The essential role of histone H3 Lys9 di-methylation and MeCP2 binding in MGMT silencing with poor DNA methylation of the promoter CpG island

Journal of Biochemistry

Volumn 137, Issue 3, 2005, Pages 431-440

  Zhao, Wei ^a   Soejima, Hidenobu ^a   Higashimoto, Ken ^a   Nakagawachi, Tetsuji ^a   Urano, Takeshi ^b   Kudo, Shinichi ^c   Matsukura, Shiroh ^a   Matsuo, Shuzo ^d   Joh, Keiichiro ^a   Mukai, Tsunehiro ^a  

^a SAGA UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c HOKKAIDO INSTITUTE OF PUBLIC HEALTH   (Japan)

^d Tanaka Hospital   (Japan)

Author keywords

DNA methylation; Gene silencing; Histone H3K9 di methylation; MeCP2; MGMT

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; HISTONE H3; METHYL CPG BINDING PROTEIN 2; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; TRICHOSTATIN A;

ACETYLATION; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; CPG ISLAND; DEACETYLATION; DNA METHYLATION; DRUG EFFECT; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; HETEROCHROMATIN; HUMAN; HUMAN CELL; METHYLATION; PROMOTER REGION; PROTEIN DNA BINDING;

AZACITIDINE; CELL LINE, TUMOR; CHROMOSOMAL PROTEINS, NON-HISTONE; CPG ISLANDS; DNA METHYLATION; DNA-BINDING PROTEINS; GENE EXPRESSION; GENE SILENCING; HISTONES; HUMANS; HYDROXAMIC ACIDS; LYSINE; METHYL-CPG-BINDING PROTEIN 2; O(6)-METHYLGUANINE-DNA METHYLTRANSFERASE; POLYMERASE CHAIN REACTION; PROMOTER REGIONS (GENETICS); REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

EID: 20944438418     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/jb/mvi048     Document Type: Article

References (32)

1. Jones, P.A. and Laird, P.W. (1999) Cancer epigenetics comes of age. Nat. Genet. 21, 163-167
2. Jones, P.A. and Baylin, S.B. (2002) The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 3, 415-428
3. Herman, J.G. and Baylin, S.B. (2003) Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med. 349, 2042-2054
4. 6-methylguanine DNA methyltransferase in human cancer. Oncogene 23, 1-8
5. Zhu, W.G., Dai, Z., Ding, H., Srinivasan, K., Hall, J., Duan, W., Villalona-Calero, M.A., Plass, C., and Otterson, G.A. (2001) Increased expression of unmethylated CDKN2D by 5Aza-CdR-2′-deoxycytidine in human lung cancer cells. Oncogene 20, 7787-7796
6. Evron, E., Umbricht, C.B., Korz, D., Raman, V., Loeb, D.M., Niranjan, B., Buluwela, L., Weitzman, S.A., Marks, J., and Sukumar, S. (2001) Loss of cyclin d2 expression in the majority of breast cancers is associated with promoter hypermethylation. Cancer Res. 61, 2782-2787
7. Loeb, D.M., Evron, E., Patel, C.B., Sharma, P.M., Niranjan, B., Buluwela, L., Weitzman, S.A., Korz, D., and Sukumar, S. (2001) Wilms' tumor suppressor gene (WT1) is expressed in primary breast tumors despite tumor-specific promoter methylation. Cancer Res. 61, 921-925
8. Satoh, Y., Nakagawachi, T., Nakadate, H., Kaneko, Y., Masaki, Z., Mukai, T., and Soejima, H. (2003) Significant reduction of WT1 gene expression possibly due to epigenetic alteration in Wilms' tumor. J. Biochem. 133, 303-308
9. Nakagawachi, T., Soejima, H., Urano, T., Zhao, W., Higashimoto, K, Satoh, Y., Matsukura, S., Kudo, S., Kitajima, Y., Harada, H., Furukawa, K., Matsuzaki, H., Emi, M., Nakabeppu, Y., Miyazaki, K., Sekiguchi, M., and Mukai, T. (2003) Silencing effect of CpG island hypermethylation and histone modifications on O6-methylguanine-DNA methyltransferase (MGMT) gene expression in human cancer. Oncogene 22, 8835-8844
10. Wolffe, A.P. and Matzke, M.A. (1999) Epigenetics: regultion through repression. Science 286, 481-486
11. Litt, M.D., Simpson, M., Gaszner, M., Allis, C.D., and Felsenfeld, G. (2001) Correlation between histone lysine methylation and developmental changes at the chicken-globin locus. Science 293, 2453-2455
12. Noma, K., Allis, C.D., and Grewal, S.I. (2001) Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293, 1150-1155
13. Peters, A.H., O'Carroll, D., Scherthan, H., Mechtler, K., Sauer, S., Schofer, C., Weipoltshammer, K., Pagani, M., Lachner, M., Kohlmaier, A., Opravil, S., Doyle, M., Sibilia, M., and Jenuwein, T. (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-337
14. Kondo, Y., Shen, L., and Issa, J.P. (2003) Critical role of histone methylation in tumor suppressor gene silencing in colorectal cancer. Mol. Cell. Biol. 23, 206-215
15. Wade, P.A. (2001) Methyl CpG-binding proteins and transcriptional repression. Bioessays 23, 1131-1137
16. Fuks, F., Hurd, P.J., Wolf, D., Nan, X., Bird, A.P., and Kouzarides, T. (2003) The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 278, 4035-4040
17. Fujita, N., Watanabe, S., Ichimura, T. Tsuruzoe, S., Shinkai, Y., Tachibana, M., Chiba, T., and Nakao, M. (2003) Methyl-CpG binding domain 1 (MBD1) interacts with the Suv39h1-HP1 heterochromatic complex for DNA methylation-based transcriptional repression. J. Biol. Chem. 278, 24132-24138
18. Ballestar, E., Paz, M.F., Valle, L., Wei, S., Fraga, M.F., Espada, J., Cigudosa, J.C., Huang, T.H., and Esteller, M. (2003) Methyl-CpG binding proteins identify novel sites of epigenetic inactivation in human cancer. EMBO J. 22, 6335-6345
19. Matsukura, S., Soejima, H., Nakagawachi, T., Yakushiji, H., Ogawa, A., Fukuhara, M., Miyazaki, K., Nakabeppu, Y., Sekiguchi, M., and Mukai T. (2003) CpG methylation of MGMT and hMLH1 promoter in hepatocellular carcinoma associated with hepatitis viral infection. Brit. J. Cancer 88, 521-529
20. Higashimoto, K., Urano, T., Sugiura, K., Yatsuki, H., Joh, K., Zhao, W., Iwakawa, M., Ohashi, H., Oshimura, M., Niikawa, N., Mukai, T., and Soejima, H. (2003) Loss of CpG methylation is strongly correlated with loss of histone H3 lysine 9 methylation at DMR-LIT1 in patients with Beckwith-Wiedemann syndrome. Amer. J. Hum. Genet. 73, 948-956
21. Soejima, H., Nakagawachi, T., Zhao, W., Higashimoto, K., Urano, T., Matsukura, S., Kitajima, Y., Takeuchi, M., Nakayama, M., Oshimura, M., Miyazaki, K., Joh, K., and Mukai, T. (2004) Silencing of imprinted CDKN1C gene expression is associated with loss of CpG and histone H3 lysine 9 methylation at DMR-LIT1 in esophageal cancer. Oncogene 23, 4380-4388
22. Kudo, S. (1998) Methyl-CpG-binding protein MeCP2 represses Sp1-activated transcription of the human leukosialin gene when the promoter is methylated. Mol. Cell. Biol. 18, 5492-5499
23. Koizume, S., Tachibana, K., Sekiya, T., Hirohashi, S., and Shiraishi, M. (2002) Heterogeneity in the modification and involvement of chromatin components of the CpG island of the silenced human CDH1 gene in cancer cells. Nucleic Acids Res. 30, 4770-4780
24. Pieper, R.O., Patel, S., Ting, S.A., Futscher, B.W., and Costello, J.F. (1996) Methylation of CpG island transcription factor binding sites is unnecessary for aberrant silencing of the human MGMT gene. J. Biol. Chem. 271, 13916-13924
25. 6-methylguanine DNA methyltransferase gene is associated with the loss of nucleosome-like positioning. Mol. Cell. Biol. 17, 5813-5822
26. Soejima, H., Joh, K., and Mukai, T: (2004) Gene silencing in DNA damage repair. Cell. Mol. Life Sci. 61, 2168-2172
27. Georgel, P.T., Horowitz-Scherer, R.A., Adkins, N., Woodcock, C.L., Wade, P.A., and Hansen, J.C. (2003) Chromatin compaction by human MeCP2: Assembly of novel secondary chromatin structures in the absence of DNA methylation. J. Biol. Chem. 278, 32181-32188
28. Yu, F., Thiesen, J., and Stratling, W.H. (2000) Histone deacetylase-independent transcriptional repression by methyl-CpG-binding protein 2. Nucleic Acids Res. 28, 2201-2206
29. Bachman, K.E., Park, B.H., Rhee, I., Rajagopalan, H., Herman, J.G., Baylin, S.B., Kinzler, K.W., and Vogelstein, B. (2003). Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. Cancer Cell 3, 89-95
30. Nguyen, C.T., Weisenberger, D.J., Velicescu, M., Gonzales, F.A., Lin, J.C., Liang, G., and Jones, P.A. (2002) Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5aza-CdR-2′-deoxycytidine. Cancer Res. 62, 6456-6461
31. El-Osta, A., Kantharidis, P., Zalcberg, J.R., and Wolffe, A.P. (2002). Precipitous release of methyl-CpG binding protein 2 and histone deacetylase 1 from the methylated human multidrug resistance gene (MDR1) on activation. Mol. Cell. Biol. 22, 1844-1857
32. Takebayashi, S., Nakao, M., Fujita, N., Sado, T., Tanaka, M., Taguchi, H., and Okumura, K. (2001) 5Aza-CdR-2′-deoxycytidine induces histone hyperacetylation of mouse centromeric heterochromatin by a mechanism independent of DNA demethylation. Biochem. Biophys. Res. Commun. 288, 921-926