DNA methylation directly silences genes with non-CpG island promoters and establishes a nucleosome occupied promoter

Human Molecular Genetics

Volumn 20, Issue 22, 2011, Pages 4299-4310

  Han, Han ^a,b   Cortez, Connie C ^b   Yang, Xiaojing ^b   Nichols, Peter W ^b   Jones, Peter A ^b   Liang, Gangning ^b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DNA; HISTONE H3; LAMININ; LAMININ BETA 3; TRANSCRIPTION FACTOR RUNX3; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; BLADDER TUMOR; CHROMATIN; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; GENE ACTIVATION; GENE EXPRESSION; GENE SILENCING; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MELANOMA CELL; NUCLEOSOME; NUCLEOSOME OCCUPANCY METHYLOME SEQUENCING; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; SEQUENCE ANALYSIS; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION TERMINATION;

CELL ADHESION MOLECULES; CELL LINE, TUMOR; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; CORE BINDING FACTOR ALPHA 3 SUBUNIT; CPG ISLANDS; DEOXYCYTIDINE; DNA METHYLATION; GENE SILENCING; HUMANS; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 80054880084     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr356     Document Type: Article

References (52)

1. Jones, P.A. and Baylin, S.B. (2002) The fundamental role of epigenetic events in cancer. Nat. Rev. Genet, 3, 415-428.
2. Jones, P.A. and Baylin, S.B. (2007) The epigenomics of cancer. Cell, 128, 683-692.
3. Kouzarides, T. (2007) Chromatin modifications and their function. Cell, 128, 693-705.
4. Suzuki, M.M. and Bird, A. (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet., 9, 465-476.
5. Jones, P.A. and Liang, G. (2009) Rethinking how DNA methylation patterns are maintained. Nat. Rev. Genet., 10, 805-811.
6. Jenuwein, T. and Allis, C.D. (2001) Translating the histone code. Science, 293, 1074-1080.
7. Lin, J.C., Jeong, S., Liang, G., Takai, D., Fatemi, M., Tsai, Y.C., Egger, G., Gal-Yam, E.N. and Jones, P.A. (2007) Role of nucleosomal occupancy in the epigenetic silencing of the MLH1 CpG island. Cancer Cell, 12, 432-444.
8. Hebbes, T.R., Thorne, A.W. and Crane-Robinson, C. (1988) A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J., 7, 1395-1402.
9. Liang, G., Lin, J.C., Wei, V., Yoo, C., Cheng, J.C., Nguyen, C.T., Weisenberger, D.J., Egger, G., Takai, D., Gonzales, F.A. et al. (2004) Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. Proc. Natl Acad. Sci. USA, 101, 7357-7362.
10. Mikkelsen, T.S., Ku, M., Jaffe, D.B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T.K., Koche, R.P. et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature, 448, 553-560.
11. Cedar, H. and Bergman, Y. (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet., 10, 295-304.
12. Yuan, G.C., Liu, Y.J., Dion, M.F., Slack, M.D., Wu, L.F., Altschuler, S.J. and Rando, O.J. (2005) Genome-scale identification of nucleosome positions in S. cerevisiae. Science, 309, 626-630.
13. Mellor, J. (2005) The dynamics of chromatin remodeling at promoters. Mol. Cell, 19, 147-157.
14. Li, B., Carey, M. and Workman, J.L. (2007) The role of chromatin during transcription. Cell, 128, 707-719.
15. Jiang, C. and Pugh, B.F. (2009) Nucleosome positioning and gene regulation: advances through genomics. Nat. Rev. Genet., 10, 161-172.
16. Jones, P.A. (1999) The DNA methylation paradox. Trends Genet., 15, 34-37.
17. Takai, D. and Jones, P.A. (2002) Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc. Natl Acad. Sci. USA, 99, 3740-3745.
18. Eckhardt, F., Lewin, J., Cortese, R., Rakyan, V.K., Attwood, J., Burger, M., Burton, J., Cox, T.V., Davies, R., Down, T.A. et al. (2006) DNA methylation profiling of human chromosomes 6, 20 and 22. Nat. Genet., 38, 1378-1385.
19. Gal-Yam, E.N., Egger, G., Iniguez, L., Holster, H., Einarsson, S., Zhang, X., Lin, J.C., Liang, G., Jones, P.A. and Tanay, A. (2008) Frequent switching of Polycomb repressive marks and DNA hypermethylation in the PC3 prostate cancer cell line. Proc. Natl Acad. Sci. USA, 105, 12979-12984.
20. Weber, M., Hellmann, I., Stadler, M.B., Ramos, L., Paabo, S., Rebhan, M. and Schubeler, D. (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet., 39, 457-466.
21. Aumailley, M. and Rousselle, P. (1999) Laminins of the dermo-epidermal junction. Matrix Biol., 18, 19-28.
22. Bangsow, C., Rubins, N., Glusman, G., Bernstein, Y., Negreanu, V., Goldenberg, D., Lotem, J., Ben-Asher, E., Lancet, D., Levanon, D. et al. (2001) The RUNX3 gene-sequence, structure and regulated expression. Gene, 279, 221-232.
23. Bae, S.C. and Choi, J.K. (2004) Tumor suppressor activity of RUNX3. Oncogene, 23, 4336-4340.
24. Kang, G.H., Lee, S., Lee, H.J. and Hwang, K.S. (2004) Aberrant CpG island hypermethylation of multiple genes in prostate cancer and prostatic intraepithelial neoplasia. J. Pathol., 202, 233-240.
25. Kim, T.Y., Lee, H.J., Hwang, K.S., Lee, M., Kim, J.W., Bang, Y.J. and Kang, G.H. (2004) Methylation of RUNX3 in various types of human cancers and premalignant stages of gastric carcinoma. Lab. Invest., 84, 479-484.
26. Jiang, Y., Tong, D., Lou, G., Zhang, Y. and Geng, J. (2008) Expression of RUNX3 gene, methylation status and clinicopathological significance in breast cancer and breast cancer cell lines. Pathobiology, 75, 244-251.
27. Wolff, E.M., Liang, G., Cortez, C.C., Tsai, Y.C., Castelao, J.E., Cortessis, V.K., Tsao-Wei, D.D., Groshen, S. and Jones, P.A. (2008) RUNX3 methylation reveals that bladder tumors are older in patients with a history of smoking. Cancer Res., 68, 6208-6214.
28. Takai, D. and Jones, P.A. (2003) The CpG island searcher: a new WWW resource. In Silico Biol., 3, 235-240.
29. Chung, D.D., Honda, K., Cafuir, L., McDuffie, M. and Wotton, D. (2007) The Runx3 distal transcript encodes an additional transcriptional activation domain. FEBS J., 274, 3429-3439.
30. Egawa, T., Tillman, R.E., Naoe, Y., Taniuchi, I. and Littman, D.R. (2007) The role of the Runx transcription factors in thymocyte differentiation and in homeostasis of naive T cells. J. Exp. Med., 204, 1945-1957.
31. Sharma, S., Kelly, T.K. and Jones, P.A. (2009) Epigenetics in cancer. Carcinogenesis, 31, 27-36.
32. Rhodes, D.R., Yu, J., Shanker, K., Deshpande, N., Varambally, R., Ghosh, D., Barrette, T., Pandey, A. and Chinnaiyan, A.M. (2004) ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia, 6, 1-6.
33. Klug, M. and Rehli, M. (2006) Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics, 1, 127-130.
34. Barski, A., Cuddapah, S., Cui, K., Roh, T.Y., Schones, D.E., Wang, Z., Wei, G., Chepelev, I. and Zhao, K. (2007) High-resolution profiling of histone methylations in the human genome. Cell, 129, 823-837.
35. Rakyan, V.K., Down, T.A., Thorne, N.P., Flicek, P., Kulesha, E., Graf, S., Tomazou, E.M., Backdahl, L., Johnson, N., Herberth, M. et al. (2008) An integrated resource for genome-wide identification and analysis of human tissue-specific differentially methylated regions (tDMRs). Genome Res., 18, 1518-1529.
36. Zhang, Z. and Pugh, B.F. (2011) High-resolution genome-wide mapping of the primary structure of chromatin. Cell, 144, 175-186.
37. Kelly, T.K., Miranda, T.B., Liang, G., Berman, B.P., Lin, J.C., Tanay, A. and Jones, P.A. (2010) H2A.Z maintenance during mitosis reveals nucleosome shifting on mitotically silenced genes. Mol. Cell, 39, 901-911.
38. Wolff, E.M., Byun, H.M., Han, H.F., Sharma, S., Nichols, P.W., Siegmund, K.D., Yang, A.S., Jones, P.A. and Liang, G. (2010) Hypomethylation of a LINE-1 promoter activates an alternate transcript of the MET oncogene in bladders with cancer. PLoS Genet., 6, e1000917.
39. Xu, M., Kladde, M.P., Van Etten, J.L. and Simpson, R.T. (1998) Cloning, characterization and expression of the gene coding for a cytosine-5-DNA methyltransferase recognizing GpC. Nucleic Acids Res., 26, 3961-3966.
40. Tycko, B. (2010) Allele-specific DNA methylation: beyond imprinting. Hum. Mol. Genet., 19, R210-R220.
41. Wang, J., Valo, Z., Bowers, C.W., Smith, D.D., Liu, Z. and Singer-Sam, J. (2010) Dual DNA methylation patterns in the CNS reveal developmentally poised chromatin and monoallelic expression of critical genes. PLoS ONE, 5, e13843.
42. Calaluce, R., Bearss, D.J., Barrera, J., Zhao, Y., Han, H., Beck, S.K., McDaniel, K. and Nagle, R.B. (2004) Laminin-5 beta3A expression in LNCaP human prostate carcinoma cells increases cell migration and tumorigenicity. Neoplasia, 6, 468-479.
43. Sathyanarayana, U.G., Maruyama, R., Padar, A., Suzuki, M., Bondaruk, J., Sagalowsky, A., Minna, J.D., Frenkel, E.P., Grossman, H.B., Czerniak, B. et al. (2004) Molecular detection of noninvasive and invasive bladder tumor tissues and exfoliated cells by aberrant promoter methylation of laminin-5 encoding genes. Cancer Res., 64, 1425-1430.
44. Sathyanarayana, U.G., Padar, A., Huang, C.X., Suzuki, M., Shigematsu, H., Bekele, B.N. and Gazdar, A.F. (2003) Aberrant promoter methylation and silencing of laminin-5-encoding genes in breast carcinoma. Clin. Cancer Res., 9, 6389-6394.
45. Sathyanarayana, U.G., Padar, A., Suzuki, M., Maruyama, R., Shigematsu, H., Hsieh, J.T., Frenkel, E.P. and Gazdar, A.F. (2003) Aberrant promoter methylation of laminin-5-encoding genes in prostate cancers and its relationship to clinicopathological features. Clin. Cancer Res., 9, 6395-6400.
46. Aumailley, M., El Khal, A., Knoss, N. and Tunggal, L. (2003) Laminin 5 processing and its integration into the ECM. Matrix Biol., 22, 49-54.
47. Wolff, E.M., Chihara, Y., Pan, F., Weisenberger, D.J., Siegmund, K.D., Sugano, K., Kawashima, K., Laird, P.W., Jones, P.A. and Liang, G. (2010) Unique DNA methylation patterns distinguish noninvasive and invasive urothelial cancers and establish an epigenetic field defect in premalignant tissue. Cancer Res., 70, 8169-8178.
48. Walsh, C.P. and Bestor, T.H. (1999) Cytosine methylation and mammalian development. Genes Dev., 13, 26-34.
49. Zhou, V.W., Goren, A. and Bernstein, B.E. (2010) Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet., 12, 7-18.
50. Frommer, M., McDonald, L.E., Millar, D.S., Collis, C.M., Watt, F., Grigg, G.W., Molloy, P.L. and Paul, C.L. (1992) A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc. Natl Acad. Sci. USA, 89, 1827-1831.
51. Gonzalgo, M.L. and Liang, G. (2007) Methylation-sensitive single-nucleotide primer extension (Ms-SNuPE) for quantitative measurement of DNA methylation. Nat. Protoc., 2, 1931-1936.
52. Gal-Yam, E.N., Jeong, S., Tanay, A., Egger, G., Lee, A.S. and Jones, P.A. (2006) Constitutive nucleosome depletion and ordered factor assembly at the GRP78 promoter revealed by single molecule footprinting. PLoS Genet, 2, e160.