Methyl-CpG binding proteins identify novel sites of epigenetic inactivation in human cancer

EMBO Journal

Volumn 22, Issue 23, 2003, Pages 6335-6345

  Ballestar, Esteban ^a   Paz, Maria F ^a   Valle, Laura ^a   Wei, Susan ^b   Fraga, Mario F ^a   Espada, Jesus ^a   Cigudosa, Juan Cruz ^a   Huang, Tim Hui Ming ^b   Esteller, Manel ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b University of Missouri   (United States)

Author keywords

ChIP on chip; DNA methylation; Epigenetic inactivation; MBD; MeCP2

Indexed keywords

DIPEPTIDYL PEPTIDASE IV; HISTONE DEACETYLASE; METHYL CPG BINDING PROTEIN; PROLACTIN RECEPTOR;

ARTICLE; BREAST CANCER; CANCER CELL; CHROMATIN; CONTROLLED STUDY; CPG ISLAND; DNA HYBRIDIZATION; DNA METHYLATION; DNA MICROARRAY; GENE; GENE INACTIVATION; GENE SILENCING; GENE TARGETING; GENETIC REGULATION; GENETIC TRANSCRIPTION; GENOME; HOMEOBOX; HUMAN; HUMAN CELL; IMMUNOLOCALIZATION; IMMUNOPRECIPITATION; NUCLEOTIDE BINDING SITE; NUCLEOTIDE SEQUENCE; PAX6 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN FUNCTION;

5-METHYLCYTOSINE; AMINO ACID SEQUENCE; BREAST NEOPLASMS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME MAPPING; CPG ISLANDS; DNA METHYLATION; DNA-BINDING PROTEINS; FEMALE; HUMANS; METHYL-CPG-BINDING PROTEIN 2; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; NEOPLASMS; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEPTIDE FRAGMENTS; POLYMERASE CHAIN REACTION; PROMOTER REGIONS (GENETICS); REPRESSOR PROTEINS; TUMOR CELLS, CULTURED;

EID: 0348134871     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg604     Document Type: Article

References (44)

1. Bakker, J., Lin, X. and Nelson, W.G. (2002) Methyl-CpG binding domain protein 2 represses transcription from hypermethylated pi-class glutathione S-transferase gene promoters in hepatocellular carcinoma cells. J. Biol. Chem., 277, 22573-22580.
2. Ballestar, E. and Wolffe, A.P. (2001) Methyl-CpG-binding proteins. Targeting specific gene repression. Eur. J. Biochem. 2681-6.
3. Bird, A.P. and Wolffe, A.P. (1999) Methylation-induced repression: belts, braces and chromatin. Cell, 99, 451-454.
4. Cedar, H. (1988) DNA methylation and gene activity. Cell, 53, 3-4.
5. Chatah, N.E. and Abrams, C.S. (2001) G-protein-coupled receptor activation induces the membrane translocation and activation of phosphatidylinositol-4-phosphate 5-kinase I α by a Rac- and Rho-dependent pathway. J. Biol. Chem., 276, 34059-34065.
6. Chen, W.Y., Zeng, X., Carter, M.G., Morrell, C.N., Chiu Yen, R.W., Esteller, M., Watkins, D.N., Herman, J.G., Mankowski, J.L. and Baylin, S.B. (2003) Heterozygous disruption of Hic1 predisposes mice to a gender-dependent spectrum of malignant tumors. Nat. Genet., 33, 197-202.
7. Cigudosa, J.C., Rao, P.H., Calasanz, M.J., Odero, M.D. Michaeli, J., Jhanwar, S.C. and Chaganti, R.S. (1998) Characterization of nonrandom chromosomal gains and losses in multiple myeloma by comparative genomic hybridization. Blood, 91, 3007-3010.
8. Clark, S.J. and Warnecke, P.M. (2002) DNA methylation analysis in mammalian cells. Methods, 27, 99-100.
9. 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.
10. Esteller, M. (2002) CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future. Oncogene, 21, 5427-5440.
11. Esteller, M., Corn, P.G., Baylin, S.B. and Herman, J.G. (2001) A gene hypermethylation profile of human cancer. Cancer Res., 61, 3225-3229.
12. Feng, Q. and Zhang, Y. (2001) The MeCP1 complex represses transcription through preferential binding, remodeling and deacetylating methylated nucleosomes. Genes Dev., 15, 827-832.
13. Fournier, C., Goto, Y., Ballestar, E., Delaval, K., Hever, A., Esteller, M. and Feil, R. (2002) Allele-specific histone lysine methylation marks regulatory regions at imprinted mouse genes. EMBO J., 21, 6560-6570.
14. Fraga, M.F. and Esteller, M. (2002) DNA methylation: a profile of methods and applications. Biotechniques, 33, 632-649.
15. Fraga, M.F., Ballestar, E., Montoya, G., Taysavang, P., Wade, P.A. and Esteller, M. (2003) The affinity of different MBD proteins for a specific methylated locus depends on their intrinsic binding properties. Nucleic Acids Res., 31, 1765-1774.
16. Fujita, N., Shimotake, N., Ohki, I., Chiba, T., Saya, H., Shirakawa, M. and Nakao, M. (2000) Mechanism of transcriptional regulation by methyl-CpG binding protein MBD1. Mol. Cell. Biol., 20, 5107-5118.
17. Fujita, N., Watanabe, S., Ichimura, T., Ohkuma, Y., Chiba, T., Saya, H. and Nakao, M. (2003) MCAF mediates MBD1-dependent transcriptional repression. Mol. Cell. Biol., 23, 2834-2843.
18. Hendrich, B., and Bird, A. (1998) Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell. Biol., 18, 6538-6547.
19. Hendrich, B., Guy, J., Ramsahoye, B., Wilson, V.A. and Bird, A. (2001) Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development. Genes Dev., 15, 710-723.
20. Herman, J.G., Graff, J.R., Myohanen, S., Nelkin, B.D. and Baylin, S.B. (1996) Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl Acad. Sci. USA, 93, 9821-9826.
21. Jonathan, N., Liby, K., McFarland, M. and Zinger, M. (2002) Prolactin as an autocrine/paracrine growth factor in human cancer. Trends Endocrinol. Metab., 13, 245-250.
22. Jones, P.A. and Baylin, S.B. (2002) The fundamental role of epigenetic events in cancer. Nat. Rev. Genet., 3, 415-428.
23. Kelly, P.A., Bachelot, A., Kedzia, C., Hennighausen, L., Ormandy, C.J., Kopchick, J.J. and Binart, N. (2002) The role of prolactin and growth hormone in mammary gland development. Mol. Cell. Endocrinol., 197, 127-131.
24. 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.
25. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K. and Jenuwein, T. (2001) Methylation of histone H3 lysine-9 creates a binding site for Hp1 protein. Nature, 410, 116-120.
26. Lefkovits, I. and Kohler, G. (1997) Immunology Methods Manual: The Comprehensive Sourcebook of Techniques. Academic Press, Orlando, FL, USA.
27. Magdinier, F. and Wolffe, A.P. (2001) Selective association of the methyl-CpG binding protein MBD2 with the silent p14/p16 locus in human neoplasia. Proc. Natl Acad. Sci. USA, 98, 4990-4995.
28. Ng, H.H., Jeppesen, P. and Bird, A. (2000) Active repression of methylated genes by the chromosomal protein MBD1. Mol. Cell. Biol., 20, 1394-1406.
29. Nguyen, C.T., Gonzales, F.A. and Jones, P.A. (2001) Altered chromatin structure associated with methylation-induced gene silencing in cancer cells: correlation of accessibility, methylation, MeCP2 binding and acetylation. Nucleic Acids Res., 29, 4598-4606.
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 5-aza-2′-deoxycytidine. Cancer Res., 62, 6456-6461.
31. Ogata, M., Takada, T., Mori, Y., Oh-hora, M., Uchida, Y., Kosugi, A., Miyake, K. and Hamaoka, T. (1999) Effects of overexpression of PTP36, a putative protein tyrosine phosphatase, on cell adhesion, cell growth and cytoskeletons in HeLa cells. J. Biol. Chem., 274, 12905-12909.
32. Paz, M.F., Fraga, M.F., Avila, S., Mingzhou, G., Herman, J.G. and Esteller, M. (2003a) A systematic profile of DNA methylation in human cancer cell lines. Cancer Res., 63, 1114-1121.
33. Paz, M.F., Wei, S., Cigudosa, J.C., Rodriguez-Perales, S., Peinado, M.A., Huang, T.H. and Esteller, M. (2003b) Genetic unmasking of epigenetically silenced tumor suppressor genes in colon cancer cells deficient in DNA methyltransferases. Hum. Mol. Genet., 12, 2209-2219.
34. Perk, J., Makedonski, K., Lande, L., Cedar, H., Razin, A. and Shemer, R. (2002) The imprinting mechanism of the Prader-Willi/Angelman regional control center. EMBO J. 12, 15807-5814.
35. Pethiyagoda, C.L., Welch, D.R. and Fleming, T.P. (2000) Dipeptidyl peptidase IV (DPPIV) inhibits cellular invasion of melanoma cells. Clin. Exp. Metastasis, 18391-400.
36. Prokhortchouk, E. and Hendrich, B. (2002) Methyl-CpG binding proteins and cancer: are MeCpGs more important than MBDs? Oncogene, 21, 5394-5349.
37. Tomizawa, Y. et al. (2001) Inhibition of lung cancer cell growth and induction of apoptosis after reexpression of 3p21.3 candidate tumor suppressor gene SEMA3B. Proc. Natl Acad. Sci. USA, 98, 13954-13959.
38. Wade, P.A. (2001) Methyl CpG binding proteins and transcriptional repression. BioEssays, 23, 1131-1137.
39. Wade, P.A., Gegonne, A., Jones, P.L., Ballestar, E., Aubry, F. and Wolffe, A.P. (1999) Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat. Genet., 23, 62-66.
40. Weinmann, A.S., Yan, P.S., Oberley, M.J., Huang, T.H. and Farnham, P.J. (2002) Isolating human transcription factor targets by coupling chromatin immunoprecipitation and CpG island microarray analysis. Genes Dev., 16, 235-244.
41. Xie, D., Jauch, A., Miller, C.W., Bartram, C.R. and Koeffler, H.P. (2002) Discovery of over-expressed genes and genetic alterations in breast cancer cells using a combination of suppression subtractive hybridization, multiplex FISH and comparative genomic hybridization. Int. J. Oncol., 21, 499-507.
42. Yan, P.S., Efferth, T., Chen, H.L., Lin, J., Rodel, F., Fuzesi, L. and Huang, T.H. (2002) Use of CpG island microarrays to identify colorectal tumors with a high degree of concurrent methylation. Methods, 27, 162-169.
43. Yoshikawa, H., Matsubara, K., Qian, G.S., Jackson, P., Groopman, J.D., Manning, J.E., Harris, C.C. and Herman, J.G. (2001) SOCS-1, a negative regulator of the JAK/STAT pathway, is silenced by methylation in human hepatocellular carcinoma and shows growth-suppression activity. Nat. Genet., 28, 29-35.
44. Zhang, Y., Ng, H.H., Erdjument-Bromage, H., Tempst, P., Bird, A. and Reinberg, D. (1999) Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev., 13, 1924-1935.