58
Views
13
CrossRef citations to date
0
Altmetric
ORIGINAL ARTICLECellular and Molecular Biology

Role of Histone Modifications and DNA Methylation in the Regulation of O6-Methylguanine-DNA Methyltransferase Gene Expression in Human Stomach Cancer Cells

, , &
Pages 331-339 | Published online: 22 Apr 2010

  • Pegg, A.E. Mammalian O6-alkylguanine-DNA alkyltransferase regulation and importance in response to alkylating carcinogenic and therapeutic agents. Cancer Res 1990, 50, 6119–6129.
  • Esteller, M.; Hamilton, S.R.; Burger, P.C.; Baylin, S.B.; Herman, J.G. Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res 1999, 59, 793–797.
  • Bugni, J.M.; Meira, L.B.; Samson, L.D. Alkylation-induced colon tumorigenesis in mice deficient in the Mgmt and Msh6 proteins. Oncogene 2009, 28(5), 734–741.
  • Oue, N.; Shigeishi, H.; Kuniyasu, H.; Yokozaki, H.; Kuraoka, K.; Ito, R.; Promoter hypermethylation of MGMT is associated with protein loss in gastric carcinoma. Int J Cancer 2001, 93, 805–809.
  • Baylin, S.B.; Herman, J.G. DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends Genet 2000, 16, 168–174.
  • Bae, S.I.; Lee, H.S.; Kim, S.H.; Kim, W.H. Inactivation of O6-methylguanine-DNA methyltransferase by promoter CpG island hypermethylation in gastric cancers. Br J Cancer 2002, 86, 1888–1892.
  • Iwakuma, T.; Sakumi, K.; Nakatsuru, Y.; Kawate, H.; Igarashi, H.; Shiraishi, A.T.; High incidence of nitrosamine-induced tumorigenesis in mice lacking DNA repair methyltransferase. Carcinogenesis 1997, 18, 1631–1635.
  • Lee, T.L.; Leung, W.K.; Chan, M.W.; Ng, E.K.; Tong, J.H.; Lo, K.W.; Detection of gene promoter hypermethylation in the tumor and serum of patients with gastric carcinoma. Clin Cancer Res 2002, 8, 1761–1766.
  • Fuks, F.; Hurd, P.J.; Deplus, R.; Kouzarides, T. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res 2003, 31(9), 2305–2312.
  • Fuks, F.; Hurd, P.J.; Wolf, D.; Nan, X.; Bird, A.P.; Kouzarides, T. The Methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem 2003, 278, 4035–4040.
  • Rice, J.C.; Briggs, S.D.; Ueberheide, B.; Barber, C.M.; Shabanowitz, J.; Hunt, D.F.; Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell 2003, 12, 1591–1598.
  • Peters, A.H.; Kubicek, S.; Mechtler, K.; O'Sullivan, R.J.; Derijck, A.A.; Perez-Burgos, L.; Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 2003, 12, 1577–1589.
  • Fuks, F. DNA methylation and histone modifications: teaming up to silence genes. Curr Opin Genet Dev 2005, 15, 490–495.
  • Santos-Rosa, H.; Schneider, R.; Bannister, A.J.; Sherriff, J.; Bernstein, B.E.; Emre, N.C.; Active genes are tri-methylated at K4 of histone H3. Nature 2002, 419, 407–411.
  • Fahrner, J.A.; Eguchi, S.; Herman, J.G.; Baylin SB. Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res 2002, 62, 7213–7218.
  • Nguyen, C.T.; Weisenberger, D.J.; Velicescu, M.; Gonzales, F.A.; Lin JCY, Liang, G.; Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-aza-2Pprime; -deoxycytidine. Cancer Res 2002, 62, 6456–6461.
  • Kondo, Y.; Shen, L.; Issa JP. Critical role of histone methylation in tumor suppressor gene silencing in colorectal cancer. Mol Cell Biol 2003, 23, 206–215.
  • Qian, X.; Li, J.; Ding, J.; Wang, Z.; Duan, L.; Hu, G. Glibenclamide exerts an antitumor activity through reactive oxygen species-c-jun NH2-terminal kinase pathway in human stomach cancer cell line MGC-803. Biochem Pharmacol 2008, 76(12), 1705–1715.
  • Zhang, W.; Tong, Q.; Li, S.; Wang, X.; Wang, Q. MG-132 inhibits telomerase activity, induces apoptosis and G(1) arrest associated with upregulated p27kip1 expression and downregulated survivin expression in gastric carcinoma cells. Cancer Invest 2008, 26(10), 1032–1036.
  • Xiao, Q.; Li, L.; Xie, Y.; Tan, N.; Wang, C.; Xu, J.; Transcription factor E2F-1 is upregulated in human gastric cancer tissues and its overexpression suppresses stomach tumor cell proliferation. Cell Oncol 2007, 29(4), 335–349.
  • Cameron, E.E.; Bachman, K.E.; Myohanen, S.; Herman, J.G.; Baylin, S.B. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 1999, 21, 103–107.
  • Herman, J.G.; Graff, J.R.; Myohanen, S.; Nelkin, B.D.; Baylin, S.B. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996, 93, 9821–9826.
  • Kuo, M.H.; Allis, C.D. In vivo cross-linking and immunoprecipitation for studying dynamic protein: DNA associations in a chromatin environment. Methods 1999, 19, 425–433.
  • Meng, C.F.; Zhu, X.J.; Peng, G.; Dai, D.Q. Re-expression of methylation-induced tumor suppressor gene silencing is associated with the state of histone modification in gastric cancer cell lines. World J Gastroenterol 2007, 13, 6166–6171.
  • Pogribny, I.P.; Ross, S.A.; Tryndyak, V.P.; Pogribna, M.; Poirier, L.A.; Karpinets, T.V. Histone H3 lysine 9 and H4 lysine 20 trimethylation and the expression of Suv4-20h2 and Suv-39h1 histone methyltransferases in hepatocarcinogenesis induced by methyl deficiency in rats. Carcinogenesis 2006, 27, 1180–1186.
  • Kim, J.S.; Shukl, S.D. Histone h3 modifications in rat hepatic stellate cells by ethanol. Alcohol & Alcoholism 2005, 40, 367–372.
  • Chen, T.; Li, E. Establishment and maintenance of DNA methylation patterns in mammals. Curr Top Microbiol Immunol 2006, 301, 179–201.
  • Wade, P.A. Methyl CpG binding proteins: coupling chromatin architecture to gene regulation. Oncogene 2001, 20, 3166–3173.
  • Smallwood, A.; Estève, P.O.; Pradhan, S.; Carey, M. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev 2007, 21(10), 1169–1178.
  • Costello, J.F.; Futscher, B.W.; Tano, K.; Graunke, D.M.; Pieper, R.O. Graded methylation in the promoter and in the body of the O6-methylguanine-DNA methyltransferase gene correlates with MGMT expression in human glioma cells. Cancer Res 1996, 56, 13916–13924.
  • Ji, W.; Yang, L.; Yu, L.; Yuan, J.; Hu, D.; Zhang, W.; Epigenetic silencing of O6-methylguanine DNA methyltransferase gene in NiS-transformed cells. Carcinogenesis 2008, 29(6), 1267–1275.
  • Watts, G.S.; Pieper, R.O.; Costello, J.F.; Peng, Y.M.; Dalton, W.S.; Futscher, B.W. Methylation of discrete regions of the O6-Methylguanine DNA methyltransferase (MGMT) CpG island is associated with heterochromatinization of the MGMT transcription start site and silencing of the gene. Mol Cell Biol 1997, 17, 5612–5619.
  • Fox, E.J.; Leahy, D.T.; Geraghty, R.; Mulcahy, H.E.; Fennelly, D.; Hyland, J.M. Mutually exclusive promoter hypermethylation patterns of hMLH1 and O6-methylguanine DNA methyltransferase in colorectal cancer. J Mol Diagn 2006, 8(1), 68–75.
  • Citron, M.; Decker, R.; Chen, S.; Schneider, S.; Graver, M.; Kleynerman, L.; O6-methylguanine-DNA methyltransferase in human normal and tumor tissue from brain, lung, and ovary. Cancer Res 1991, 51, 4131–4134.
  • Zaidi, N.H.; Liu, L.; Gerson, S.L. Quantitative immunohistochemical estimates of O6-alkylguanine-DNA alkyltransferase expression in normal and malignant human colon. Clin Cancer Res 1996, 2, 577–584.
  • Baumann, S.; Keller, G.; Pühringer, F.; Napieralski, R.; Feith, M.; Langer, R.; The prognostic impact of O6-Methylguanine-DNA Methyltransferase (MGMT) promotor hypermethylation in esophageal adenocarcinoma. Int J Cancer 2006, 119(2), 264–268.
  • Mattern, J.; Koomagi, R.; Volm, M. Smoking-related increase of O6-methylguanine-DNA methyltransferase expression in human lung carcinomas. Carcinogenesis (Lond.) 1998, 19, 1247–1250.
  • Zhang, Y.; Reinberg, D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 2001, 15, 2343–2360.
  • Lachner, M.; Jenuwein, T. The many faces of histone lysine methylation. Curr Opin Cell Biol 2002, 14, 286–298.
  • Kouzarides, T. Histone methylation in transcriptional control. Curr Opin Genet Dev 2002, 12, 198–209.
  • Tsukada, Y.; Fang, J.; Erdjument-Bromage, H.; Warren, M.E.; Borchers, C.H.; Tempst, P.; Histone demethylation by a family of JmjC domain-containing proteins. Nature 2006, 439, 811–816.
  • Guo, H.B.; Guo, H. Mechanism of histone methylation catalyzed by protein lysine methyltransferase SET7/9 and origin of product specificity. Proc Natl Acad Sci USA 2007, 104(21), 8797–8802.
  • Maison, C.; Bailly, D.; Peters, A.H.; Quivy, J.P.; Roche, D.; Taddei, A.; Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet 2002, 30, 329–334.
  • Musri, M.M.; Corominola, H.; Casamitjana, R.; Gomis, R.; P´rrizas, M. Histone H3 lysine 4 dimethylation signals the transcriptional competence of the adiponectin promoter in preadipocytes. J Biol Chem 2006, 281(25), 17180–17188.
  • Zegerman, P.; Canas, B.; Pappin, D.; Kouzarides, T. Histone H3 lysine 4 methylation disrupts binding of nucleosome remodeling and deacetylase (NuRD) repressor complex. J Biol Chem 2002, 277, 11621–11624.
  • Nguyen, C.; Liang, G.; Nguyen, T.T.; Tsao-Wei, D.; Groshen, S.; Lubbert, M.; Susceptibility of nonpromoter CpG islands to de novo methylation in normal and neoplastic cells. J Natl Cancer Inst (Bethesda) 2001, 93, 1465–1472.
  • Jones, P.A. The DNA methylation paradox. Trends Genet 1999, 15, 34–37.
  • Palii, S.S.; Van Emburgh, B.O.; Sankpal, U.T.; Brown, K.D.; Robertson, K.D. DNA methylation inhibitor 5-Aza-2Pprime; -deoxycytidine induces reversible genome-wide DNA damage that is distinctly influenced by DNA methyltransferases 1 and 3B. Mol Cell Biol 2008, 28(2), 752–771.
  • Creusot, F.; Acs, G.; Christman, J.K. Inhibition of DNA methyltransferase and induction of Friend erythroleukemia cell differentiation by 5-azacytidine and 5-aza-2Pprime;-deoxycytidine. J Biol Chem 1982, 257, 2041–2048.
  • Herman, J.G.; Umar, A.; Polyak, K.; Graff, J.R.; Ahuja, N.; Issa, J.P.; Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci USA 1998, 95, 6870–6875.
  • Bovenzi, V.; Momparler, R.L. Antineoplastic action of 5-aza-2Pprime; -deoxycytidine and histone deacetylase inhibitor and their effect on the expression of retinoic acid receptor beta and estrogen receptor alpha genes in breast carcinoma cells. Cancer Chemother Pharmacol 2001, 8(1), 71–76.
  • Bachman, K.E.; Rountree, M.R.; Baylin, S.B. Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J Biol Chem 2001, 276, 32282–32287.
  • Rountree, M.R.; Bachman, K.E.; Baylin, S.B. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 2000, 25, 269–277.
  • Yang, X.; Phillips, D.L.; Ferguson, A.T.; Nelson, W.G.; Herman, J.G.; Davidson N.E. Synergistic activation of functional estrogen receptor (ER)- by DNA methyltransferase and histone deacetylase inhibition in human ER- -negative breast cancer cells. Cancer Res 2001, 61, 7025–7029.
  • Suzuki, H.; Gabrielson, E.; Chen, W.; Anbazhagan, R.; van Engeland, M.; Weijenberg, M.P.; A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat Genet 2002, 31, 141–149.
  • Chiurazzi, P.; Pomponi, M.G.; Pietrobono, R.; Bakker, C.E.; Neri, G.; Oostra, B.A. Synergistic effect of histone hyperacetylation and DNA demethylation in the reactivation of the FMR1 gene. Hum Mol Genet 1999, 8, 2317–2323.
  • Chiurazzi, P.; Pomponi M.G., Willemsen, R.; Oostra, B.A.; Neri, G. In vitro reactivation of the FMR1 gene involved in fragile × syndrome. Hum Mol Genet 1998, 7, 109–113.
  • Grunstein, M. Histone acetylation in chromatin structure and transcription. Nature 1997, 389, 349–352.
  • Marks, P.A.; Rifkind, R.A.; Richon, V.M.; Breslow, R.; Miller, T.; Kelly, W.K. Histone deacetylases and cancer: causes and therapies. Nat Rev Cancer 2001, 1, 194–202.
  • Roth, S.Y.; Denu, J.M.; Allis, C.D. Histone acetyltransferases. Annu Rev Biochem 2001, 70, 81–120.
  • Budillon, A.; Di Gennaro, E.; Bruzzese, F.; Rocco, M.; Manzo, G.; Caraglia, M. Histone deacetylase inhibitors: a new wave of molecular targeted anticancer agents. Recent Patents Anticancer Drug Discov 2007, 2(2), 119–134.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.