Control of NF-kB activity in human melanoma by bromodomain and extra-terminal protein inhibitor I-BET151

Pigment Cell and Melanoma Research

Volumn 27, Issue 6, 2014, Pages 1126-1137

  Gallagher, Stuart J ^a   Mijatov, Branka ^a   Gunatilake, Dilini ^a   Gowrishankar, Kavitha ^a   Tiffen, Jessamy ^a   James, Wilmott ^b   Jin, Lei ^a   Pupo, Gulietta ^a   Cullinane, Carleen ^c   Mcarthur, Grant A ^c   Tummino, Peter J ^d   Rizos, Helen ^a   Hersey, Peter ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b MELANOMA INSTITUTE AUSTRALIA   (Australia)

^c PETER MACCALLUM CANCER CENTRE   (Australia)

^d GLAXOSMITHKLINE   (United States)

Author keywords

Bromodomain and extra terminal; Cancer; Chemokine; Cytokine; Melanoma; NF kappaB

Indexed keywords

BET 151; BROMODOMAIN INHIBITOR; CHEMOKINE; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; PROTEIN BRD2; PROTEIN P50; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; 7 (3,5 DIMETHYL 4 ISOXAZOLYL) 1,3 DIHYDRO 8 METHOXY 1 [1 (2 PYRIDINYL)ETHYL] 2H IMIDAZO[4,5 C]QUINOLIN 2 ONE; BRD2 PROTEIN, HUMAN; FUSED HETEROCYCLIC RINGS; PROTEIN SERINE THREONINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANOREXIA; APOPTOSIS; ARTICLE; CANCER FATIGUE; CANCER GROWTH; CELL CYCLE REGULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; DRUG POTENCY; DRUG SELECTIVITY; HUMAN; HUMAN CELL; INFLAMMATION; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; TRANSCRIPTION REGULATION; UPREGULATION; WEIGHT REDUCTION; ANIMAL; AUTOCRINE EFFECT; BIOSYNTHESIS; CELL CYCLE; CELL PROLIFERATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PATHOLOGY; SKIN TUMOR; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; AUTOCRINE COMMUNICATION; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CHEMOKINES; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMANS; INTERLEUKIN-6; INTERLEUKIN-8; MELANOMA; MICE; NF-KAPPA B; PROTEIN-SERINE-THREONINE KINASES; SKIN NEOPLASMS;

EID: 84913607582     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/pcmr.12282     Document Type: Article

References (53)

1. Ammirante, M., Rosati, A., Arra, C. et al. (2010). IKK{gamma} protein is a target of BAG3 regulatory activity in human tumor growth. Proc. Natl Acad. Sci. USA 107, 7497-7502.
2. Basseres, D.S., Ebbs, A., Levantini, E., and Baldwin, A.S. (2010). Requirement of the NF-kappaB subunit p65/RelA for K-Ras-induced lung tumorigenesis. Cancer Res. 70, 3537-3546.
3. Becker, T.M., Rizos, H., de la Pena, A., Leclercq, I.A., Woodruff, S., Kefford, R.F., and Mann, G.J. (2005). Impaired inhibition of NF-kappaB activity by melanoma-associated p16INK4a mutations. Biochem. Biophys. Res. Commun. 332, 873-879.
4. Belkina, A.C., Nikolajczyk, B.S., and Denis, G.V. (2013). BET protein function is required for inflammation: Brd2 genetic disruption and BET inhibitor JQ1 impair mouse macrophage inflammatory responses. J. Immunol. 190, 3670-3678.
5. Beutler, B., Greenwald, D., Hulmes, J.D., Chang, M., Pan, Y.C., Mathison, J., Ulevitch, R., and Cerami, A. (1985). Identity of tumour necrosis factor and the macrophage-secreted factor cachectin. Nature 316, 552-554.
6. Binns, D., Dimmer, E., Huntley, R., Barrell, D., O'Donovan, C., and Apweiler, R. (2009). QuickGO: a web-based tool for Gene Ontology searching. Bioinformatics 25, 3045-3046.
7. Bollrath, J., and Greten, F.R. (2009). IKK/NF-kappaB and STAT3 pathways: central signalling hubs in inflammation-mediated tumour promotion and metastasis. EMBO Rep. 10, 1314-1319.
8. Chaturvedi, M.M., Sung, B., Yadav, V.R., Kannappan, R., and Aggarwal, B.B. (2011). NF-kappaB addiction and its role in cancer: 'one size does not fit all'. Oncogene 30, 1615-1630.
9. Chen, Z., Liu, M., Liu, X. et al. (2013). COX-2 regulates E-cadherin expression through the NF-kappaB/Snail signaling pathway in gastric cancer. Int. J. Mol. Med. 32, 93-100.
10. Dawson, M.A., Prinjha, R.K., Dittmann, A. et al. (2011). Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature 478, 529-533.
11. Denis, G.V., McComb, M.E., Faller, D.V., Sinha, A., Romesser, P.B., and Costello, C.E. (2006). Identification of transcription complexes that contain the double bromodomain protein Brd2 and chromatin remodeling machines. J. Proteome Res. 5, 502-511.
12. Devaiah, B.N., Lewis, B.A., Cherman, N., Hewitt, M.C., Albrecht, B.K., Robey, P.G., Ozato, K., Sims, R.J. III, and Singer, D.S. (2012). BRD4 is an atypical kinase that phosphorylates serine2 of the RNA polymerase II carboxy-terminal domain. Proc. Natl Acad. Sci. USA 109, 6927-6932.
13. Dhawan, P., Su, Y., Thu, Y.M. et al. (2008). The lymphotoxin-beta receptor is an upstream activator of NF-kappaB-mediated transcription in melanoma cells. J. Biol. Chem. 283, 15399-15408.
14. Filippakopoulos, P., Qi, J., Picaud, S. et al. (2010). Selective inhibition of BET bromodomains. Nature 468, 1067-1073.
15. Franco, A.V., Zhang, X.D., Van Berkel, E., Sanders, J.E., Zhang, X.Y., Thomas, W.D., Nguyen, T., and Hersey, P. (2001). The role of NF-kappa B in TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis of melanoma cells. J. Immunol. 166, 5337-5345.
16. Gallagher, S.J., Mijatov, B., Gunatilake, D. et al. (2014). The epigenetic regulator I-BET151 induces BIM dependent apoptosis and cell cycle arrest of human melanoma cells. J. Invest. Dermatol. doi: 10.1038/jid.2014.243. In press.
17. Girotti, M.R., Pedersen, M., Sanchez-Laorden, B. et al. (2013). Inhibiting EGF receptor or SRC family kinase signaling overcomes BRAF inhibitor resistance in melanoma. Cancer Discov. 3, 158-167.
18. Gupta, S.C., Sundaram, C., Reuter, S., and Aggarwal, B.B. (2010). Inhibiting NF-kappaB activation by small molecules as a therapeutic strategy. Biochim. Biophys. Acta 1799, 775-787.
19. Gupta, S.C., Kim, J.H., Kannappan, R., Reuter, S., Dougherty, P.M., and Aggarwal, B.B. (2011). Role of nuclear factor kappaB-mediated inflammatory pathways in cancer-related symptoms and their regulation by nutritional agents. Exp. Biol. Med. 236, 658-671.
20. Hayden, M.S., and Ghosh, S. (2012). NF-kappaB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 26, 203-234.
21. Huang, B., Yang, X.D., Zhou, M.M., Ozato, K., and Chen, L.F. (2009). Brd4 coactivates transcriptional activation of NF-kappaB via specific binding to acetylated RelA. Mol. Cell. Biol. 29, 1375-1387.
22. Irvine, M., Philipsz, S., Frausto, M., Mijatov, B., Gallagher, S.J., Fung, C., Becker, T.M., Kefford, R.F., and Rizos, H. (2010). Amino terminal hydrophobic import signals target the p14(ARF) tumor suppressor to the mitochondria. Cell Cycle 9, 829-839.
23. Jazirehi, A.R., Baritaki, S., Koya, R.C., Bonavida, B., and Economou, J.S. (2011). Molecular mechanism of MART-1+/A*0201+ human melanoma resistance to specific CTL-killing despite functional tumor-CTL interaction. Cancer Res. 71, 1406-1417.
24. Jiang, X., Zhou, J., Giobbie-Hurder, A., Wargo, J., and Hodi, F.S. (2013). The activation of MAPK in melanoma cells resistant to BRAF inhibition promotes PD-L1 expression that is reversible by MEK and PI3K inhibition. Clin. Cancer Res. 19, 598-609.
25. Karin, M., and Greten, F.R. (2005). NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 5, 749-759.
26. Lai, F., Jiang, C.C., Farrelly, M.L., Zhang, X.D., and Hersey, P. (2012). Evidence for upregulation of Bim and the splicing factor SRp55 in melanoma cells from patients treated with selective BRAF inhibitors. Melanoma Res. 22, 244-251.
27. Landsberg, J., Kohlmeyer, J., Renn, M. et al. (2012). Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation. Nature 490, 412-416.
28. Li, N., Grivennikov, S.I., and Karin, M. (2011). The unholy trinity: inflammation, cytokines, and STAT3 shape the cancer microenvironment. Cancer Cell 19, 429-431.
29. Lito, P., Pratilas, C.A., Joseph, E.W. et al. (2012). Relief of profound feedback inhibition of mitogenic signaling by RAF inhibitors attenuates their activity in BRAFV600E melanomas. Cancer Cell 22, 668-682.
30. Liu, J., Suresh Kumar, K.G., Yu, D., Molton, S.A., McMahon, M., Herlyn, M., Thomas-Tikhonenko, A., and Fuchs, S.Y. (2007). Oncogenic BRAF regulates beta-Trcp expression and NF-kappaB activity in human melanoma cells. Oncogene 26, 1954-1958.
31. Lu, C., Sheehan, C., Rak, J.W., Chambers, C.A., Hozumi, N., and Kerbel, R.S. (1996). Endogenous interleukin 6 can function as an in vivo growth- stimulatory factor for advanced-stage human melanoma cells. Clin. Cancer Res. 2, 1417-1425.
32. Madonna, G., Ullman, C.D., Gentilcore, G., Palmieri, G., and Ascierto, P.A. (2012). NF-kappaB as potential target in the treatment of melanoma. J. Transl. Med. 10, 53.
33. Mijatov, B.S.K., Jin, L., Gallagher, S., and Hersey, P. (2012). Cytokines and the NF-kB pathway in resistance of melanoma to BRAF inhibitors. Pigment cell and Melanoma Res. 25, 875.
34. Mouawad, R., Benhammouda, A., Rixe, O., Antoine, E.C., Borel, C., Weil, M., Khayat, D., and Soubrane, C. (1996). Endogenous interleukin 6 levels in patients with metastatic malignant melanoma: correlation with tumor burden. Clin. Cancer Res. 2, 1405-1409.
35. Natoli, G. (2012). NF-kappaB and chromatin: ten years on the path from basic mechanisms to candidate drugs. Immunol. Rev. 246, 183-192.
36. Nicodeme, E., Jeffrey, K.L., Schaefer, U. et al. (2010). Suppression of inflammation by a synthetic histone mimic. Nature 468, 1119-1123.
37. Perkins, N.D. (2012). The diverse and complex roles of NF-kappaB subunits in cancer. Nat. Rev. Cancer 12, 121-132.
38. Rauert-Wunderlich, H., Siegmund, D., Maier, E., Giner, T., Bargou, R.C., Wajant, H., and Stuhmer, T. (2013). The IKK inhibitor Bay 11-7082 induces cell death independent from inhibition of activation of NFkappaB transcription factors. PLoS ONE 8, 20.
39. Richmond, A. (2002). Nf-kappa B, chemokine gene transcription and tumour growth. Nat. Rev. Immunol. 2, 664-674.
40. Richmond, A., Yang, J., and Su, Y. (2009). The good and the bad of chemokines/chemokine receptors in melanoma. Pigment Cell Melanoma Res. 22, 175-186.
41. Segura, M.F., Fontanals-Cirera, B., Gaziel-Sovran, A. et al. (2013). BRD4 sustains proliferation and represents a new target for epigenetic therapy in melanoma. Cancer Res. 73, 6264-6276.
42. Singh, S., Singh, A.P., Sharma, B., Owen, L.B., and Singh, R.K. (2010). CXCL8 and its cognate receptors in melanoma progression and metastasis. Future Oncol. 6, 111-116.
43. Smale, S.T. (2012). Dimer-specific regulatory mechanisms within the NF-kappaB family of transcription factors. Immunol. Rev. 246, 193-204.
44. Straussman, R., Morikawa, T., Shee, K. et al. (2012). Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487, 500-504.
45. Thu, Y.M., Su, Y., Yang, J., Splittgerber, R., Na, S., Boyd, A., Mosse, C., Simons, C., and Richmond, A. (2012). NF-kappaB inducing kinase (NIK) modulates melanoma tumorigenesis by regulating expression of pro-survival factors through the beta-catenin pathway. Oncogene 31, 2580-2592.
46. Ueda, Y., and Richmond, A. (2006). NF-kappaB activation in melanoma. Pigment Cell Res. 19, 112-124.
47. Wilson, T.R., Fridlyand, J., Yan, Y. et al. (2012). Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 487, 505-509.
48. Yang, J., Amiri, K.I., Burke, J.R., Schmid, J.A., and Richmond, A. (2006). BMS-345541 targets inhibitor of kappaB kinase and induces apoptosis in melanoma: involvement of nuclear factor kappaB and mitochondria pathways. Clin. Cancer Res. 12, 950-960.
49. Yang, J., Kantrow, S., Sai, J. et al. (2012). Ikk4a/Arf inactivation with activation of the NF-kappaB/IL-6 pathway is sufficient to drive the development and growth of angiosarcoma. Cancer Res. 72, 4682-4695.
50. Zhang, X.D., Franco, A., Myers, K., Gray, C., Nguyen, T., and Hersey, P. (1999). Relation of TNF-related apoptosis-inducing ligand (TRAIL) receptor and FLICE-inhibitory protein expression to TRAIL-induced apoptosis of melanoma. Cancer Res. 59, 2747-2753.
51. Zhang, G., Liu, R., Zhong, Y. et al. (2012). Down-regulation of NF-kappaB transcriptional activity in HIV-associated kidney disease by BRD4 inhibition. J. Biol. Chem. 287, 28840-28851.
52. Zhang, W., Chen, H., Liu, D.L., Li, H., Luo, J., Zhang, J.H., Li, Y., Chen, K.J., Tong, H.F., and Lin, S.Z. (2013). Emodin sensitizes the gemcitabine-resistant cell line Bxpc-3/Gem to gemcitabine via downregulation of NF-kappaB and its regulated targets. Int. J. Oncol. 42, 1189-1196.
53. Zou, Z., Huang, B., Wu, X., Zhang, H., Qi, J., Bradner, J., Nair, S., and Chen, L.F. (2013). Brd4 maintains constitutively active NF-kappaB in cancer cells by binding to acetylated RelA. Oncogene 33, 2395-2404.