DNA methylation-mediated repression of miR-941 enhances lysine (K)-specific demethylase 6B expression in hepatoma cells

Journal of Biological Chemistry

Volumn 289, Issue 35, 2014, Pages 24724-24735

  Zhang, Pei Pei ^a   Wang, Xiang Ling ^a   Zhao, Wei ^a   Qi, Bing ^a   Yang, Qian ^a   Wan, Hai Ying ^a   Shuang, Ze Yu ^b   Liu, Min ^a   Li, Xin ^a   Li, Shengping ^b   Tang, Hua ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL CULTURE; CELL PROLIFERATION; PATHOLOGY; RNA;

ECTOPIC EXPRESSIONS; EPIGENETIC SILENCING; EPITHELIAL-MESENCHYMAL TRANSITION; HEPATOCELLULAR CARCINOMA; HYPERMETHYLATION; OVER-EXPRESSION; PHENOTYPIC CHANGES; TUMOR SUPPRESSION;

TUMORS;

HISTONE DEMETHYLASE; LYSINE SPECIFIC DEMETHYLASE 6B; MICRORNA; MICRORNA 941; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; KDM6B PROTEIN, HUMAN; MESSENGER RNA; MIRN941 MICRORNA, HUMAN; PRIMER DNA;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE MUTATION; HEPATOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; KDM6B GENE; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; ONCOGENE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; UPREGULATION; ENZYMOLOGY; GENETICS; LIVER TUMOR; NUCLEOTIDE SEQUENCE; PATHOLOGY; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DNA METHYLATION; DNA PRIMERS; DOWN-REGULATION; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; LIVER NEOPLASMS; MICRORNAS; RNA, MESSENGER;

EID: 84906871291     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.567818     Document Type: Article

References (49)

1. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297
2. Esquela-Kerscher, A., and Slack, F. J. (2006) Oncomirs: microRNAs with a role in cancer. Nat. Rev. Cancer 6, 259-269
3. Song, S. J., Poliseno, L., Song, M. S., Ala, U., Webster, K., Ng, C., Beringer, G., Brikbak, N. J., Yuan, X., Cantley, L. C., Richardson, A. L., and Pandolfi, P. P. (2013) MicroRNA-antagonism regulates breast cancer stemness and metastasis via TET family-dependent chromatin remodeling. Cell 154, 311-324
4. Calin, G. A., Liu, C. G., Sevignani, C., Ferracin, M., Felli, N., Dumitru, C. D., Shimizu, M., Cimmino, A., Zupo, S., Dono, M., Dell'Aquila, M. L., Alder, H., Rassenti, L., Kipps, T. J., Bullrich, F., Negrini, M., and Croce, C. M. (2004) MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proc. Natl. Acad. Sci. U.S.A. 101, 11755-11760 (Pubitemid 39095368)
5. Pallante, P., Visone, R., Ferracin, M., Ferraro, A., Berlingieri, M. T., Troncone, G., Chiappetta, G., Liu, C. G., Santoro, M., Negrini, M., Croce, C. M., and Fusco, A. (2006) MicroRNA deregulation in human thyroid papillary carcinomas. Endocr. Relat. Cancer 13, 497-508 (Pubitemid 43886672)
6. Yan, Y., Luo, Y. C., Wan, H. Y., Wang, J., Zhang, P. P., Liu, M., Li, X., Li, S., and Tang, H. (2013 miR-10a is involved in metastatic process by regulating EphA4-mediated epithelial-mesenchymal transition and adhesion in hepatoma cells. Hepatology 57, 667-677
7. Zhang, J. F., He, M. L., Fu, W. M., Wang, H., Chen, L. Z., Zhu, X., Chen, Y., Xie, D., Lai, P., Chen, G., Lu, G., Lin, M. C., and Kung, H. F. (2011) Primate-specific microRNA-637 inhibits tumorigenesis in hepatocellular carcinoma by disrupting signal transducer and activator of transcription 3 signaling. Hepatology 54, 2137-2148
8. El-Serag, H. B., and Rudolph, K. L. (2007) Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132, 2557-2576 (Pubitemid 46890874)
9. Zhang, L. Y., Liu, M., Li, X., and Tang, H. (2013) MiR-490-3p modulates cell growth and epithelial to mesenchymal transition of hepatocellular carcinoma cells by targeting endoplasmic reticulum-Golgi intermediate compartment protein 3*(ERGIC3). J. Biol. Chem. 288, 4035-4047
10. Meng, F., Henson, R., Wehbe-Janek, H., Ghoshal, K., Jacob, S. T., and Patel, T. (2007) MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133, 647-658 (Pubitemid 47187346)
11. Hou, Y. Y., Cao, W. W., Li, L., Li, S. P., Liu, T., Wan, H. Y., Liu, M., Li, X., and Tang, H. (2011) MicroRNA-519d targets MKi67 and suppresses cell growth in the hepatocellular carcinoma cell line QGY-7703. Cancer Lett. 307, 182-190
12. Díaz-Martín, J., Díaz-López, A., Moreno-Bueno, G., Castilla, M. Á., Rosa-Rosa, J. M., Cano, A., and Palacios, J. (2014) A core microRNA signature associated with inducers of the epithelial-to-mesenchymal transition. J. Pathol. 232, 319-329
13. Ding, X. M. (2014) MicroRNAs: regulators of cancer metastasis and epithelial-mesenchymal transition (EMT). Chin. J. Cancer 33, 140-147
14. Thiery, J. P., Acloque, H., Huang, R. Y., and Nieto, M. A. (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890
15. Watts, G. S., Futscher, B. W., Holtan, N., Degeest, K., Domann, F. E., and Rose, S. L. (2008) DNA methylation changes in ovarian cancer are cumulative with disease progression and identify tumor stage. BMC Med. Genomics 1, 47
16. Aran, D., and Hellman, A. (2013) DNA methylation of transcriptional enhancers and cancer predisposition. Cell 154, 11-13
17. Saito, Y., Liang, G., Egger, G., Friedman, J. M., Chuang, J. C., Coetzee, G. A., and Jones, P. A. (2006) Specific activation of microRNA-127 with down-regulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 9, 435-443 (Pubitemid 43832188)
18. Lujambio, A., Ropero, S., Ballestar, E., Fraga, M. F., Cerrato, C., Setién, F., Casado, S., Suarez-Gauthier, A., Sanchez-Cespedes, M., Git, A., Gitt, A., Spiteri, I., Das, P. P., Caldas, C., Miska, E., and Esteller, M. (2007) Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res. 67, 1424-1429 (Pubitemid 46383366)
19. Han, L., Witmer, P. D., Casey, E., Valle, D., and Sukumar, S. (2007) DNA methylation regulates microRNA expression. Cancer Biol. Ther. 6, 1284-1288 (Pubitemid 351590384)
20. Agger, K., Cloos, P. A., Christensen, J., Pasini, D., Rose, S., Rappsilber, J., Issaeva, I., Canaani, E., Salcini, A. E., and Helin, K. (2007) UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449, 731-734 (Pubitemid 47552088)
21. Hong, S., Cho, Y. W., Yu, L. R., Yu, H., Veenstra, T. D., and Ge, K. (2007) Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc. Natl. Acad. Sci. U.S.A. 104, 18439-18444 (Pubitemid 350210715)
22. Sen, G. L., Webster, D. E., Barragan, D. I., Chang, H. Y., and Khavari, P. A. (2008) Control of differentiation in a self-renewing mammalian tissue by the histone demethylase JMJD3. Genes Dev. 22, 1865-1870 (Pubitemid 352008635)
23. Lan, F., Bayliss, P. E., Rinn, J. L., Whetstine, J. R., Wang, J. K., Chen, S., Iwase, S., Alpatov, R., Issaeva, I., Canaani, E., Roberts, T. M., Chang, H. Y., and Shi, Y. (2007) A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449, 689-694 (Pubitemid 47552096)
24. Ichi, S., Costa, F. F., Bischof, J. M., Nakazaki, H., Shen, Y. W., Boshnjaku, V., Sharma, S., Mania-Farnell, B., McLone, D. G., Tomita, T., Soares, M. B., and Mayanil, C. S. (2010) Folic acid remodels chromatin on Hes1 and Neurog2 promoters during caudal neural tube development. J. Biol. Chem. 285, 36922-36932
25. Li, L. C., and Dahiya, R. (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18, 1427-1431
26. Jones, P. A., and Takai, D. (2001) The role of DNA methylation in mammalian epigenetics. Science 293, 1068-1070 (Pubitemid 32758075)
27. Saito, Y., Hibino, S., and Saito, H. (2014) Alterations of epigenetics and microRNA in hepatocellular carcinoma. Hepatol. Res. 44, 31-42
28. Goeppert, B., Schmezer, P., Dutruel, C., Oakes, C., Renner, M., Breinig, M., Warth, A., Vogel, M. N., Mittelbronn, M., Mehrabi, A., Gdynia, G., Penzel, R., Longerich, T., Breuhahn, K., Popanda, O., Plass, C., Schirmacher, P., and Kern, M. A. (2010) Down-regulation of tumor suppressor A kinase anchor protein 12 in human hepatocarcinogenesis by epigenetic mechanisms. Hepatology 52, 2023-2033
29. Xu, N., Zhang, L., Meisgen, F., Harada, M., Heilborn, J., Homey, B., Grandér, D., Ståhle, M., Sonkoly, E., and Pivarcsi, A. (2012) MicroRNA-125b down-regulates matrix metallopeptidase 13 and inhibits cutaneous squamous cell carcinoma cell proliferation, migration, and invasion. J. Biol. Chem. 287, 29899-29908
30. Yamane, K., Tateishi, K., Klose, R. J., Fang, J., Fabrizio, L. A., Erdjument-Bromage, H., Taylor-Papadimitriou, J., Tempst, P., and Zhang, Y. (2007) PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol. Cell 25, 801-812 (Pubitemid 46436533)
31. van Haaften, G., Dalgliesh, G. L., Davies, H., Chen, L., Bignell, G., Greenman, C., Edkins, S., Hardy, C., O'Meara, S., Teague, J., Butler, A., Hinton, J., Latimer, C., Andrews, J., Barthorpe, S., Beare, D., Buck, G., Campbell, P. J., Cole, J., Forbes, S., Jia, M., Jones, D., Kok, C. Y., Leroy, C., Lin, M. L., McBride, D. J., Maddison, M., Maquire, S., McLay, K., Menzies, A., Mironenko, T., Mulderrig, L., Mudie, L., Pleasance, E., Shepherd, R., Smith, R., Stebbings, L., Stephens, P., Tang, G., Tarpey, P. S., Turner, R., Turrell, K., Varian, J., West, S., Widaa, S., Wray, P., Collins, V. P., Ichimura, K., Law, S., Wong, J., Yuen, S. T., Leung, S. Y., Tonon, G., DePinho, R. A., Tai, Y. T., Anderson, K. C., Kahnoski, R. J., Massie, A., Khoo, S. K., Teh, B. T., Stratton, M. R., and Futreal, P. A. (2009) Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nat. Genet. 41, 521-523
32. Dalgliesh, G. L., Furge, K., Greenman, C., Chen, L., Bignell, G., Butler, A., Davies, H., Edkins, S., Hardy, C., Latimer, C., Teague, J., Andrews, J., Barthorpe, S., Beare, D., Buck, G., Campbell, P. J., Forbes, S., Jia, M., Jones, D., Knott, H., Kok, C. Y., Lau, K. W., Leroy, C., Lin, M. L., McBride, D. J., Maddison, M., Maguire, S., McLay, K., Menzies, A., Mironenko, T., Mulderrig, L., Mudie, L., O'Meara, S., Pleasance, E., Rajasingham, A., Shepherd, R., Smith, R., Stebbings, L., Stephens, P., Tang, G., Tarpey, P. S., Turrell, K., Dykema, K. J., Khoo, S. K., Petillo, D., Wondergem, B., Anema, J., Kahnoski, R. J., Teh, B. T., Stratton, M. R., and Futreal, P. A. (2010) Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature 463, 360-363
33. Pereira, F., Barbáchano, A., Silva, J., Bonilla, F., Campbell, M. J., Muñoz, A., and Larriba, M. J. (2011) KDM6B/JMJD3 histone demethylase is induced by vitamin D and modulates its effects in colon cancer cells. Hum. Mol. Genet. 20, 4655-4665
34. De Santa, F., Totaro, M. G., Prosperini, E., Notarbartolo, S., Testa, G., and Natoli, G. (2007) The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130, 1083-1094 (Pubitemid 47410272)
35. Barradas, M., Anderton, E., Acosta, J. C., Li, S., Banito, A., Rodriguez-Niedenführ, M., Maertens, G., Banck, M., Zhou, M. M., Walsh, M. J., Peters, G., and Gil, J. (2009) Histone demethylase JMJD3 contributes to epigenetic control of INK4a/ARF by oncogenic RAS. Genes Dev. 23, 1177-1182
36. Agger, K., Cloos, P. A., Rudkjaer, L., Williams, K., Andersen, G., Christensen, J., and Helin, K. (2009) The H3K27me3 demethylase JMJD3 contributes to the activation of the INK4A-ARF locus in response to oncogene-and stress-induced senescence. Genes Dev. 23, 1171-1176
37. Ene, C. I., Edwards, L., Riddick, G., Baysan, M., Woolard, K., Kotliarova, S., Lai, C., Belova, G., Cam, M., Walling, J., Zhou, M., Stevenson, H., Kim, H. S., Killian, K., Veenstra, T., Bailey, R., Song, H., Zhang, W., and Fine, H. A. (2012) Histone demethylase Jumonji D3 (JMJD3) as a tumor suppressor by regulating p53 protein nuclear stabilization. PLoS One 7, e51407
38. McLaughlin-Drubin, M. E., Crum, C. P., and Münger, K. (2011) Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc. Natl. Acad. Sci. U.S.A. 108, 2130-2135
39. Xiang, Y., Zhu, Z., Han, G., Lin, H., Xu, L., and Chen, C. D. (2007) JMJD3 is a histone H3K27 demethylase. Cell Res. 17, 850-857 (Pubitemid 47585113)
40. Anderton, J. A., Bose, S., Vockerodt, M., Vrzalikova, K., Wei, W., Kuo, M., Helin, K., Christensen, J., Rowe, M., Murray, P. G., and Woodman, C. B. (2011) The H3K27me3 demethylase, KDM6B, is induced by Epstein-Barr virus and over-expressed in Hodgkin's lymphoma. Oncogene 30, 2037-2043
41. Svotelis, A., Bianco, S., Madore, J., Huppé, G., Nordell-Markovits, A., Mes-Masson, A. M., and Gévry, N. (2011) H3K27 demethylation by JMJD3 at a poised enhancer of anti-apoptotic gene BCL2 determines ERα ligand dependency. EMBO J. 30, 3947-3961
42. Shen, Y., Guo, X., Wang, Y., Qiu, W., Chang, Y., Zhang, A., and Duan, X. (2012) Expression and significance of histone H3K27 demethylases in renal cell carcinoma. BMC Cancer 12, 470
43. Gregory, P. A., Bracken, C. P., Bert, A. G., and Goodall, G. J. (2008) MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle 7, 3112-3118
44. Kraljevic Pavelic, S., Sedic, M., Bosnjak, H., Spaventi, S., and Pavelic, K. (2011) Metastasis: new perspectives on an old problem. Mol. Cancer 10, 22
45. Kajita, M., McClinic, K. N., and Wade, P. A. (2004) Aberrant expression of the transcription factors snail and slug alters the response to genotoxic stress. Mol. Cell. Biol. 24, 7559-7566 (Pubitemid 39121483)
46. Vega, S., Morales, A. V., Ocaña, O. H., Valdés, F., Fabregat, I., and Nieto, M. A. (2004) Snail blocks the cell cycle and confers resistance to cell death. Genes Dev. 18, 1131-1143 (Pubitemid 38669034)
47. Zhang, J. P., Zeng, C., Xu, L., Gong, J., Fang, J. H., and Zhuang, S. M. (2013) MicroRNA-148a suppresses the epithelial-mesenchymal transition and metastasis of hepatoma cells by targeting Met/Snail signaling. Oncogene 33, 4069-4076
48. Kroepil, F., Fluegen, G., Totikov, Z., Baldus, S. E., Vay, C., Schauer, M., Topp, S. A., Esch, J. S., Knoefel, W. T., and Stoecklein, N. H. (2012) Downregulation of CDH1 is associated with expression of SNAI1 in colorectal adenomas. PLoS One 7, e46665
49. Ramadoss, S., Chen, X., and Wang, C. Y. (2012) Histone demethylase KDM6B promotes epithelial-mesenchymal transition. J. Biol. Chem. 287, 44508-44517