Constitutive activation of signal transducers and activators of transcription predicts vorinostat resistance in cutaneous T-cell lymphoma

Cancer Research

Volumn 68, Issue 10, 2008, Pages 3785-3794

  Fantin, Valeria R ^a   Loboda, Andrey ^a   Paweletz, Cloud P ^a   Hendrickson, Ronald C ^a   Pierce, Jacqueline W ^a   Roth, Jennifer A ^a   Li, Lixia ^a   Gooden, Frank ^a   Korenchuk, Susan ^a   Hou, Xiaoli S ^a   Harrington, Elizabeth A ^a   Randolph, Sophia ^a   Reilly, John F ^a   Ware, Christopher M ^a   Kadin, Marshall E ^b,c   Frankel, Stanley R ^a   Richon, Victoria M ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c ROGER WILLIAMS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 7; HISTONE DEACETYLASE INHIBITOR; JANUS KINASE; MYC PROTEIN; PROTEIN BAD; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; SMALL INTERFERING RNA; STAT PROTEIN; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; SURVIVIN; TRANSCRIPTION FACTOR JUNB; VORINOSTAT; ANTINEOPLASTIC AGENT; HYDROXAMIC ACID; TUMOR MARKER;

APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER RESISTANCE; CELL CYCLE; CONTROLLED STUDY; CUTANEOUS T CELL LYMPHOMA; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN TISSUE; IC 50; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; LYMPHOMA CELL LINE; MAJOR CLINICAL STUDY; MYCOSIS FUNGOIDES; PRIORITY JOURNAL; PROGNOSIS; REAL TIME POLYMERASE CHAIN REACTION; SEZARY SYNDROME; SKIN BIOPSY; WESTERN BLOTTING; B CELL LYMPHOMA; CELL PROLIFERATION; DRUG RESISTANCE; METABOLISM; SKIN TUMOR; T CELL LYMPHOMA; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION PROFILING; HUMANS; HYDROXAMIC ACIDS; LYMPHOMA, B-CELL; LYMPHOMA, T-CELL; PROGNOSIS; SKIN NEOPLASMS; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR; TUMOR MARKERS, BIOLOGICAL;

EID: 45549083112     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-6091     Document Type: Article

References (51)

1. Kim EJ, Hess S, Richardson SK, et al. Immunopathogenesis and therapy of cutaneous T cell lymphoma. J Clin Invest 2005;115:798-812.
2. Demierre MF, Kim YH, Zackheim HS. Prognosis, clinical outcomes and quality of life issues in cutaneous T-cell lymphoma. Hematol Oncol Clin North Am 2003;17:1485-507.
3. Foss F. Overview of cutaneous T-cell lymphoma: prognostic factors and novel therapeutic approaches. Leuk Lymphoma 2003;44 Suppl 3:S55-61.
4. Richon VM, Emiliani S, Verdin E, et al. A class of hybrid polar inducers of transformed cell differentiation inhibits histone deacetylases. Proc Natl Acad Sci U S A 1998;95:3003-7.
5. Richon VM. Cancer biology: mechanism of antitumour action of vorinostat (suberoylanilide hydroxamic acid), a novel histone deacetylase inhibitor. Br J Cancer 2006;95 Suppl 1:S2-6.
6. Duvic M, Talpur R, Ni X, et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood 2007;109:31-9.
7. Olsen EA, Kim YH, Kuzel TM, et al. A phase IIb multicenter trial of vorinostat (suberoylanilide hydroxamic acid, SAHA) in patients with persistent, progressive or treatment refractory mycosis fungoides or sézary syndrome subtypes of cutaneous T-cell lymphoma. J Clin Oncol 2007;25:3109-15.
8. Marks PA. Discovery and development of SAHA as an anticancer agent. Oncogene 2007;26:1351-6.
9. Grant S, Easley C, Kirkpatrick P. Vorinostat. Nat Rev Drug Discov 2007;6:21-2.
10. Johnstone RW. Suberanilohydroxamic acid. Aton Pharma. IDrugs 2004;7:674-82.
11. Leonard WJ, O'Shea JJ. Jaks and STATs: biological implications. Annu Rev Immunol 1998;16:293-322.
12. Darnell JE, Jr. Studies of IFN-induced transcriptional activation uncover the Jak-Stat pathway. J Interferon Cytokine Res 1998;18:549-54.
13. Yu H, Jove R. The STATs of cancer-new molecular targets come of age. Nat Rev Cancer 2004;4:97-105.
14. Buettner R, Mora LB, Jove R. Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin Cancer Res 2002;8:945-54.
15. Frank DA. STAT signaling in cancer: insights into pathogenesis and treatment strategies. In: Signal transduction in cancer. Secaucus: Kluwer Academic Publishers; 2002. p. 267-91.
16. Verma A, Kambhampati S, Parmar S, Platanias LC. Jak family of kinases in cancer. Cancer Metastasis Rev 2003;22:423-34.
17. Li L, Shaw PE. A STAT3 dimer formed by inter-chain disulphide bridging during oxidative stress. Biochem Biophys Res Commun 2004;322:1005-11.
18. Valentino L, Pierre J. JAK/STAT signal transduction: regulators and implication in hematological malignancies. Biochem Pharmacol 2006;71:713-21.
19. Mitchell TJ, John S. Signal transducer and activator of transcription (STAT) signalling and T-cell lymphomas. Immunology 2005;114:301-12.
20. Bowman T, Garcia R, Turkson J, Jove R. STATs in oncogenesis. Oncogene 2000;19:2474-88.
21. Bromberg J. Stat proteins and oncogenesis. J Clin Invest 2002;109:1139-42.
22. Zhang Q, Nowak I, Vonderheid EC, et al. Activation of Jak/STAT proteins involved in signal transduction pathway mediated by receptor for interleukin 2 in malignant T lymphocytes derived from cutaneous anaplastic large T-cell lymphoma and Sezary syndrome. Proc Natl Acad Sci U S A 1996;93:9148-53.
23. Sommer VH, Clemmensen OJ, Nielsen O, et al. In vivo activation of STAT3 in cutaneous T-cell lymphoma. Evidence for an antiapoptotic function of STAT3. Leukemia 2004;18:1288-95.
24. Bromberg JF, Wrzeszczynska MH, Devgan G, et al. Stat3 as an oncogene. Cell 1999;98:295-303.
25. Ikuta K, Takemura K, Kihara M, et al. Overexpression of constitutive signal transducer and activator of transcription 3 mRNA in cisplatin-resistant human non-small cell lung cancer cells. Oncol Rep 2005;13:217-22.
26. Roberts D, Schick J, Conway S, et al. Identification of genes associated with platinum drug sensitivity and resistance in human ovarian cancer cells. Br J Cancer 2005;92:1149-58.
27. Gritsko T, Williams A, Turkson J, et al. Persistent activation of stat3 signaling induces survivin gene expression and confers resistance to apoptosis in human breast cancer cells. Clin Cancer Res 2006;12:11-9.
28. Khoury JD, Medeiros LJ, Rassidakis GZ, et al. Differential expression and clinical significance of tyrosine-phosphorylated STAT3 in ALK+ and ALK-anaplastic large cell lymphoma. Clin Cancer Res 2003;9:3692-9.
29. Alas S, Bonavida B. Inhibition of constitutive STAT3 activity sensitizes resistant non-Hodgkin's lymphoma and multiple myeloma to chemotherapeutic drug-mediated apoptosis. Clin Cancer Res 2003;9:316-26.
30. Paweletz CP, Charboneau L, Bichsel VE, et al. Reverse phase protein microarrays which capture disease progression show activation of pro-survival pathways at the cancer invasion front. Oncogene 2001;20:1981-9.
31. Hughes TR, Mao M, Jones AR, et al. Expression profiling using microarrays fabricated by an ink-jet oligonucleotide synthesizer. Nat Biotechnol 2001;19:342-7.
32. van 't Veer LJ, Dai H, van de Vijver MJ, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002;415:530-6.
33. Fantin VR, Berardi MJ, Babbe H, et al. A bifunctional targeted peptide that blocks HER-2 tyrosine kinase and disables mitochondrial function in HER-2-positive carcinoma cells. Cancer Res 2005;65:6891-900.
34. Fisher R. On the interpretation of x2 from contingency tables, and the calculation of P. J R Stat Soc 1922;85:87-94.
35. Kelly WK, O'Connor OA, Krug LM, et al. Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer. J Clin Oncol 2005;23:3923-31.
36. Ni X, Hazarika P, Zhang C, et al. Fas ligand expression by neoplastic T lymphocytes mediates elimination of CD8+ cytotoxic T-lymphocytes in mycosis fungoides: a potential mechanism of tumor immune escape? Clin Cancer Res 2001;7:2682-92.
37. Shao RH, Tian X, Gorgun G, et al. Arginine butyrate increases the cytotoxicity of DAB(389)IL-2 in leukemia and lymphoma cells by upregulation of IL-2Rh gene. Leuk Res 2002;26:1077-83.
38. Zhang C, Richon V, Ni X, et al. Selective induction of apoptosis by histone deacetylase inhibitor SAHA in cutaneous T-cell lymphoma cells: relevance to mechanism of therapeutic action. J Invest Dermatol 2005;125:1045-52.
39. Nishizuka S, Charboneau L, Young L, et al. Proteomic profiling of the NCI-60 cancer cell lines using new highdensity reverse-phase lysate microarrays. Proc Natl Acad Sci U S A 2003;100:14229-34.
40. Eriksen KW, Kaltoft K, Mikkelsen G, et al. Constitutive STAT3-activation in Sezary syndrome: tyrphostin AG490 inhibits STAT3-activation, interleukin-2 receptor expression and growth of leukemic Sezary cells. Leukemia 2001;15:787-93.
41. Nielsen M, Kaltoft K, Nordahl M, et al. Constitutive activation of a slowlymigrating isoform of Stat3 in mycosis fungoides: tyrphostin AG490 inhibits Stat3 activation and growth of mycosis fungoides tumor cell lines. Proc Natl Acad Sci U S A 1997;94:6764-9.
42. Rascle A, Johnston JA, Amati B. Deacetylase activity is required for recruitment of the basal transcription machinery and transactivation by STAT5. Mol Cell Biol 2003;23:4162-73.
43. Xu M, Nie L, Kim SH, Sun XH. STAT5-induced Id-1 transcription involves recruitment of HDAC1 and deacetylation of C/EBPβ. EMBO J 2003;22:893-904.
44. Catania A, Iavarone C, Carlomagno SM, Chiariello M. Selective transcription and cellular proliferation induced by PDGF require histone deacetylase activity. Biochem Biophys Res Commun 2006;343:544-54.
45. Klampfer L, Huang J, Sasazuki T, et al. Inhibition of interferon γ signaling by the short chain fatty acid butyrate. Mol Cancer Res 2003;1:855-62.
46. Wang R, Cherukuri P, Luo J. Activation of Stat3 sequence-specific DNA binding and transcription by p300/CREB-binding protein-mediated acetylation. J Biol Chem 2005;280:11528-34.
47. Sakamoto S, Potla R, Larner AC. Histone deacetylase activity is required to recruit RNA polymerase II to the promoters of selected interferon-stimulated early response genes. J Biol Chem 2004;279:40362-7.
48. Catlett-Falcone R, Landowski TH, Oshiro MM, et al. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 1999;10:105-15.
49. Epling-Burnette PK, Liu JH, Catlett-Falcone R, et al. Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl-1 expression. J Clin Invest 2001;107:351-62.
50. 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.
51. Witkiewicz A, Raghunath P, Wasik A, et al. Loss of SHP-1 tyrosine phosphatase expression correlates with the advanced stages of cutaneous T-cell lymphoma. Hum Pathol 2007;38:462-7.