins 90alpha and beta in multiple myeloma cells, which critically contribute to tumor-cell survival. Blood, 109, 720-728.
12. Ciocca, D.R., Clark, G.M., Tandon, A.K., Fuqua, S.A., Welch, W.J. & McGuire, W.L. (1993) Heat shock protein hsp70 in patients with axillary lymph node-negative breast cancer: prognostic implications. Journal of the National Cancer Institute, 85, 570-574.
13. Davenport, E.L., Moore, H.E., Dunlop, A.S., Sharp, S.Y., Workman, P., Morgan, G.J. & Davies, F.E. (2007) Heat shock protein inhibition is associated with activation of the unfolded protein response pathway in myeloma plasma cells. Blood, 110, 2641-2649.
14. Dimopoulos, M., Spencer, A., Attal, M., Prince, H.M., Harousseau, J.L., Dmoszynska, A., San Miguel, J., Hellmann, A., Facon, T., Foà, R., Corso, A., Masliak, Z., Olesnyckyj, M., Yu, Z., Patin, J., Zeldis, J.B., Knight, R.D. & Multiple Myeloma (010) Study Investigators. (2007) Lenalidomide plus dexamethasone for relapsed or refractory multiple myeloma. New England Journal of Medicine, 357, 2123-2132.
15. Dong, H., Chen, L., Chen, X., Gu, H., Gao, G., Gao, Y. & Dong, B. (2009) Dysregulation of unfolded protein response partially underlies proapoptotic activity of bortezomib in multiple myeloma cells. Leukaemia & Lymphoma, 50, 974-984.
16. Duus, J., Bahar, H.I., Venkataraman, G., Ozpuyan, F., Izban, K.F., Al-Masri, H., Maududi, T., Toor, A. & Alkan, S. (2006) Analysis of expression of heat shock protein-90 (HSP90) and the effects of HSP90 inhibitor (17-AAG) in multiple myeloma. Leukaemia & Lymphoma, 47, 1369-1378.
17. Erchlichman, C. (2009) Tanespimycin: the opportunities and challenges of targeting heat shock protein 90. Expert Opinion on Investigational Drugs, 18, 861-868.
18. Fadden, P., Barabasz, B., Barta, T., Eaves, J., Foley, B., Geng, L., Hall, S., Hanson, G., Huang, H., Otto, J., Pronk, B., Rice, J. & Veal, J. (2006) A novel, orally active, small molecule Hsp90 inhibitor. Proceedings of the American Association for Cancer Research, 47, Abstract 5548.
19. Giffard, R.G., Han, R.Q., Emery, J.F., Duan, M. & Pittet, J.F. (2008) Regulation of apoptotic and inflammatory cell signaling in cerebral ischemia: the complex roles of heat shock protein 70. Anesthesiology, 109, 339-348.
20. Goetz, M.P., Toft, D.O., Ames, M.M. & Erlichman, C. (2003) The Hsp90 chaperone complex as a novel target for cancer therapy. Annals of Oncology, 14, 1169-1176.
21. Goetz, M.P., Toft, D., Reid, J., Ames, M., Stensgard, B., Safgren, S., Adjei, A.A., Sloan, J., Atherton, P., Vasile, V., Salazaar, S., Adjei, A., Croghan, G. & Erlichman, C. (2005) Phase I trial of 17-allylamino-17-demethoxygeldanamycin in patients with advanced cancer. Journal of Clinical Oncology, 23, 1078-1087.
22. Grem, J.L., Morrison, G., Guo, X.D., Agnew, E., Takimoto, C.H., Thomas, R., Szabo, E., Grochow, L., Grollman, F., Hamilton, J.M., Neckers, L. & Wilson, R.H. (2005) Phase I and pharmacologic study of 17-(allylamino)-17-demethoxygeldanamycin in adult patients with solid tumors. Journal of Clinical Oncology, 23, 1885-1893.
23. Hanson, B.E. & Vesole, D.H. (2009) Retaspimycin hydrochloride (IPI-405): a novel heat shock protein inhibitor as an anticancer agent. Expert Opinion on Investigational Drugs, 18, 1375-1383.
24. Harousseau, J.L. & Moreau, P. (2009) Autologous hematopoietic stem-cell transplantation for multiple myeloma. New England Journal of Medicine, 360, 2645-2654.
25. Hartl, F.U. & Hayer-Hartl, M. (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science, 295, 1852-1858.
26. Heath, E.I., Hillman, D.W., Vaishampayan, U., Sheng, S., Sarkar, F., Harper, F., Gaskins, M., Pitot, H.C., Tan, W., Ivy, S.P., Pili, R., Carducci, M.A., Erlichman, C. & Liu, G. (2008) A phase II trial of 17-allylamino-17-demethoxygeldanamycin in patients with hormone-refractory metastatic prostate cancer. Clinical Cancer Research, 14, 7940-7946.
27. Hideshima, T., Bergsagel, P.L., Kuehl, W.M. & Anderson, K.C. (2004) Advances in biology of multiple myeloma: clinical applications. Blood, 104, 607-618.
28. Huston, A., Leleu, X., Jia, X., Moreau, A.S., Ngo, H.T., Runnels, J., Anderson, J., Alsayed, Y., Roccaro, A., Vallet, S., Hatjiharissi, E., Tai, Y.T., Sportelli, P., Munshi, N., Richardson, P., Hideshima, T., Roodman, D.G., Anderson, K.C. & Ghobrial, I.M. (2008) Targeting Akt and heat shock protein 90 produces synergistic multiple myeloma cell cytotoxicity in the bone marrow microenvironment. Clinical Cancer Research, 14, 865-874.
29. Isaacs, J.S., Xu, W. & Neckers, L. (2003) Heat shock protein 90 as a molecular target for cancer therapeutics. Cancer Cell, 3, 213-217.
30. Jameel, A., Skilton, R.A., Campbell, T.A., Chander, S.K., Coombes, R.C. & Luqmani, Y.A. (1992) Clinical and biological significance of HSP89 alpha in human breast cancer. International Journal of Cancer, 50, 409-415.
31. Kaur, J. & Ralhan, R. (1995) Differential expression of 70-kDa heat shock-protein in human oral tumorigenesis. International Journal of Cancer, 63, 774-779.
32. Kimura, E., Enns, R.E., Alcaraz, J.E., Arboleda, J., Slamon, D.J. & Howell, S.B. (1993) Correlation of the survival of ovarian cancer patients with mRNA expression of the 60-kD heat-shock protein HSP-60. Journal of Clinical Oncology, 11, 891-898.
33. Koreth, J., Cutler, C.S., Djulbegovic, B., Behl, R., Schlossman, R.L., Munshi, N.C., Richardson, P.G., Anderson, K.C., Soiffer, R.J. & Alyea, III, E.P. (2007) High-dose therapy with single autologous transplantation versus chemotherapy for newly diagnosed multiple myeloma: a systematic review and meta-analysis of randomized controlled trials. Biology of Blood and Marrow Transplantation, 13, 183-196.
34. Kumar, S., Finn, I.W., Noga, S.J., Hari, P., Rifkin, R.M., Callendar, N.S., Bhandari, M., Wolf, J.L., Gasparetto, C., Krishnan, A., Grosman, D.D., Glass, J., Sahovic, E.A., Shi, H., Webb, I.J., Richardson, P. & Rajkumar, S.V. (2008) Safety and efficacy of novel combination therapy with bortezomib, dexamethasone, cyclophosphamide, and lenalidomide in newly diagnosed multiple myeloma: initial results from the phase I/II multi-center EVOLUTION study. Blood (ASH Annual Meeting Abstracts), 112, 93.
35. Kyle, R.A. & Rajkumar, S.V. (2004) Multiple myeloma. New England Journal of Medicine, 351, 1860-1873.
36. Lancet, J.E., Gojo, I., Burton, M., Quinn, M., Tighe, S.M., Kersey, K., Zhong, Z., Albitar, M.X., Bhalla, K., Hannah, A.L. & Baer, M.R. (2010) Phase I study of the heat shock protein 90 inhibitor alvespimycin (KOS-1022, 17-DMAG) administered intravenously twice weekly to patients with acute myeloid leukemia. Leukemia, 24, 699-705.
37. Lee, J., Grenier, L., Holson, E., Slocum, K., Ge, J., Normant, E. & Hoyt, J. (2008) IPI-493, a potent, orally available Hsp90 inhibitor of the ansamycin class. European Journal of Cancer Supplements, 6, 49.
38. Lin, T.Y., Bear, M., Du, Z., Foley, K.P., Ying, W., Barsoum, J. & London, C. (2008) The novel HSP90 inhibitor STA-9090 exhibits activity against Kit-dependent and -independent malignant mast cell tumors. Experimental Hematology, 36, 1266-1277.
39. Lundgren, K., Zhang, H., Brekken, J., Huser, N., Powell, R.E., Timple, N., Busch, D.J., Neely, L., Sensintaffar, J.L., Yang, Y.C., McKenzie, A., Friedman, J., Scannevin, R., Kamal, A., Hong, K., Kasibhatla, S.R., Boehm, M.F. & Burrows, F.J. (2009) BIIB021, an orally available, fully synthetic small-molecule inhibitor of the heat shock protein Hsp90. Molecular Cancer Therapeutics, 8, 921-929.
40. Lyons, J., Graham, B., Curry, J., Reule, M., Smyth, T., Fazal, L., Williams, B., Yule, M., Squires, M. & Thompson, N. (2008) AT13387, a fragment derived clinical candidate is active in lung and melanoma models. European Journal of Cancer Supplements, 6, 47.
41. McMillin, D.W., Negri, J., Delmore, J., Hayden, P., Ooi, M., Mitsiades, M., Schlossman, R., Richardson, P.G., Munshi, N.C., Jensen, M.R., Quadt, C., Chène, P., Schoepfer, J., García-Echeverría, C., Anderson, K.C. & Mitsiades, C.S. (2007) Activity of New Heat Shock Protein 90 (hsp90) Inhibitor NVP-AUY922 Against Myeloma Cells Sensitive and Resistant to Conventional Agents. Blood (ASH Annual Meeting Abstracts), 110, 1587.
42. Mitsiades, N., Mitsiades, C.S., Poulaki, V., Chauhan, D., Fanourakis, G., Gu, X., Bailey, C., Joseph, M., Libermann, T.A., Treon, S.P., Munshi, N.C., Richardson, P.G., Hideshima, T. & Anderson, K.C. (2002) Molecular sequelae of proteasome inhibition in human multiple myeloma cells. Proceedings of the National Academy of Sciences of the United States of America, 99, 14374-14379.
43. Mitsiades, C.S., Mitsiades, N.S., McMullan, C.J., Poulaki, V., Kung, A.L., Davies, F.E., Morgan, G., Akiyama, M., Shringarpure, R., Munshi, N.C., Richardson, P.G., Hideshima, T., Chauhan, D., Gu, X., Bailey, C., Joseph, M., Libermann, T.A., Rosen, N.S. & Anderson, K.C. (2006) Antimyeloma activity of heat shock protein-90 inhibition. Blood, 107, 1092-1100.
44. Morimoto, R.I., Kline, M.P., Bimston, D.N. & Cotto, J.J. (1997) The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays in Biochemistry, 32, 17-29.
45. Nicoll, M. (2008) XL888, a novel, synthetic, orally bioavailable inhibitor of Hsp90. European Journal of Cancer Supplements, 6, 46.
46. Oikonomopoulou, K., Soosaipillai, A. & Diamandis, E.P. (2009) Evaluation of prostate-specific antigen as a novel biomarker of Hsp90 inhibition. Clinical Biochemistry, 42, 1705-1712.
47. Okawa, Y., Hideshima, T., Steed, P., Vallet, S., Hall, S., Huang, K., Rice, J., Barabasz, A., Foley, B., Ikeda, H., Raje, N., Kiziltepe, T., Yasui, H., Enatsu, S. & Anderson, K.C. (2009) SNX-2112, a selective Hsp90 inhibitor, potently inhibits tumor cell growth, angiogenesis, and osteoclastogenesis in multiple myeloma and other hematologic tumors by abrogating signaling via Akt and ERK. Blood, 113, 846-855.
48. Patterson, J., Palombella, V.J., Fritz, C. & Normant, E. (2008) IPI-504, a novel and soluble HSP-90 inhibitor, blocks the unfolded protein response in multiple myeloma cells. Cancer Chemotherapy and Pharmacology, 61, 923-932.
49. Periyasamy-Thandavan, S., Jackson, W.H., Samaddar, J.S., Erickson, B., Barrett, J.R., Raney, L., Gopal, E., Ganapathy, V., Hill, W.D., Bhalla, K.N. & Schoenlein, P.V. (2010) Bortezomib blocks the catabolic process of autophagy via a cathepsin- dependent mechanism, affects endoplasmic reticulum stress and induces caspase-dependent cell death in antiestrogen-sensitive and resistant ER+ breast cancer cells. Autophagy, 6, 19-35.
50. Picard, D. (2009) HSP90 Interactors, Department of Cell Biology, University of Geneva, Geneva, Switzerland.
51. Pratt, W.B. (1998) The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proceedings of the Society for Experimental Biology and Medicine, 217, 420-434.
52. Ralhan, R. & Kaur, J. (1995) Differential expression of Mr 70, 000 heat shock protein in normal, premalignant, and malignant human uterine cervix. Clinical Cancer Research, 1, 1217-1222.
53. Ramanathan, R.K., Egorin, M.J., Eiseman, J.L., Ramalingam, S., Friedland, D., Agarwala, S.S., Ivy, S.P., Potter, D.M., Chatta, G., Zuhowski, E.G., Stoller, R.G., Naret, C., Guo, J. & Belani, C.P. (2007) Phase I and pharmacodynamic study of 17-(allylamino)-17-demethoxygeldanamycin in adult patients with refractory advanced cancers. Clinical Cancer Research, 13, 1769-1774.
54. Richardson, P.G., Barlogie, B., Berenson, J., Singhal, S., Jagannath, S., Irwin, D., Rajkumar, S.V., Srkalovic, G., Alsina, M., Alexanian, R., Siegel, D., Orlowski, R.Z., Kuter, D., Limentani, S.A., Lee, S., Hideshima, T., Esseltine, D.L., Kauffman, M., Adams, J., Schenkein, D.P. & Anderson, K. (2003) A phase 2 study of bortezomib in relapsed, refractory myeloma. New England Journal of Medicine, 348, 2609-2617.
55. Richardson, P., Chanan-Khan, A., Alsina, M., Doss, D., Landrigan, B., Kettner, D., Albitar, M., Mitsiades, C., Cropp, G.F., Johnson, R.G., Hannah, A.L. & Anderson, K.C. (2005a) Safety and activity of KOS-953 in patients with relapsed refractory multiple myeloma (MM): interim results of a phase 1 trial. Blood (ASH Annual Meeting Abstracts), 106, 361.
56. Richardson, P.G., Sonneveld, P., Schuster, M.W., Irwin, D., Stadtmauer, E.A., Facon, T., Harousseau, J.L., Ben-Yehuda, D., Lonial, S., Goldschmidt, H., Reece, D., San-Miguel, J.F., Bladé, J., Boccadoro, M., Cavenagh, J., Dalton, W.S., Boral, A.L., Esseltine, D.L., Porter, J.B., Schenkein, D. & Anderson, K.C. & Assessment of Proteasome Inhibition for Extending Remissions (APEX) investigators. (2005b) Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. New England Journal of Medicine, 352, 2487-2498.
57. Richardson, P.G., Mitsiades, C., Schlossman, R., Munshi, N. & Anderson, K. (2007a) New drugs for myeloma. Oncologist, 12, 664-689.
58. Richardson, P.G., Sonneveld, P., Schuster, M., Irwin, D., Stadtmauer, E., Facon, T., Harousseau, J.L., Ben-Yehuda, D., Lonial, S., Goldschmidt, H., Reece, D., Miguel, J.S., Bladé, J., Boccadoro, M., Cavenagh, J., Alsina, M., Rajkumar, S.V., Lacy, M., Jakubowiak, A., Dalton, W., Boral, A., Esseltine, D.L., Schenkein, D. & Anderson, K.C. (2007b) Extended follow-up of a phase 3 trial in relapsed multiple myeloma: final time-to-event results of the APEX trial. Blood, 110, 3557-3560.
59. Richardson, P., Chanan-Khan, A., Lonial, S., Krishnan, A., Carroll, M., Alsina, M., Albitar, M., Berman, D., Kaplita, S. & Anderson, K.C. (2009a) Tanespimycin+Bortezomib in patients with relapsed and refractory multiple myeloma: final results of a phase 1/2 study. Journal of Clinical Oncology (ASCO Annual Meeting Proceedings), 27, 8503.
60. Richardson, P.G., Sonneveld, P., Schuster, M.W., Stadtmauer, E.A., Facon, T., Harousseau, J.L., Ben-Yehuda, D., Lonial, S., Goldschmidt, H., Reece, D., Bladé, J., Boccadoro, M., Cavenagh, J.D., Boral, A.L., Esseltine, D.L., Wen, P.Y., Amato, A.A., Anderson, K.C. & San Miguel, J. (2009b) Reversibility of symptomatic peripheral neuropathy with bortezomib in the phase III APEX trial in relapsed multiple myeloma: impact of a dose-modification guideline. British Journal of Haematology, 144, 895-903.
61. Ritossa, F. (1996) Discovery of the heat shock response. Cell Stress & Chaperones, 1, 97-98.
62. Roe, S.M., Prodromou, C., O'Brien, R., Ladbury, J.E., Piper, P.W. & Pearl, L.H. (1999) Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin. Journal of Medicinal Chemistry, 42, 260-266.
63. San Miguel, J.F., Schlag, R., Khuageva, N.K., Dimopoulos, M.A., Shpilberg, O., Kropff, M., Spicka, I., Petrucci, M.T., Palumbo, A., Samoilova, O.S., Dmoszynska, A., Abdulkadyrov, K.M., Schots, R., Jiang, B., Mateos, M.V., Anderson, K.C., Esseltine, D.L., Liu, K., Cakana, A., van de Velde, H., Richardson, P.G. & VISTA Trial Investigators. (2008) Bortezomib plus melphalan and prednisone for initial treatment of multiple myeloma. New England Journal of Medicine, 359, 906-917.
64. Santarosa, M., Favaro, D., Quaia, M. & Galligioni, E. (1997) Expression of heat shock protein 72 in renal cell carcinoma: possible role and prognostic implications in cancer patients. European Journal of Cancer, 33, 873-877.
65. Solit, D.B., Ivy, S.P., Kopil, C., Sikorski, R., Morris, M.J., Slovin, S.F., Kelly, W.K., DeLaCruz, A., Curley, T., Heller, G., Larson, S., Schwartz, L., Egorin, M.J., Rosen, N. & Scher, H.I. (2007) Phase I trial of 17-allylamino-17-demethoxygeldanamycin in patients with advanced cancer. Clinical Cancer Research, 13, 1775-1782.
66. Solit, D.B., Osman, I., Polsky, D., Panageas, K.S., Daud, A., Goydos, J.S., Teitcher, J., Wolchok, J.D., Germino, F.J., Krown, S.E., Coit, D., Rosen, N. & Chapman, P.B. (2008) Phase II trial of 17-allylamino-17-demethoxygeldanamycin in patients with metastatic melanoma. Clinical Cancer Research, 14, 8302-8307.
67. Stuhmer, T., Zöllinger, A., Siegmund, D., Chatterjee, M., Grella, E., Knop, S., Kortüm, M., Unzicker, C., Jensen, M.R., Quadt, C., Chène, P., Schoepfer, J., García-Echeverría, C., Einsele, H., Wajant, H. & Bargou, R.C. (2008) Signalling profile and antitumour activity of the novel Hsp90 inhibitor NVP-AUY922 in multiple myeloma. Leukemia, 22, 1604-1612.
68. Sydor, J.R., Normant, E., Pien, C.S., Porter, J.R., Ge, J., Grenier, L., Pak, R.H., Ali, J.A., Dembski, M.S., Hudak, J., Patterson, J., Penders, C., Pink, M., Read, M.A., Sang, J., Woodward, C., Zhang, Y., Grayzel, D.S., Wright, J., Barrett, J.A., Palombella, V.J., Adams, J. & Tong, J.K. (2006) Development of 17-allylamino-17-demethoxygeldanamycin hydroquinone hydrochloride (IPI-504), an anti-cancer agent directed against Hsp90. Proceedings of the National Academy of Sciences of the United States of America, 103, 17408-17413.
69. The Myeloma Trialists' Collaborative Group. (1998) Combination chemotherapy versus melphalan plus prednisone as treatment for multiple myeloma: an overview of 6, 633 patients from 27 randomized trials. Journal of Clinical Oncology, 16, 3832-3842.
70. Wettstein, D., Baichwal, V., Papac, D., Cimbora, D., McKinnon, R., Bajji, A., Kim, S.H., Tangallapally, R., Markovitz, B. & Trovato, R. (2008) MPC-3100: a non-natural product Hsp90 inhibitor with anti-tumor activty in pre-clincal models. European Journal of Cancer Supplements, 6, 48.
71. Whitesell, L. & Lindquist, S.L. (2005) HSP90 and the chaperoning of cancer. Nature Reviews. Cancer, 5, 761-772.
72. Xu, W., Mimnaugh, E., Rosser, M.F., Nicchitta, C., Marcu, M., Yarden, Y. & Neckers, L. (2001) Sensitivity of mature Erbb2 to geldanamycin is conferred by its kinase domain and is mediated by the chaperone protein Hsp90. Journal of Biological Chemistry, 276, 3702-3708.
73. Xu, W., Marcu, M., Yuan, X., Mimnaugh, E., Patterson, C. & Neckers, L. (2002) Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu. Proceedings of the National Academy of Sciences of the United States of America, 99, 12847-12852.
74. Yenari, M.A., Liu, J., Zheng, Z., Vexler, Z.S., Lee, J.E. & Giffard, R.G. (2005) Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection. Annals of the New York Academy of Sciences, 1053, 74-83.
75. Yufu, Y., Nishimura, J. & Nawata, H. (1992) High constitutive expression of heat shock protein 90 alpha in human acute leukemia cells. Leukemia Research, 16, 597-605.
76. Zhang, H., Neely, L., Lundgren, K., Yang, Y.C., Lough, R., Timple, N. & Burrows, F. (2010) BIIB021, a synthetic Hsp90 inhibitor, has broad application against tumors with acquired multidrug resistance. International Journal of Cancer, 126, 1226-1234.
77. Zhong, Z., Simmons, J. & Timmermans, P. (2008) Prevention and treatment of bortezomib-induced peripheral neuropathy by the Hsp90 inhibitor tanespimycin (KOS-953) in the rat. European Journal of Cancer Supplements, 6, 23.