Global histone modification profiling reveals the epigenomic dynamics during malignant transformation in a Four-Stage breast cancer model

Clinical Epigenetics

Volumn 8, Issue 1, 2016, Pages

  Zhao, Quan Yi ^a   Lei, Pin Ji ^a   Zhang, Xiaoran ^b   Zheng, Jun Yi ^a   Wang, Hui Yi ^a   Zhao, Jiao ^a   Li, Yi Ming ^a   Ye, Mei ^a   Li, Lianyun ^a   Wei, Gang ^b   Wu, Min ^a  

^a WUHAN UNIVERSITY   (China)

^b Chinese Academy of Sciences   (China)

Author keywords

Breast cancer transformation; Epigenomics; H3K9 methylation; KDM3A; Transcription regulation

Indexed keywords

HISTONE DEMETHYLASE; HISTONE H3; KDM3A PROTEIN; UNCLASSIFIED DRUG; HISTONE; KDM3A PROTEIN, HUMAN;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER INHIBITION; CANCER MODEL; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; ENZYME DEFICIENCY; EPIGENETICS; GENE; GENE EXPRESSION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALIGNANT TRANSFORMATION; NEXT GENERATION SEQUENCING; ONCOGENE; ONCOGENE MYC; PAX3 GENE; PRIORITY JOURNAL; PROTEIN BINDING; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; WESTERN BLOTTING; ANIMAL; BREAST TUMOR; CELL TRANSFORMATION; DISEASE MODEL; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; MCF-7 CELL LINE; METABOLISM; METHYLATION; MOUSE; NUDE MOUSE; PATHOLOGY; PROCEDURES; TUMOR CELL LINE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; EPIGENESIS, GENETIC; EPIGENOMICS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MCF-7 CELLS; METHYLATION; MICE; MICE, NUDE;

EID: 85007071957     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-016-0201-x     Document Type: Article

References (47)

1. Rodriguez-Paredes M, Esteller M. Cancer epigenetics reaches mainstream oncology. Nat Med. 2011;17(3):330-9. doi:10.1038/nm.2305.
2. Lawrence MS, Stojanov P, Mermel CH, Robinson JT, Garraway LA, Golub TR, et al. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature. 2014;505(7484):495-501. doi:10.1038/nature12912.
3. Easwaran H, Tsai HC, Baylin SB. Cancer epigenetics: tumor heterogeneity, plasticity of stem-like states, and drug resistance. Mol Cell. 2014;54(5):716-27. doi:10.1016/j.molcel.2014.05.015.
4. Kandoth C, McLellan MD, Vandin F, Ye K, Niu B, Lu C, et al. Mutational landscape and significance across 12 major cancer types. Nature. 2013; 502(7471):333-9. doi:10.1038/nature12634.
5. Watson IR, Takahashi K, Futreal PA, Chin L. Emerging patterns of somatic mutations in cancer. Nat Rev Genet. 2013;14(10):703-18. doi:10.1038/nrg3539.
6. Esteller M. Epigenetics in cancer. N Engl J Med. 2008;358(11):1148-59. doi:10.1056/NEJMra072067.
7. Ellis L, Atadja PW, Johnstone RW. Epigenetics in cancer: targeting chromatin modifications. Mol Cancer Ther. 2009;8(6):1409-20. doi:10.1158/1535-7163. MCT-08-0860.
8. Seligson DB, Horvath S, Shi T, Yu H, Tze S, Grunstein M, et al. Global histone modification patterns predict risk of prostate cancer recurrence. Nature. 2005;435(7046):1262-6. doi:10.1038/nature03672.
9. Seligson DB, Horvath S, McBrian MA, Mah V, Yu H, Tze S, et al. Global levels of histone modifications predict prognosis in different cancers. Am J Pathol. 2009;174(5):1619-28. doi:10.2353/ajpath.2009.080874.
10. Elsheikh SE, Green AR, Rakha EA, Powe DG, Ahmed RA, Collins HM, et al. Global histone modifications in breast cancer correlate with tumor phenotypes, prognostic factors, and patient outcome. Cancer Res. 2009; 69(9):3802-9. doi:10.1158/0008-5472.CAN-08-3907.
11. Sharma S, Kelly TK, Jones PA. Epigenetics in cancer. Carcinogenesis. 2010; 31(1):27-36. doi:10.1093/carcin/bgp220.
12. Herz HM, Garruss A, Shilatifard A. SET for life: biochemical activities and biological functions of SET domain-containing proteins. Trends Biochem Sci. 2013;38(12):621-39. doi:10.1016/j.tibs.2013.09.004.
13. Black JC, Van Rechem C, Whetstine JR. Histone lysine methylation dynamics: establishment, regulation, and biological impact. Mol Cell. 2012;48(4):491-507. doi:10.1016/j.molcel.2012.11.006.
14. Liu Y, Liu K, Qin S, Xu C, Min J. Epigenetic targets and drug discovery: part 1: histone methylation. Pharmacol Ther. 2014;143(3):275-94. doi:10.1016/j. pharmthera.2014.03.007.
15. Xu K, Wu ZJ, Groner AC, He HH, Cai C, Lis RT, et al. EZH2 oncogenic activity in castration-resistant prostate cancer cells is polycomb-independent. Science. 2012;338(6113):1465-9. doi:10.1126/science.1227604.
16. Morin RD, Johnson NA, Severson TM, Mungall AJ, An J, Goya R, et al. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat Genet. 2010;42(2):181-5. doi:10.1038/ng.518.
17. Beguelin W, Popovic R, Teater M, Jiang Y, Bunting KL, Rosen M, et al. EZH2 is required for germinal center formation and somatic EZH2 mutations promote lymphoid transformation. Cancer Cell. 2013;23(5):677-92. doi:10. 1016/j.ccr.2013.04.011.
18. McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS, et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature. 2012;492(7427):108-12. doi:10.1038/nature11606.
19. Ibragimova I, Maradeo ME, Dulaimi E, Cairns P. Aberrant promoter hypermethylation of PBRM1, BAP1, SETD2, KDM6A and other chromatinmodifying genes is absent or rare in clear cell RCC. Epigenetics. 2013;8(5): 486-93. doi:10.4161/epi.24552.
20. Cancer Genome Atlas Research N. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature. 2013;499(7456):43-9. doi:10.1038/ nature12222.
21. Fontebasso AM, Schwartzentruber J, Khuong-Quang DA, Liu XY, Sturm D, Korshunov A, et al. Mutations in SETD2 and genes affecting histone H3K36 methylation target hemispheric high-grade gliomas. Acta Neuropathol. 2013;125(5):659-69. doi:10.1007/s00401-013-1095-8.
22. Zhu X, He F, Zeng H, Ling S, Chen A, Wang Y, et al. Identification of functional cooperative mutations of SETD2 in human acute leukemia. Nat Genet. 2014;46(3):287-93. doi:10.1038/ng.2894.
23. Li F, Mao G, Tong D, Huang J, Gu L, Yang W, et al. The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSalpha. Cell. 2013;153(3):590-600. doi:10.1016/j.cell.2013.03.025.
24. Pfister SX, Ahrabi S, Zalmas LP, Sarkar S, Aymard F, Bachrati CZ, et al. SETD2-dependent histone H3K36 trimethylation is required for homologous recombination repair and genome stability. Cell reports. 2014;7(6):2006-18. doi:10.1016/j.celrep.2014.05.026.
25. Carvalho S, Vitor AC, Sridhara SC, Martins FB, Raposo AC, Desterro JM et al. SETD2 is required for DNA double-strand break repair and activation of the p53-mediated checkpoint. eLife. 2014:e02482. doi:10.7554/eLife.02482.
26. Black JC, Manning AL, Van Rechem C, Kim J, Ladd B, Cho J, et al. KDM4A lysine demethylase induces site-specific copy gain and rereplication of regions amplified in tumors. Cell. 2013;154(3):541-55. doi:10.1016/j.cell.2013.06.051.
27. Krieg AJ, Rankin EB, Chan D, Razorenova O, Fernandez S, Giaccia AJ. Regulation of the histone demethylase JMJD1A by hypoxia-inducible factor 1 alpha enhances hypoxic gene expression and tumor growth. Mol Cell Biol. 2010;30(1):344-53. doi:10.1128/MCB.00444-09.
28. Chen L, Fu L, Kong X, Xu J, Wang Z, Ma X, et al. Jumonji domain-containing protein 2B silencing induces DNA damage response via STAT3 pathway in colorectal cancer. Br J Cancer. 2014;110(4):1014-26. doi:10.1038/bjc.2013.808.
29. Young LC, Hendzel MJ. The oncogenic potential of Jumonji D2 (JMJD2/ KDM4) histone demethylase overexpression. Biochem Cell Biol. 2013;91(6): 369-77. doi:10.1139/bcb-2012-0054.
30. Mallette FA, Richard S. JMJD2A promotes cellular transformation by blocking cellular senescence through transcriptional repression of the tumor suppressor CHD5. Cell reports. 2012;2(5):1233-43. doi:10.1016/j.celrep.2012.09.033.
31. Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell. 2010;141(1):69-80. doi:10.1016/j.cell.2010.02.027.
32. Saeed S, Quintin J, Kerstens HH, Rao NA, Aghajanirefah A, Matarese F, et al. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science. 2014;345(6204):1251086. doi:10.1126/ science.1251086.
33. Hahn WC, Counter CM, Lundberg AS, Beijersbergen RL, Brooks MW, Weinberg RA. Creation of human tumour cells with defined genetic elements. Nature. 1999;400(6743):464-8. doi:10.1038/22780.
34. Elenbaas B, Spirio L, Koerner F, Fleming MD, Zimonjic DB, Donaher JL, et al. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev. 2001;15(1):50-65.
35. Danielsson F, Skogs M, Huss M, Rexhepaj E, O’Hurley G, Klevebring D, et al. Majority of differentially expressed genes are down-regulated during malignant transformation in a four-stage model. Proc Natl Acad Sci U S A. 2013;110(17):6853-8. doi:10.1073/pnas.1216436110.
36. Putiri EL, Tiedemann RL, Liu C, Choi JH, Robertson KD. Impact of human MLL/COMPASS and polycomb complexes on the DNA methylome. Oncotarget. 2014;5(15):6338-52.
37. Reddington JP, Perricone SM, Nestor CE, Reichmann J, Youngson NA, Suzuki M, et al. Redistribution of H3K27me3 upon DNA hypomethylation results in de-repression of polycomb target genes. Genome Biol. 2013;14(3):R25. doi:10.1186/gb-2013-14-3-r25.
38. Wen B, Wu H, Shinkai Y, Irizarry RA, Feinberg AP. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat Genet. 2009;41(2):246-50. doi:10.1038/ng.297.
39. Meyer N, Penn LZ. Reflecting on 25 years with MYC. Nat Rev Cancer. 2008; 8(12):976-90. doi:10.1038/nrc2231.
40. Wang X, Zhu K, Li S, Liao Y, Du R, Zhang X, et al. MLL1, a H3K4 methyltransferase, regulates the TNFalpha-stimulated activation of genes downstream of NFkappaB. J Cell Sci. 2012;125(Pt 17):4058-66. doi:10.1242/jcs.103531.
41. Kuroki S, Matoba S, Akiyoshi M, Matsumura Y, Miyachi H, Mise N, et al. Epigenetic regulation of mouse sex determination by the histone demethylase Jmjd1a. Science. 2013;341(6150):1106-9. doi:10.1126/science.1239864.
42. Okada Y, Scott G, Ray MK, Mishina Y, Zhang Y. Histone demethylase JHDM2A is critical for Tnp1 and Prm1 transcription and spermatogenesis. Nature. 2007;450(7166):119-23. doi:10.1038/nature06236.
43. Wade MA, Jones D, Wilson L, Stockley J, Coffey K, Robson CN, et al. The histone demethylase enzyme KDM3A is a key estrogen receptor regulator in breast cancer. Nucleic Acids Res. 2015;43(1):196-207. doi:10.1093/nar/gku1298.
44. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009; 4(1):44-57. doi:10.1038/nprot.2008.211.
45. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754-60. doi:10.1093/bioinformatics/btp324.
46. Zang C, Schones DE, Zeng C, Cui K, Zhao K, Peng W. A clustering approach for identification of enriched domains from histone modification ChIP-seq data. Bioinformatics. 2009;25(15):1952-8. doi:10.1093/bioinformatics/btp340.
47. Zhao Q, Fan J, Hong W, Li L, Wu M. Inhibition of cancer cell proliferation by 5-fluoro-2’-deoxycytidine, a DNA methylation inhibitor, through activation of DNA damage response pathway. Springer Plus. 2012;1(1):65. doi:10.1186/ 2193-1801-1-65.