A purine scaffold HSP90 inhibitor BIIB021 has selective activity against KSHV-associated primary effusion lymphoma and blocks vFLIP k13-induced NF-κB

Clinical Cancer Research

Volumn 19, Issue 18, 2013, Pages 5016-5026

  Gopalakrishnan, Ramakrishnan ^a   Matta, Hittu ^a   Chaudhary, Preet M ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALVESPIMYCIN; BIIB 021; CASPASE 3; CASPASE 7; CASPASE 9; CELL PROTEIN; FLICE INHIBITORY PROTEIN; HEAT SHOCK PROTEIN 90 INHIBITOR; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LUMINESPIB; NCP AUY 922; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG SELECTIVITY; DRUG STRUCTURE; ENZYME SUBUNIT; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; LYMPHOMA CELL; MOUSE; NONHUMAN; PRIMARY EFFUSION LYMPHOMA; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; TUMOR VOLUME; TUMOR XENOGRAFT;

ADENINE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CASPASES; CELL CYCLE; CELL PROLIFERATION; HERPESVIRIDAE INFECTIONS; HERPESVIRUS 8, HUMAN; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LYMPHOMA, PRIMARY EFFUSION; MICE; MICE, NUDE; NF-KAPPA B; POLY(ADP-RIBOSE) POLYMERASES; PURINES; PYRIDINES; TUMOR CELLS, CULTURED; VIRAL PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84884566110     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-3510     Document Type: Article

References (44)

1. Nador RG, Cesarman E, Chadburn A, Dawson DB, Ansari MQ, Sald J, et al. Primary effusion lymphoma: a distinct clinicopathologic entity associated with the Kaposi's sarcoma-associated herpes virus. Blood 1996;88:645-56.
2. Boulanger E, Gerard L, Gabarre J, Molina JM, Rapp C, Abino JF, et al. Prognostic factors and outcome of human herpesvirus 8-associated primary effusion lymphoma in patients with AIDS. J Clin Oncol 2005;23:4372-80.
3. Hayden MS, Ghosh S. Signaling to NF-kappaB. Genes Dev 2004;18:2195-224.
4. Keller SA, Schattner EJ, Cesarman E. Inhibition of NF-kappaB induces apoptosis of KSHV-infected primary effusion lymphoma cells. Blood 2000;96:2537-42.
5. Liu L, Eby MT, Rathore N, Sinha SK, Kumar A, Chaudhary PM. The human herpes virus 8-encoded viral FLICE inhibitory protein physically associates with and persistently activates the ikappa B kinase complex. J Biol Chem 2002;277:13745-51.
6. Matta H, Chaudhary PM. Activation of alternative NF-kappaB pathway by human herpes virus 8-encoded Fas-associated death domain-like IL-1 beta-converting enzyme inhibitory protein (vFLIP). Proc Natl Acad Sci U S A 2004;101:9399-404.
7. Guasparri I, Keller SA, Cesarman E. KSHV vFLIP is essential for the survival of infected lymphoma cells. J Exp Med 2004;199:993-1003.
8. Chaudhary PM, Jasmin A, Eby MT, Hood L. Modulation of the NFkappa B pathway by virally encoded death effector domains-containing proteins. Oncogene 1999;18:5738-46.
9. Bagneris C, Ageichik AV, Cronin N, Wallace B, Collins M, Boshoff C, et al. Crystal structure of a vFlip-IKKgamma complex: insights into viral activation of the IKK signalosome. Mol Cell 2008;30:620-31.
10. Jhaveri K, Taldone T, Modi S, Chiosis G. Advances in the clinical development of heat shock protein 90 (Hsp90) inhibitors in cancers. Biochim Biophys Acta 2012;1823:742-55.
11. Chen G, Cao P, Goeddel DV. TNF-induced recruitment and activation of the IKK complex require Cdc37 and Hsp90. Mol Cell 2002;9:401-10.
12. Field N, Low W, Daniels M, Howell S, Daviet L, Boshoff C, et al. KSHV vFLIP binds to IKK-{gamma} to activate IKK. J Cell Sci 2003;116:3721-8.
13. Chiosis G, Caldas Lopes E, Solit D. Heat shock protein-90 inhibitors: a chronicle from geldanamycin to today's agents. Curr Opin Investig Drugs 2006;7:534-41.
14. Taldone T, Gozman A, Maharaj R, Chiosis G. Targeting Hsp90: smallmolecule inhibitors and their clinical development. Curr Opin Pharmacol 2008;8:370-4.
15. 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 2003;3:371-6.
16. Shin KJ, Wall EA, Zavzavadjian JR, Santat LA, Liu J, Hwang JI, et al. A single lentiviral vector platform for microRNA-based conditional RNA interference and coordinated transgene expression. Proc Natl Acad Sci U S A 2006;103:13759-64.
17. Yang Y, Groshong JS, Matta H, Gopalakrishnan R, Yi H, Chaudhary PM. Constitutive NF-kappaB activation confers interleukin 6 (IL6) independence and resistance to dexamethasone and janus kinase inhibitor INCB018424 in murine plasmacytoma cells. J Biol Chem 2011;286:27988-97.
18. Uddin S, Hussain AR, Al-Hussein KA, Manogaran PS, Wickrema A, Gutierrez MI, et al. Inhibition of phosphatidylinositol 30-kinase/AKT signaling promotes apoptosis of primary effusion lymphoma cells. Clin Cancer Res 2005;11:3102-8.
19. Aoki Y, Feldman GM, Tosato G. Inhibition of STAT3 signaling induces apoptosis and decreases survivin expression in primary effusion lymphoma. Blood 2003;101:1535-42.
20. Fujimuro M, Hayward SD. Manipulation of glycogen-synthase kinase-3 activity in KSHV-associated cancers. J Mol Med 2004;82:223-31.
21. An J, Sun Y, Sun R, Rettig MB. Kaposi's sarcoma-associated herpesvirus encoded vFLIP induces cellular IL-6 expression: the role of the NF-kappaB and JNK/AP1 pathways. Oncogene 2003;22:3371-85.
22. Aoki Y, Yarchoan R, Braun J, Iwamoto A, Tosato G. Viral and cellular cytokines in AIDS-related malignant lymphomatous effusions. Blood 2000;96:1599-601.
23. Matta H, Gopalakrishnan R, Punj V, Yi H, Suo Y, Chaudhary PM. A20 is induced by Kaposi sarcoma-associated herpesvirus-encoded viral FLICE inhibitory protein (vFLIP) K13 and blocks K13-induced nuclear factor-kappaB in a negative feedback manner. J Biol Chem 2011;286:21555-64.
24. Turner DJ, Alaish SM, Zou T, Rao JN, Wang JY, Strauch ED. Bile salts induce resistance to apoptosis through NF-kappaB-mediated XIAP expression. Ann Surg 2007;245:415-25.
25. Dittmer D, Lagunoff M, Renne R, Staskus K, Haase A, Ganem D. A cluster of latently expressed genes in Kaposi's sarcoma-associated herpesvirus. J Virol 1998;72:8309-15.
26. Chen W, Sin SH, Wen KW, Damania B, Dittmer DP. Hsp90 inhibitors are efficacious against Kaposi Sarcoma by enhancing the degradation of the essential viral gene LANA, of the viral co-receptor EphA2 as well as other client proteins. PLoS Pathog 2012;8:e1003048.
27. Lundgren K, Zhang H, Brekken J, Huser N, Powell RE, Timple N, et al. BIIB021, an orally available, fully synthetic small-molecule inhibitor of the heat shock protein Hsp90. Mol Cancer Ther 2009;8:921-9.
28. Pomerantz JL, Baltimore D. Two pathways to NF-kappaB. Mol Cell 2002;10:693-5.
29. Dong X, Craig T, Xing N, Bachman LA, Paya CV, Weih F, et al. Direct transcriptional regulation of RelB by 1a, 25-dihydroxyvitamin D3 and its analogs. J Biol Chem 2003;278:49378-85.
30. Dejardin E, Droin NM, Delhase M, Haas E, Cao Y, Makris C, et al. The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity 2002;17:525-35.
31. Zhao J, Punj V, Matta H, Mazzacurati L, Schamus S, Yang Y, et al. K13 blocks KSHV lytic replication and deregulates vIL6 and hIL6 expression: a model of lytic replication induced clonal selection in viral oncogenesis. PLoS ONE 2007;2:e1067.
32. Ye FC, Zhou FC, Xie JP, Kang T, Greene W, Kuhne K, et al. Kaposi's sarcoma-associated herpesvirus latent gene vFLIP inhibits viral lytic replication through NF-kappaB-mediated suppression of the AP-1 pathway: a novel mechanism of virus control of latency. J Virol 2008;82:4235-49.
33. Chatterjee M, Osborne J, Bestetti G, Chang Y, Moore PS. Viral IL-6-induced cell proliferation and immune evasion of interferon activity. Science 2002;298:1432-5.
34. Wen KW, Damania B. Hsp90 and Hsp40/Erdj3 are required for the expression and anti-apoptotic function of KSHV K1. Oncogene 2010;29:3532-44.
35. Pacey S, Wilson RH, Walton M, Eatock MM, Hardcastle A, Zetterlund A, et al. A phase I study of the heat shock protein 90 inhibitor alvespimycin (17-DMAG) given intravenously to patients with advanced solid tumors. Clin Cancer Res 2011;17:1561-70.
36. Demetri G, LeCesne A, von Mehren M, Chmielowski B, Bauer S, Chow WA, et al. Final results from a phase III study of IPI-504 (retaspimycin hydrochloride) versus placebo in patients (pts) with gastrointestinal stromal tumors (GIST) following failure of kinase inhibitor therapies. American Society of Clinical Oncology Gastrointestinal Cancers Symposium (January 22-24, 2010, Orlando, FL); Abstract 64.
37. Gaspar N, Sharp SY, Pacey S, Jones C, Walton M, Vassal G, et al. Acquired resistance to 17-allylamino-17-demethoxygeldanamycin (17-AAG, tanespimycin) in glioblastoma cells. Cancer Res 2009;69:1966-75.
38. Zhang H, Neely L, Lundgren K, Yang YC, Lough R, Timple N, et al. BIIB021, a synthetic Hsp90 inhibitor, has broad application against tumors with acquired multidrug resistance. Int J Cancer 2010;126:1226-34.
39. Broemer M, Krappmann D, Scheidereit C. Requirement of Hsp90 activity for IkappaB kinase (IKK) biosynthesis and for constitutive and inducible IKKand NF-kappaBactivation. Oncogene 2004;23:5378-86.
40. Trepel J, Mollapour M, Giaccone G, Neckers L. Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 2010;10:537-49.
41. Brown HJ, Song MJ, Deng H, Wu T-T, Cheng G, Sun R. NF-{kappa}B inhibits gammaherpesvirus lytic replication. J Virol 2003;77:8532-40.
42. Nicholas J. Human herpesvirus 8-encoded proteins with potential roles in virus-associated neoplasia. Front Biosci 2007;12:265-81.
43. Higashi C, Saji C, Yamada K, Kagawa H, Ohga R, Taira T, et al. The effects of heat shock protein 90 inhibitors on apoptosis and viral replication in primary effusion lymphoma cells. Biol Pharm Bull 2012;35:725-30.
44. Dickson MA, Okuno SH, Keohan ML, Maki RG, D'Adamo DR, Akhurst TJ, et al. Phase II study of the HSP90-inhibitor BIIB021 in gastrointestinal stromal tumors. Ann Oncol 2013;24:252-7.