Inactivating ARID1A tumor suppressor enhances TERT transcription and maintains telomere length in cancer cells

Journal of Biological Chemistry

Volumn 291, Issue 18, 2016, Pages 9690-9699

  Rahmanto, Yohan Suryo ^a,b   Jung, Jin Gyoung ^a,b   Wu, Ren Chin ^a,b,c   Kobayashi, Yusuke ^a,b,d   Heaphy, Christopher M ^a,b   Meeker, Alan K ^a,b   Wang, Tian Li ^a,b   Shih, Ie Ming ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c CHANG GUNG UNIVERSITY   (Taiwan)

^d KEIO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOMES; DISEASES; GENES; PROTEINS; TUMORS;

CHROMATIN REMODELING; HUMAN TELOMERASE REVERSE TRANSCRIPTASE; PROTEIN EXPRESSIONS; REGULATORY ELEMENTS; TRANSCRIPTIONAL ACTIVITY; TRANSCRIPTIONAL REGULATION; TUMOR SUPPRESSOR GENES; TUMOR SUPPRESSORS;

TRANSCRIPTION;

ARID1A PROTEIN; MESSENGER RNA; ONCOPROTEIN; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR SIN3A; UNCLASSIFIED DRUG; ARID1A PROTEIN, HUMAN; HISTONE; NUCLEAR PROTEIN; REPRESSOR PROTEIN; SIN3A TRANSCRIPTION FACTOR; TERT PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ARID1A GENE; ARTICLE; CANCER CELL; CHROMATIN IMMUNOPRECIPITATION; CLEAR CELL CARCINOMA; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME ACTIVITY; FEMALE; GENE INACTIVATION; GENE MUTATION; GENE SILENCING; HISTONE MODIFICATION; HUMAN; HUMAN CELL; OVARIAN CLEAR CELL CARCINOMA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TELOMERE; TELOMERE LENGTH; TERT GENE; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; NEOPLASM; PATHOLOGY; TELOMERE HOMEOSTASIS; TUMOR CELL LINE;

CELL LINE, TUMOR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; MUTATION; NEOPLASMS; NUCLEAR PROTEINS; REPRESSOR PROTEINS; TELOMERASE; TELOMERE HOMEOSTASIS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 84983342683     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.707612     Document Type: Article

References (52)

1. Watanabe, R., Ui, A., Kanno, S., Ogiwara, H., Nagase, T., Kohno, T., and Yasui, A. (2014) SWI/SNF factors required for cellular resistance to DNA damage include ARID1A and ARID1B and show interdependent protein stability. Cancer Res. 74, 2465-2475
2. Clapier, C. R., and Cairns, B. R. (2009) The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273-304
3. Shen, J., Peng, Y., Wei, L., Zhang, W., Yang, L., Lan, L., Kapoor, P., Ju, Z., Mo, Q., Shih, I. M., Uray, I. P., Wu, X., Brown, P. H., Shen, X., Mills, G. B., and Peng, G. (2015) ARID1A deficiency impairs the DNA damage checkpoint and sensitizes cells to PARP inhibitors. Cancer Discov. 5, 752-767
4. Jones, S., Wang, T. L., Shih, I. M., Mao, T. L., Nakayama, K., Roden, R., Glas, R., Slamon, D., Diaz, L. A., Jr., Vogelstein, B., Kinzler, K. W., Velculescu, V. E., and Papadopoulos, N. (2010) Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 330, 228-231
5. 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., Yang, W., Heravi-Moussavi, A., Giuliany, R., Chow, C., Fee, J., et al. (2010) ARID1A mutations in endometriosis-associated ovarian carcinomas. New Engl. J. Med. 363, 1532-1543
6. Wilson, B. G., and Roberts, C. W. (2011) SWI/SNF nucleosome remodellers and cancer. Nat. Rev. Cancer 11, 481-492
7. Wu, R. C., Wang, T. L., and Shih, I. M. (2014) The emerging roles of ARID1A in tumor suppression. Cancer Biol. Ther. 15, 655-664
8. Guan, B., Wang, T. L., and Shih, I. M. (2011) ARID1A, a factor that promotes formation of SWI/SNF-mediated chromatin remodeling, is a tumor suppressor in gynecologic cancers. Cancer Res. 71, 6718-6727
9. Mamo, A., Cavallone, L., Tuzmen, S., Chabot, C., Ferrario, C., Hassan, S., Edgren, H., Kallioniemi, O., Aleynikova, O., Przybytkowski, E., Malcolm, K., Mousses, S., Tonin, P. N., and Basik, M. (2012) An integrated genomic approach identifies ARID1A as a candidate tumor-suppressor gene in breast cancer. Oncogene 31, 2090-2100
10. Wu, J. N., and Roberts, C. W. (2013) ARID1A mutations in cancer: another epigenetic tumor suppressor? Cancer Discov. 3, 35-43
11. Guan, B., Rahmanto, Y. S., Wu, R. C., Wang, Y., Wang, Z., Wang, T. L., and Shih, Ie-M. (2014) Roles of deletion of Arid1a, a tumor suppressor, in mouse ovarian tumorigenesis. J. Natl. Cancer Inst. 106, dju146
12. 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., Darr, D. B., Pardo-Manuel de Villena, F., Kim, W. Y., and Magnuson, T. (2015) Coexistent ARID1A-PIK3CA mutations promote ovarian clear-cell tumorigenesis through pro-tumorigenic inflammatory cytokine signalling. Nat. Commun. 6, 6118
13. Chan, T. L., Zhao, W., Leung, S. Y., and Yuen, S. T. (2003) BRAF and KRAS mutations in colorectal hyperplastic polyps and serrated adenomas. Cancer Res. 63, 4878-4881
14. Singer, G., Oldt, R., 3rd, Cohen, Y., Wang, B. G., Sidransky, D., Kurman, R. J., and Shih, I. M. (2003) Mutations in BRAF and KRAS characterize the development of low-grade ovarian serous carcinoma. J. Natl. Cancer Inst. 95, 484-486
15. Ardighieri, L., Zeppernick, F., Hannibal, C. G., Vang, R., Cope, L., Junge, J., Kjaer, S. K., Kurman, R. J., and Shih, I. M. (2014) Mutational analysis of BRAF and KRAS in ovarian serous borderline (atypical proliferative) tumours and associated peritoneal implants. J. Pathol. 232, 16-22
16. Wu, R. C., Ayhan, A., Maeda, D., Kim, K. R., Clarke, B. A., Shaw, P., Chui, M. H., Rosen, B., Shih, I. M., and Wang, T. L. (2014) Frequent somatic mutations of the telomerase reverse transcriptase promoter in ovarian clear cell carcinoma but not in other major types of gynaecological malignancy. J. Pathol. 232, 473-481
17. Horn, S., Figl, A., Rachakonda, P. S., Fischer, C., Sucker, A., Gast, A., Kadel, S., Moll, I., Nagore, E., Hemminki, K., Schadendorf, D., and Kumar, R. (2013) TERT promoter mutations in familial and sporadic melanoma. Science 339, 959-961
18. Huang, F. W., Hodis, E., Xu, M. J., Kryukov, G. V., Chin, L., and Garraway, L. A. (2013) Highly recurrent TERT promoter mutations in human melanoma. Science 339, 957-959
19. Killela, P. J., Reitman, Z. J., Jiao, Y., Bettegowda, C., Agrawal, N., Diaz, L. A., Jr., Friedman, A. H., Friedman, H., Gallia, G. L., Giovanella, B. C., Grollman, A. P., He, T. C., He, Y., Hruban, R. H., Jallo, G. I., et al. (2013) TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. Proc. Natl. Acad. Sci. U. S. A. 110, 6021-6026
20. Nault, J. C., Mallet, M., Pilati, C., Calderaro, J., Bioulac-Sage, P., Laurent, C., Laurent, A., Cherqui, D., Balabaud, C., and Zucman Rossi, J. (2013) High frequency of telomerase reverse-transcriptase promoter somatic mutations in hepatocellular carcinoma and preneoplastic lesions. Nat. Commun. 4, 2218
21. Vinagre, J., Almeida, A., Pópulo, H., Batista, R., Lyra, J., Pinto, V., Coelho, R., Celestino, R., Prazeres, H., Lima, L., Melo, M., da Rocha, A. G., Preto, A., Castro, P., Castro, L., et al. (2013) Frequency of TERT promoter mutations in human cancers. Nat. Commun. 4, 2185
22. Borah, S., Xi, L., Zaug, A. J., Powell, N. M., Dancik, G. M., Cohen, S. B., Costello, J. C., Theodorescu, D., and Cech, T. R. (2015) Cancer. TERT promoter mutations and telomerase reactivation in urothelial cancer. Science 347, 1006-1010
23. Bell, R. J., Rube, H. T., Kreig, A., Mancini, A., Fouse, S. D., Nagarajan, R. P., Choi, S., Hong, C., He, D., Pekmezci, M., Wiencke, J. K., Wrensch, M. R., Chang, S. M., Walsh, K. M., Myong, S., et al. (2015) Cancer: the transcription factor GABP selectively binds and activates the mutant TERT promoter in cancer. Science 348, 1036-1039
24. Stern, J. L., Theodorescu, D., Vogelstein, B., Papadopoulos, N., and Cech, T. R. (2015) Mutation of the TERT promoter, switch to active chromatin, and monoallelic TERT expression in multiple cancers. Genes Dev. 29, 2219-2224
25. Lin, S. Y., and Elledge, S. J. (2003) Multiple tumor suppressor pathways negatively regulate telomerase. Cell 113, 881-889
26. Moore, C. B., and Allen, I. C. (2013) Primary ear fibroblast derivation from mice. Methods Mol. Biol. 1031, 65-70
27. Guan, B., Gao, M., Wu, C. H., Wang, T. L., and Shih, I. M. (2012) Functional analysis of in-frame indel ARID1A mutations reveals new regulatory mechanisms of its tumor suppressor functions. Neoplasia 14, 986-993
28. Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., and Zhang, F. (2013) Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308
29. Cawthon, R. M. (2002) Telomere measurement by quantitative PCR. Nucleic Acids Res. 30, e47
30. Gil, M. E., and Coetzer, T. L. (2004) Real-time quantitative PCR of telomere length. Mol. Biotechnol. 27, 169-172
31. Heaphy, C. M., de Wilde, R. F., Jiao, Y., Klein, A. P., Edil, B. H., Shi, C., Bettegowda, C., Rodriguez, F. J., Eberhart, C. G., Hebbar, S., Offerhaus, G. J., McLendon, R., Rasheed, B. A., He, Y., Yan, H., et al. (2011) Altered telomeres in tumors with ATRX and DAXX mutations. Science 333, 425
32. Nakayama, J., Tahara, H., Tahara, E., Saito, M., Ito, K., Nakamura, H., Nakanishi, T., Tahara, E., Ide, T., and Ishikawa, F. (1998) Telomerase activation by hTRT in human normal fibroblasts and hepatocellular carcinomas. Nat. Genet. 18, 65-68
33. Wege, H., Chui, M. S., Le, H. T., Tran, J. M., and Zern, M. A. (2003) SYBR Green real-time telomeric repeat amplification protocol for the rapid quantification of telomerase activity. Nucleic Acids Res. 31, E3-3
34. Euskirchen, G., Auerbach, R. K., and Snyder, M. (2012) SWI/SNF chromatin-remodeling factors: multiscale analyses and diverse functions. J. Biol. Chem. 287, 30897-30905
35. Nagl, N. G., Jr., Wang, X., Patsialou, A., Van Scoy, M., and Moran, E. (2007) Distinct mammalian SWI/SNF chromatin remodeling complexes with opposing roles in cell-cycle control. EMBO J. 26, 752-763
36. Wahlström, T., Belikov, S., and Arsenian Henriksson, M. (2013) Chromatin dynamics at the hTERT promoter during transcriptional activation and repression by c-Myc and Mnt inXenopus leavis oocytes. Exp. Cell Res. 319, 3160-3169
37. Silverstein, R. A., and Ekwall, K. (2005) Sin3: a flexible regulator of global gene expression and genome stability. Curr. Genet. 47, 1-17
38. Xu, M., Luo, W., Elzi, D. J., Grandori, C., and Galloway, D. A. (2008) NFX1 interacts with mSin3A/histone deacetylase to repress hTERT transcription in keratinocytes. Mol. Cell Biol. 28, 4819-4828
39. Chen, X., Kamranvar, S. A., and Masucci, M. G. (2014) Tumor viruses and replicative immortality: avoiding the telomere hurdle. Semin. Cancer Biol. 26, 43-51
40. Günes, C., and Rudolph, K. L. (2013) The role of telomeres in stem cells and cancer. Cell 152, 390-393
41. Clynes, D., Jelinska, C., Xella, B., Ayyub, H., Scott, C., Mitson, M., Taylor, S., Higgs, D. R., and Gibbons, R. J. (2015) Suppression of the alternative lengthening of telomere pathway by the chromatin remodelling factor ATRX. Nat. Commun. 6, 7538
42. Min, J. N., Tian, Y., Xiao, Y., Wu, L., Li, L., and Chang, S. (2013) The mINO80 chromatin remodeling complexisrequired for efficient telomere replication and maintenance of genome stability. Cell Res. 23, 1396-1413
43. Artandi, S. E., and DePinho, R. A. (2010) Telomeres and telomerase in cancer. Carcinogenesis 31, 9-18
44. Kyo, S., and Inoue, M. (2002) Complex regulatory mechanisms of telomerase activity in normal and cancer cells: how can we apply them for cancer therapy? Oncogene 21, 688-697
45. Bryan, T. M., Englezou, A., Gupta, J., Bacchetti, S., and Reddel, R. R. (1995) Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J. 14, 4240-4248
46. Heaphy, C. M., Subhawong, A. P., Hong, S. M., Goggins, M. G., Montgomery, E. A., Gabrielson, E., Netto, G. J., Epstein, J. I., Lotan, T. L., Westra, W. H., Shih, I. M., Iacobuzio-Donahue, C. A., Maitra, A., Li, Q. K., Eberhart, C. G., et al. (2011) Prevalence ofthe alternative lengthening oftelomeres telomere maintenance mechanism in human cancer subtypes. Am. J. Pathol. 179, 1608-1615
47. Wu, S., Ge, Y., Huang, L., Liu, H., Xue, Y., and Zhao, Y. (2014) BRG1, the ATPase subunit of SWI/SNF chromatin remodeling complex, interacts with HDAC2 to modulate telomerase expression in human cancer cells. Cell Cycle 13, 2869-2878
48. Kortschak, R. D., Tucker, P. W., and Saint, R. (2000) ARID proteins come in from the desert. Trends Biochem. Sci. 25, 294-299
49. Nair, S. S., and Kumar, R. (2012) Chromatin remodeling in cancer: a gateway to regulate gene transcription. Mol. Oncol. 6, 611-619
50. Pal, S., Yun, R., Datta, A., Lacomis, L., Erdjument-Bromage, H., Kumar, J., Tempst, P., and Sif, S. (2003) mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol. Cell Biol. 23, 7475-7487
51. Koh, C. M., Khattar, E., Leow, S. C., Liu, C. Y., Muller, J., Ang, W. X., Li, Y., Franzoso, G., Li, S., Guccione, E., and Tergaonkar, V. (2015) Telomerase regulates MYC-driven oncogenesis independent of its reverse transcriptase activity. J. Clin. Invest. 125, 2109-2122
52. Ayhan, A., Mao, T. L., Seckin, T., Wu, C. H., Guan, B., Ogawa, H., Futagami, M., Mizukami, H., Yokoyama, Y., Kurman, R. J., and Shih, I. M. (2012) Loss of ARID1A expression is an early molecular event in tumor progression from ovarian endometriotic cyst to clear cell and endometrioid carcinoma. Int. J. Gynecol. Cancer 22, 1310-1315