Heat shock protein 90 inhibitor NVP-AUY922 exerts potent activity against adult T-cell leukemia-lymphoma cells

Cancer Science

Volumn 105, Issue 12, 2014, Pages 1601-1608

  Taniguchi, Hiroaki ^a,b,c   Hasegawa, Hiroo ^d   Sasaki, Daisuke ^d   Ando, Koji ^c   Sawayama, Yasushi ^c   Imanishi, Daisuke ^c   Taguchi, Jun ^c   Imaizumi, Yoshitaka ^c   Hata, Tomoko ^c   Tsukasaki, Kunihiro ^e   Uno, Naoki ^d   Morinaga, Yoshitomo ^d   Yanagihara, Katsunori ^d   Miyazaki, Yasushi ^c  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^b Sasebo Shiritsu Sogo Hospital   (Japan)

^c NAGASAKI UNIVERSITY   (Japan)

^d NAGASAKI UNIVERSITY HOSPITAL   (Japan)

^e NATIONAL CANCER CENTER HOSPITAL EAST   (Japan)

Author keywords

Adult T cell leukemia lymphoma; HSP90 inhibitors; NF B; NVP AUY922; PIM kinases

Indexed keywords

5-(2,4-DIHYDROXY-5-ISOPROPYLPHENYL)-4-(4-MORPHOLIN-4-YLMETHYLPHENYL)ISOXAZOLE-3-CARBOXYLIC ACID ETHYLAMIDE; ANTINEOPLASTIC AGENT; HEAT SHOCK PROTEIN 90; ISOXAZOLE DERIVATIVE; RESORCINOL DERIVATIVE;

ANTAGONISTS AND INHIBITORS; CELL CYCLE CHECKPOINT; CELL SURVIVAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; HUMAN; LEUKEMIA-LYMPHOMA, ADULT T-CELL; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HSP90 HEAT-SHOCK PROTEINS; HUMANS; ISOXAZOLES; LEUKEMIA-LYMPHOMA, ADULT T-CELL; RESORCINOLS;

EID: 84917676081     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.12540     Document Type: Article

References (49)

1. Whitesell L, Lindquist SL. HSP90 and the chaperoning of cancer. Nat Rev Cancer 2005; 5: 761-72.
2. Kurashina R, Ohyashiki JH, Kobayashi C et al. Anti-proliferative activity of heat shock protein (Hsp) 90 inhibitors via beta-catenin/TCF7L2 pathway in adult T cell leukemia cells. Cancer Lett 2009; 284: 62-70.
3. Ikebe E, Kawaguchi A, Tezuka K et al. Oral administration of an HSP90 inhibitor, 17-DMAG, intervenes tumor-cell infiltration into multiple organs and improves survival period for ATL model mice. Blood Cancer J 2013; 3: e132.
4. Goetz MP, Toft D, Reid J et al. Phase I trial of 17-allylamino-17-demethoxygeldanamycin in patients with advanced cancer. J Clin Oncol 2005; 23: 1078-87.
5. Grem JL, Morrison G, Guo XD et al. Phase I and pharmacologic study of 17-(allylamino)-17-demethoxygeldanamycin in adult patients with solid tumors. J Clin Oncol 2005; 23: 1885-93.
6. Banerji U, O'Donnell A, Scurr M et al. Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advanced malignancies. J Clin Oncol 2005; 23: 4152-61.
7. Brough PA, Aherne W, Barril X et al. 4, 5-diarylisoxazole Hsp90 chaperone inhibitors: potential therapeutic agents for the treatment of cancer. J Med Chem 2008; 51: 196-218.
8. Eccles SA, Massey A, Raynaud FI et al. NVP-AUY922: a novel heat shock protein 90 inhibitor active against xenograft tumor growth, angiogenesis, and metastasis. Cancer Res 2008; 68: 2850-60.
9. Jensen MR, Schoepfer J, Radimerski T et al. NVP-AUY922: a small molecule HSP90 inhibitor with potent antitumor activity in preclinical breast cancer models. Breast Cancer Res 2008; 10: R33.
10. Stingl L, Stuhmer T, Chatterjee M, Jensen MR, Flentje M, Djuzenova CS. Novel HSP90 inhibitors, NVP-AUY922 and NVP-BEP800, radiosensitise tumour cells through cell-cycle impairment, increased DNA damage and repair protraction. Br J Cancer 2010; 102: 1578-91.
11. Garon EB, Finn RS, Hamidi H et al. The HSP90 inhibitor NVP-AUY922 potently inhibits non-small cell lung cancer growth. Mol Cancer Ther 2013; 12: 890-900.
12. Sessa C, Shapiro GI, Bhalla KN et al. First-in-human phase I dose-escalation study of the HSP90 inhibitor AUY922 in patients with advanced solid tumors. Clin Cancer Res 2013; 19: 3671-80.
13. Yamada Y, Tomonaga M. The current status of therapy for adult T-cell leukaemia-lymphoma in Japan. Leuk Lymphoma 2003; 44: 611-8.
14. Mori N, Fujii M, Ikeda S et al. Constitutive activation of NF-kappaB in primary adult T-cell leukemia cells. Blood 1999; 93: 2360-8.
15. Mori N, Fujii M, Iwai K et al. Constitutive activation of transcription factor AP-1 in primary adult T-cell leukemia cells. Blood 2000; 95: 3915-21.
16. Fukuda R, Hayashi A, Utsunomiya A et al. Alteration of phosphatidylinositol 3-kinase cascade in the multilobulated nuclear formation of adult T cell leukemia/lymphoma (ATLL). Proc Natl Acad Sci U S A 2005; 102: 15213-8.
17. Tsukasaki K, Utsunomiya A, Fukuda H et al. VCAP-AMP-VECP compared with biweekly CHOP for adult T-cell leukemia-lymphoma: Japan Clinical Oncology Group Study JCOG9801. J Clin Oncol 2007; 25: 5458-64.
18. Yamada Y, Fujita M, Suzuki H et al. Established IL-2-dependent double-negative (CD4- CD8-) TCR alpha beta/CD3 + ATL cells: induction of CD4 expression. Br J Haematol 1994; 88: 234-41.
19. Yamada Y, Ohmoto Y, Hata T et al. Features of the cytokines secreted by adult T cell leukemia (ATL) cells. Leuk Lymphoma 1996; 21: 443-7.
20. Maeda T, Yamada Y, Moriuchi R et al. Fas gene mutation in the progression of adult T cell leukemia. J Exp Med 1999; 189: 1063-71.
21. Hasegawa H, Yamada Y, Harasawa H et al. Sensitivity of adult T-cell leukaemia lymphoma cells to tumour necrosis factor-related apoptosis-inducing ligand. Br J Haematol 2005; 128: 253-65.
22. Yoshida M, Miyoshi I, Hinuma Y. Isolation and characterization of retrovirus from cell lines of human adult T-cell leukemia and its implication in the disease. Proc Natl Acad Sci U S A 1982; 79: 2031-5.
23. Posner LE, Robert-Guroff M, Kalyanaraman VS et al. Natural antibodies to the human T cell lymphoma virus in patients with cutaneous T cell lymphomas. J Exp Med 1981; 154: 333-46.
24. Hasegawa H, Yamada Y, Iha H et al. Activation of p53 by Nutlin-3a, an antagonist of MDM2, induces apoptosis and cellular senescence in adult T-cell leukemia cells. Leukemia 2009; 23: 2090-101.
25. Hong DS, Banerji U, Tavana B, George GC, Aaron J, Kurzrock R. Targeting the molecular chaperone heat shock protein 90 (HSP90): lessons learned and future directions. Cancer Treat Rev 2013; 39: 375-87.
26. Kamal A, Thao L, Sensintaffar J et al. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 2003; 425: 407-10.
27. Zhang H, Burrows F. Targeting multiple signal transduction pathways through inhibition of Hsp90. J Mol Med (Berl) 2004; 82: 488-99.
28. Che XF, Zheng CL, Owatari S et al. Overexpression of survivin in primary ATL cells and sodium arsenite induces apoptosis by down-regulating survivin expression in ATL cell lines. Blood 2006; 107: 4880-7.
29. Broemer M, Krappmann D, Scheidereit C. Requirement of Hsp90 activity for IkappaB kinase (IKK) biosynthesis and for constitutive and inducible IKK and NF-kappaB activation. Oncogene 2004; 23: 5378-86.
30. Peloponese JM Jr, Jeang KT. Role for Akt/protein kinase B and activator protein-1 in cellular proliferation induced by the human T-cell leukemia virus type 1 tax oncoprotein. J Biol Chem 2006; 281: 8927-38.
31. Jeong SJ, Pise-Masison CA, Radonovich MF, Park HU, Brady JN. Activated AKT regulates NF-kappaB activation, p53 inhibition and cell survival in HTLV-1-transformed cells. Oncogene 2005; 24: 6719-28.
32. Liu Y, Wang Y, Yamakuchi M et al. Phosphoinositide-3 kinase-PKB/Akt pathway activation is involved in fibroblast Rat-1 transformation by human T-cell leukemia virus type I tax. Oncogene 2001; 20: 2514-26.
33. Sato S, Fujita N, Tsuruo T. Modulation of Akt kinase activity by binding to Hsp90. Proc Natl Acad Sci U S A 2000; 97: 10832-7.
34. Fujita N, Sato S, Ishida A, Tsuruo T. Involvement of Hsp90 in signaling and stability of 3-phosphoinositide-dependent kinase-1. J Biol Chem 2002; 277: 10346-53.
35. Tawara M, Hogerzeil SJ, Yamada Y et al. Impact of p53 aberration on the progression of Adult T-cell Leukemia/Lymphoma. Cancer Lett 2006; 234: 249-55.
36. Nishimura S, Asou N, Suzushima H et al. p53 gene mutation and loss of heterozygosity are associated with increased risk of disease progression in adult T cell leukemia. Leukemia 1995; 9: 598-604.
37. Wang Z, Bhattacharya N, Weaver M et al. Pim-1: a serine/threonine kinase with a role in cell survival, proliferation, differentiation and tumorigenesis. J Vet Sci 2001; 2: 167-79.
38. Bachmann M, Moroy T. The serine/threonine kinase Pim-1. Int J Biochem Cell Biol 2005; 37: 726-30.
39. Brault L, Gasser C, Bracher F, Huber K, Knapp S, Schwaller J. PIM serine/threonine kinases in the pathogenesis and therapy of hematologic malignancies and solid cancers. Haematologica 2010; 95: 1004-15.
40. Dhanasekaran SM, Barrette TR, Ghosh D et al. Delineation of prognostic biomarkers in prostate cancer. Nature 2001; 412: 822-6.
41. Alizadeh AA, Eisen MB, Davis RE et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000; 403: 503-11.
42. Wright G, Tan B, Rosenwald A, Hurt EH, Wiestner A, Staudt LM. A gene expression-based method to diagnose clinically distinct subgroups of diffuse large B cell lymphoma. Proc Natl Acad Sci U S A 2003; 100: 9991-6.
43. Poulsen CB, Borup R, Nielsen FC et al. Microarray-based classification of diffuse large B-cell lymphoma. Eur J Haematol 2005; 74: 453-65.
44. Hsi ED, Jung SH, Lai R et al. Ki67 and PIM1 expression predict outcome in mantle cell lymphoma treated with high dose therapy, stem cell transplantation and rituximab: a Cancer and Leukemia Group B 59909 correlative science study. Leuk Lymphoma 2008; 49: 2081-90.
45. Nawijn MC, Alendar A, Berns A. For better or for worse: the role of Pim oncogenes in tumorigenesis. Nat Rev Cancer 2011; 11: 23-34.
46. Chen LS, Redkar S, Taverna P, Cortes JE, Gandhi V. Mechanisms of cytotoxicity to Pim kinase inhibitor, SGI-1776, in acute myeloid leukemia. Blood 2011; 118: 693-702.
47. Chen LS, Redkar S, Bearss D, Wierda WG, Gandhi V. Pim kinase inhibitor, SGI-1776, induces apoptosis in chronic lymphocytic leukemia cells. Blood 2009; 114: 4150-7.
48. Batra V, Maris JM, Kang MH et al. Initial testing (stage 1) of SGI-1776, a PIM1 kinase inhibitor, by the pediatric preclinical testing program. Pediatr Blood Cancer 2012; 59: 749-52.
49. Shay KP, Wang Z, Xing PX, McKenzie IF, Magnuson NS. Pim-1 kinase stability is regulated by heat shock proteins and the ubiquitin-proteasome pathway. Mol Cancer Res 2005; 3: 170-81.