Loss of HDAC-Mediated Repression and Gain of NF-κB Activation Underlie Cytokine Induction in ARID1A- and PIK3CA-Mutation-Driven Ovarian Cancer

Cell Reports

Volumn 17, Issue 1, 2016, Pages 275-288

  Kim, Minchul ^a   Lu, Falong ^a   Zhang, Yi ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

ARID1A; HDAC; ovarian clear cell carcinoma; PIK3CA; pro inflammatory cytokine; RelA

Indexed keywords

CARBOPLATIN; CYTOKINE; HISTONE DEACETYLASE; I KAPPA B; I KAPPA B KINASE; I KAPPA B KINASE 2; I KAPPA B KINASE 2 INHIBITOR V; I KAPPA B KINASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN ARID1A; PROTEIN KINASE B; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR SIN3A; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; ARID1A PROTEIN, HUMAN; I KAPPA B KINASE ALPHA; NUCLEAR PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PIK3CA PROTEIN, HUMAN; RELA PROTEIN, HUMAN; REPRESSOR PROTEIN; SIN3A TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CARCINOGENESIS; CELL TRANSFORMATION; CLEAR CELL CARCINOMA; COMPLEX FORMATION; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; GENE EXPRESSION; GENE INDUCTION; GENE MUTATION; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; MOUSE MODEL; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN SECRETION; ADENOCARCINOMA, CLEAR CELL; ANIMAL; BIOSYNTHESIS; CELL LINE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; DRUG SCREENING; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OVARIAN NEOPLASMS; PATHOLOGY; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

ADENOCARCINOMA, CLEAR CELL; ANIMALS; ANTINEOPLASTIC AGENTS; CARBOPLATIN; CELL LINE; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CLASS I PHOSPHATIDYLINOSITOL 3-KINASES; CYTOKINES; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASES; HUMANS; MICE; NF-KAPPA B; NF-KAPPAB INHIBITOR ALPHA; NUCLEAR PROTEINS; OVARIAN NEOPLASMS; REPRESSOR PROTEINS; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84989853721     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.09.003     Document Type: Article

References (52)

1. Acharyya, S., Oskarsson, T., Vanharanta, S., Malladi, S., Kim, J., Morris, P.G., Manova-Todorova, K., Leversha, M., Hogg, N., Seshan, V.E., et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 150 (2012), 165–178.
2. Bast, R.C. Jr., Hennessy, B., Mills, G.B., The biology of ovarian cancer: new opportunities for translation. Nat. Rev. Cancer 9 (2009), 415–428.
3. Baud, V., Karin, M., Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls. Nat. Rev. Drug Discov. 8 (2009), 33–40.
4. Bitler, B.G., Aird, K.M., Garipov, A., Li, H., Amatangelo, M., Kossenkov, A.V., Schultz, D.C., Liu, Q., Shih, IeM., Conejo-Garcia, J.R., et al. Synthetic lethality by targeting EZH2 methyltransferase activity in ARID1A-mutated cancers. Nat. Med. 21 (2015), 231–238.
5. Brown, K., Gerstberger, S., Carlson, L., Franzoso, G., Siebenlist, U., Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 267 (1995), 1485–1488.
6. Chandler, R.L., Damrauer, J.S., Raab, J.R., Schisler, J.C., Wilkerson, M.D., Didion, J.P., Starmer, J., Serber, D., Yee, D., Xiong, J., et al. Coexistent ARID1A-PIK3CA mutations promote ovarian clear-cell tumorigenesis through pro-tumorigenic inflammatory cytokine signalling. Nat. Commun., 6, 2015, 6118.
7. Gerritsen, M.E., Williams, A.J., Neish, A.S., Moore, S., Shi, Y., Collins, T., CREB-binding protein/p300 are transcriptional coactivators of p65. Proc. Natl. Acad. Sci. USA 94 (1997), 2927–2932.
8. Grivennikov, S.I., Karin, M., Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth Factor Rev. 21 (2010), 11–19.
9. Grivennikov, S., Karin, E., Terzic, J., Mucida, D., Yu, G.Y., Vallabhapurapu, S., Scheller, J., Rose-John, S., Cheroutre, H., Eckmann, L., Karin, M., IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 15 (2009), 103–113.
10. Harikrishnan, K.N., Chow, M.Z., Baker, E.K., Pal, S., Bassal, S., Brasacchio, D., Wang, L., Craig, J.M., Jones, P.L., Sif, S., El-Osta, A., Brahma links the SWI/SNF chromatin-remodeling complex with MeCP2-dependent transcriptional silencing. Nat. Genet. 37 (2005), 254–264.
11. He, H.H., Meyer, C.A., Hu, S.S., Chen, M.W., Zang, C., Liu, Y., Rao, P.K., Fei, T., Xu, H., Long, H., et al. Refined DNase-seq protocol and data analysis reveals intrinsic bias in transcription factor footprint identification. Nat. Methods 11 (2014), 73–78.
12. Hendrix, N.D., Wu, R., Kuick, R., Schwartz, D.R., Fearon, E.R., Cho, K.R., Fibroblast growth factor 9 has oncogenic activity and is a downstream target of Wnt signaling in ovarian endometrioid adenocarcinomas. Cancer Res. 66 (2006), 1354–1362.
13. Horie, R., Molecularly-targeted Strategy and NF-κB in lymphoid malignancies. J. Clin. Exp. Hematop. 53 (2013), 185–195.
14. Iliopoulos, D., Hirsch, H.A., Struhl, K., An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell 139 (2009), 693–706.
15. Jones, S., Wang, T.L., Shih, IeM., Mao, T.L., Nakayama, K., Roden, R., Glas, R., Slamon, D., Diaz, L.A. Jr., Vogelstein, B., et al. Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 330 (2010), 228–231.
16. Kadoch, C., Crabtree, G.R., Mammalian SWI/SNF chromatin remodeling complexes and cancer: Mechanistic insights gained from human genomics. Sci. Adv., 1, 2015, e1500447.
17. Kane, L.P., Shapiro, V.S., Stokoe, D., Weiss, A., Induction of NF-kappaB by the Akt/PKB kinase. Curr. Biol. 9 (1999), 601–604.
18. Karin, M., Yamamoto, Y., Wang, Q.M., The IKK NF-kappa B system: a treasure trove for drug development. Nat. Rev. Drug Discov. 3 (2004), 17–26.
19. Kim, J.W., Jang, S.M., Kim, C.H., An, J.H., Kang, E.J., Choi, K.H., New molecular bridge between RelA/p65 and NF-κB target genes via histone acetyltransferase TIP60 cofactor. J. Biol. Chem. 287 (2012), 7780–7791.
20. Kumar, J., Ward, A.C., Role of the interleukin 6 receptor family in epithelial ovarian cancer and its clinical implications. Biochim. Biophys. Acta 1845 (2014), 117–125.
21. Lai, A.Y., Wade, P.A., Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat. Rev. Cancer 11 (2011), 588–596.
22. Langmead, B., Salzberg, S.L., Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 (2012), 357–359.
23. Liu, J., Yang, G., Thompson-Lanza, J.A., Glassman, A., Hayes, K., Patterson, A., Marquez, R.T., Auersperg, N., Yu, Y., Hahn, W.C., et al. A genetically defined model for human ovarian cancer. Cancer Res. 64 (2004), 1655–1663.
24. Mackay, H.J., Hirte, H., Colgan, T., Covens, A., MacAlpine, K., Grenci, P., Wang, L., Mason, J., Pham, P.A., Tsao, M.S., et al. Phase II trial of the histone deacetylase inhibitor belinostat in women with platinum resistant epithelial ovarian cancer and micropapillary (LMP) ovarian tumours. Eur. J. Cancer 46 (2010), 1573–1579.
25. Mercurio, F., Zhu, H., Murray, B.W., Shevchenko, A., Bennett, B.L., Li, J., Young, D.B., Barbosa, M., Mann, M., Manning, A., Rao, A., IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 278 (1997), 860–866.
26. Minucci, S., Pelicci, P.G., Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat. Rev. Cancer 6 (2006), 38–51.
27. Nakanishi, C., Toi, M., Nuclear factor-kappaB inhibitors as sensitizers to anticancer drugs. Nat. Rev. Cancer 5 (2005), 297–309.
28. Napetschnig, J., Wu, H., Molecular basis of NF-κB signaling. Annu. Rev. Biophys. 42 (2013), 443–468.
29. Neph, S., Vierstra, J., Stergachis, A.B., Reynolds, A.P., Haugen, E., Vernot, B., Thurman, R.E., John, S., Sandstrom, R., Johnson, A.K., et al. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 489 (2012), 83–90.
30. Perkins, N.D., Felzien, L.K., Betts, J.C., Leung, K., Beach, D.H., Nabel, G.J., Regulation of NF-kappaB by cyclin-dependent kinases associated with the p300 coactivator. Science 275 (1997), 523–527.
31. Romashkova, J.A., Makarov, S.S., NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401 (1999), 86–90.
32. Samartzis, E.P., Noske, A., Dedes, K.J., Fink, D., Imesch, P., ARID1A mutations and PI3K/AKT pathway alterations in endometriosis and endometriosis-associated ovarian carcinomas. Int. J. Mol. Sci. 14 (2013), 18824–18849.
33. Samuels, Y., Diaz, L.A. Jr., Schmidt-Kittler, O., Cummins, J.M., Delong, L., Cheong, I., Rago, C., Huso, D.L., Lengauer, C., Kinzler, K.W., et al. Mutant PIK3CA promotes cell growth and invasion of human cancer cells. Cancer Cell 7 (2005), 561–573.
34. Schafer, Z.T., Brugge, J.S., IL-6 involvement in epithelial cancers. J. Clin. Invest. 117 (2007), 3660–3663.
35. Schwitalla, S., Fingerle, A.A., Cammareri, P., Nebelsiek, T., Göktuna, S.I., Ziegler, P.K., Canli, O., Heijmans, J., Huels, D.J., Moreaux, G., et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 152 (2013), 25–38.
36. Sun, S.C., Non-canonical NF-κB signaling pathway. Cell Res. 21 (2011), 71–85.
37. Suryo Rahmanto, Y., Jung, J.G., Wu, R.C., Kobayashi, Y., Heaphy, C.M., Meeker, A.K., Wang, T.L., Shih, I.M., Inactivating ARID1A tumor suppressor enhances TERT transcription and maintains telomere length in cancer cells. J. Biol. Chem 291 (2016), 9690–9699.
38. Takahashi, H., Ogata, H., Nishigaki, R., Broide, D.H., Karin, M., Tobacco smoke promotes lung tumorigenesis by triggering IKKbeta- and JNK1-dependent inflammation. Cancer Cell 17 (2010), 89–97.
39. Trapnell, C., Pachter, L., Salzberg, S.L., TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 (2009), 1105–1111.
40. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., Pachter, L., Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28 (2010), 511–515.
41. Wang, Y., Zhang, H., Chen, Y., Sun, Y., Yang, F., Yu, W., Liang, J., Sun, L., Yang, X., Shi, L., et al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138 (2009), 660–672.
42. Waugh, D.J., Wilson, C., The interleukin-8 pathway in cancer. Clin. Cancer Res. 14 (2008), 6735–6741.
43. Wiegand, K.C., Shah, S.P., Al-Agha, O.M., Zhao, Y., Tse, K., Zeng, T., Senz, J., McConechy, M.K., Anglesio, M.S., Kalloger, S.E., et al. ARID1A mutations in endometriosis-associated ovarian carcinomas. N. Engl. J. Med. 363 (2010), 1532–1543.
44. Wilson, B.G., Roberts, C.W., SWI/SNF nucleosome remodellers and cancer. Nat. Rev. Cancer 11 (2011), 481–492.
45. Xia, Y., Shen, S., Verma, I.M., NF-κB, an active player in human cancers. Cancer Immunol. Res. 2 (2014), 823–830.
46. Xu, H., Wei, C.L., Lin, F., Sung, W.K., An HMM approach to genome-wide identification of differential histone modification sites from ChIP-seq data. Bioinformatics 24 (2008), 2344–2349.
47. Yamaguchi, K., Mandai, M., Oura, T., Matsumura, N., Hamanishi, J., Baba, T., Matsui, S., Murphy, S.K., Konishi, I., Identification of an ovarian clear cell carcinoma gene signature that reflects inherent disease biology and the carcinogenic processes. Oncogene 29 (2010), 1741–1752.
48. Yamamoto, S., Tsuda, H., Takano, M., Tamai, S., Matsubara, O., Loss of ARID1A protein expression occurs as an early event in ovarian clear-cell carcinoma development and frequently coexists with PIK3CA mutations. Mod. Pathol. 25 (2012), 615–624.
49. Zang, Z.J., Cutcutache, I., Poon, S.L., Zhang, S.L., McPherson, J.R., Tao, J., Rajasegaran, V., Heng, H.L., Deng, N., Gan, A., et al. Exome sequencing of gastric adenocarcinoma identifies recurrent somatic mutations in cell adhesion and chromatin remodeling genes. Nat. Genet. 44 (2012), 570–574.
50. Zhang, Y., Iratni, R., Erdjument-Bromage, H., Tempst, P., Reinberg, D., Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex. Cell 89 (1997), 357–364.
51. Zhang, Y., LeRoy, G., Seelig, H.P., Lane, W.S., Reinberg, D., The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95 (1998), 279–289.
52. Zhang, H.S., Gavin, M., Dahiya, A., Postigo, A.A., Ma, D., Luo, R.X., Harbour, J.W., Dean, D.C., Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell 101 (2000), 79–89.