Methyl-CpG-binding proteins in cancer: Blaming the DNA methylation messenger

Biochemistry and Cell Biology

Volumn 83, Issue 3, 2005, Pages 374-384

  Ballestar, Esteban ^a   Esteller, Manel ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

Cancer epigenetics; DNA methylation; MeCP2; Methyl CpG binding; Rett syndrome

Indexed keywords

CYTOLOGY; GENES; PATTERN RECOGNITION; TUMORS;

CANCER EPIGENETICS; DNA METHYLATION; MECP2; METHYL-CPG-BINDING; RETT SYNDROME;

PROTEINS;

HISTONE; METHYL CPG BINDING PROTEIN 2;

AMINO ACID SEQUENCE; CANCER; DNA BINDING; DNA METHYLATION; EPIGENETICS; EXCISION REPAIR; GENE REPRESSION; GENETIC TRANSCRIPTION; HUMAN; MISMATCH REPAIR; NONHUMAN; PROTEIN MODIFICATION; PROTEIN PROCESSING; REVIEW; TUMOR CELL; TUMOR SUPPRESSOR GENE;

ANIMALS; CELL NUCLEUS; CHROMOSOMAL PROTEINS, NON-HISTONE; CPG ISLANDS; DNA METHYLATION; DNA REPAIR; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; GENOME, HUMAN; HUMANS; METHYL-CPG-BINDING PROTEIN 2; MODELS, BIOLOGICAL; MODELS, GENETIC; NEOPLASMS; PROTEIN BINDING; REPRESSOR PROTEINS; RETT SYNDROME; TRANSCRIPTION, GENETIC;

EID: 24744453331     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o05-035     Document Type: Review

References (100)

1. Aissani, B., and Bernardi, G. 1991. CpG islands: features and distribution in the genomes of vertebrates. Gene, 106: 173-183.
2. Allfrey, V.G. 1966. Structural modifications of histones and their possible role in the regulation of ribonucleic acid synthesis. Proc. Can. Cancer Res. Conf. 6: 313-335.
3. Amir, R.E., Van den Veyver, I.B., Wan, M., Tran, C.Q., Francke, U., and Zoghbi, H.Y. 1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23:185-188.
4. Bader, S., Walker, M., McQueen, H.A., Sellar, R., Oei, E., Wopereis, S. et al. 2003. MBD1, MBD2 and CGBP genes at chromosome 18q21 are infrequently mutated in human colon and lung cancers. Oncogene, 22: 3506-3510.
5. 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.
6. Ballestar, E., and Esteller, M. 2003. Methylated DNA-binding proteins. In Nature encyclopedia of the human genome, London. Edited by D.N. Cooper. Nature Publishing Group. Vol. 3, pp. 903-907.
7. Ballestar, E., Pile, L.A., Wassarman, D.A., Wolffe, A.P., and Wade, P.A. 2001. A Drosophila MBD member is a transcriptional corepressor associated with specific genes. Eur. J. Biochem. 268: 5397-5406.
8. Ballestar, E., Paz, M.F., Valle, L., Wei, S., Fraga, M.F., Espada, J. et al. 2003. Methyl-CpG binding proteins identify novel sites of epigenetic inactivation in human cancer. EMBO J. 22: 6335-6345.
9. Ballestar, E., Ropero, S. Alaminos, M., Armstrong, J., Setien, F., Agrelo, R. et al. 2005. The impact of MECP2 mutations in the expression patterns of Rett syndrome patients. Hum. Genet. 116: 91-104.
10. Balmer, D., Arredondo, J., Samaco, R.C., and LaSalle, J.M. 2002. MECP2 mutations in Rett syndrome adversely affect lymphocyte growth, but do not affect imprinted gene expression in blood or brain. Hum. Genet. 110: 545-552.
11. Bauer, U.M., Daujat, S., Nielsen, S.J., Nightingale, K., and Kouzarides, T. 2002. Methylation at arginine 17 of histone H3 is linked to gene activation. EMBO Rep. 3: 39-44.
12. Billard, L.M., Magdinier, F., Lenoir, G.M., Frappart, L., and Dante, R. 2002. MeCP2 and MBD2 expression during normal and pathological growth of the human mammary gland. Oncogene, 21: 2704-2712.
13. Chahal, S.S., Matthews, H.R., and Bradbury, E.M. 1980. Acetylation of histone H4 and its role in chromatin structure and function. Nature (London), 287: 76-79.
14. Chen, T., and Li, E. 2004. Structure and function of eukaryotic DNA methyltransferases. Curr. Top. Dev. Biol. 60: 55-89.
15. Chen, R.Z., Pettersson, U., Beard, C., Jackson-Grusby, L., and Jaenisch, R. 1998. DNA hypomethylation leads to elevated mutation rates. Nature (London), 395: 89-93.
16. Chen, W.G., Chang, Q., Lin, Y., Meissner, A., West, A.E., Griffith, E.C. et al. 2003. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science (Wash.), 302: 885-889.
17. Costello, J.F., Fruhwald, M.C., Smiraglia, D.J., Rush, L.J., Robertson, G.P., Gao, X. et al. 2000. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat. Genet. 24(2): 132-138.
18. Cross, S.H., Charlton, J.A., Nan, X., and Bird, A.P. Purification of CpG islands using a methylated DNA binding column. 1994. Nat. Genet. 6: 236-244.
19. Espada, J., Ballestar, E., Fraga, M.F., Villar-Garea, A., Juarranz, A., Stockert, J.C. et al. Human DNMT1 is essential to maintain the histone H3 modification pattern. 2004. J. Biol. Chem. 279: 37175-37184.
20. Esteller, M. 2002. CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future. Oncogene, 21: 5427-5440.
21. Esteller, M., Levine, R., Baylin, S.B., Ellenson, L.H., and Herman, J.G. 1998. MLH1 promoter hypermethylation is associated with the microsatellite instability phenotype in sporadic endometrial carcinomas. Oncogene, 17: 2413-2417.
22. Esteller, M., Catasus, L., Matias-Guiu, X., Mutter, G.L., Prat, J., Baylin, S.B. et al. 1999. hMLH1 promoter hypermethylation is an early event in human endometrial tumorigenesis. Am. J. Pathol. 155: 1767-1772.
23. Esteller, M., Toyota, M., Sanchez-Cespedes, M., Capella, G., Peinado, M.A., Watkins, D.N. et al. 2000. Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is associated with G to A mutations in K-ras in colorectal tumorigenesis. Cancer Res. 60: 2368-2371.
24. Esteller, M., Corn, P.G., Baylin, S.B., and Herman, J.G. 2001. A gene hypermethylation profile of human cancer. Cancer Res. 61(8): 3225-3229.
25. Feinberg, A.P., and Vogelstein, B. 1983. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature (London), 301: 89-92.
26. Feng, Q., and Zhang, Y. 2001. The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev. 15: 827-832.
27. Fleisher, A.S., Esteller, M., Wang, S., Tamura, G., Suzuki, H., Yin, J. et al. 1999. Hypermethylation of the hMLH1 gene promoter in human gastric cancers with microsatellite instability. Cancer Res. 59: 1090-1095.
28. Fournier, C., Goto, Y., Ballestar, E., Delaval, K., Hever, A., Esteller, M. et al. 2002. Allele-specific histone lysine methylation marks regulatory regions at imprinted mouse genes. EMBO J. 21: 6560-6570.
29. 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.
30. Fraga, M.F., Ballestar, E., Villar-Garea, A., Boix-Chornet, M., Espada, J., Schotta, G. et al. 2005. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat. Genet. 37: 391-400.
31. Fujita, N., Shimotake, N., Ohki, I., Chiba, T., Saya, H., Shirakawa, M. et al. 2000. Mechanism of transcriptional regulation by methyl-CpG binding protein MBD1. Mol. Cell. Biol. 20: 5107-5018.
32. Fujita, H., Fujii, R., Aratani, S., Amano, T., Fukamizu, A., and Nakajima, T. 2003a. Antithetic effects of MBD2a on gene regulation. Mol. Cell. Biol. 23: 2645-2657.
33. Fujita, N., Watanabe, S., Ichimura, T., Tsuruzoe, S., Shinkai, Y., Tachibana, M. et al. 2003b. 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.
34. 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.
35. Gardineriner-Garden, M., and Frommer, M. 1987. CpG islands in vertebrate genomes. J. Mol. Biol. 196: 261-282.
36. 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.
37. Gonzalez-Zulueta, M., Bender, C.M., Yang, A.S., Nguyen, T., Beart, R.W., Van Tornout, J.M. et al. 1995. Methylation of the 5′ CpG island of the p16/CDKN2 tumor suppressor gene in normal and transformed human tissues correlates with gene silencing. Cancer Res. 55: 4531-4535.
38. Hardeland, U., Bentele, M., Lettieri, T., Steinacher, R., Jiricny, J., and Schar, P. 2001. Thymine DNA glycosylase. Prog. Nucleic Acid Res. Mol. Biol. 68: 235-253.
39. Hendrich, B., and Bird, A. 1998. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell. Biol. 18: 6538-6547.
40. Hendrich, B., Hardeland, U., Ng, H.H., Jiricny, J., and Bird, A. 1999. The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature (London), 401: 301-304.
41. 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.
42. Herman, J.G., Umar, A., Polyak, K., Graff, J.R., Ahuja, N., Issa, J.P. et al. 1998. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc. Natl. Acad. Sci. U.S.A. 95: 6870-6875.
43. Jones, P.L., Veenstra, G.J., Wade, P.A., Vermaak, D., Kass, S.U., Landsberger, N. et al. 1998. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19: 187-191.
44. Jorgensen, H.F., Ben-Porath, I., Bird, A.P. 2004. Mbd1 is recruited to both methylated and nonmethylated CpGs via distinct DNA binding domains. Mol. Cell Biol. 24: 3387-3395.
45. Kaludov, N.K., and Wolffe, A.P. 2000. MeCP2 driven transcriptional repression in vitro: selectivity for methylated DNA, action at a distance and contacts with the basal transcription machinery. Nucleic Acids Res. 28: 1921-1928.
46. Keshet, I., Lieman-Hurwitz, J., and Cedar H. 1986. DNA methylation affects the formation of active chromatin. Cell, 44: 535-543.
47. Koch, C., and Stratling, W.H. 2004. DNA binding of methyl-CpG-binding protein MeCP2 in human MCF7 cells. Biochemistry, 43: 5011-5021.
48. 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 proteins. Nature (London), 410: 116-120.
49. Lembo, F., Pero, R., Angrisano, T., Vitiello, C., Iuliano, R., Bruni, C.B. et al. 2003. MBDin, a novel MBD2-interacting protein, relieves MBD2 repression potential and reactivates transcription from methylated promoters. Mol. Cell Biol. 23: 1656-1665.
50. Leu, Y.W., Yan, P.S., Fan, M., Jin, V.X., Liu, J.C., Curran, E.M. et al. Loss of estrogen receptor signaling triggers epigenetic silencing of downstream targets in breast cancer. Cancer Res. 64: 8184-8192.
51. Lewis, J.D., Meehan, R.R., Henzel, W.J., Maurer-Fogy, I., Jeppesen, P., Klein, F. et al. 1992. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell, 69: 905-914.
52. Magdinier, F., Billard, L.M., Wittmann, G., Frappart, L., Benchaib, M., Lenoir, G.M. et al. 2000. Regional methylation of the 5′ end CpG island of BRCA1 is associated with reduced gene expression in human somatic cells. FASEB J. 14: 1585-1594.
53. 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. U.S.A. 98: 4990-4995.
54. Mancini, D.N., Singh, S.M., Archer, T.K., and Rodenhiser, D.I. 1999. Site-specific DNA methylation in the neurofibromatosis (NF1) promoter interferes with binding of CREB and SP1 transcription factors. Oncogene, 18: 4108-4119.
55. Matarazzo, V., and Ronnett, G.V. 2004. Temporal and regional differences in the olfactory proteome as a consequence of MeCP2 deficiency. Proc. Natl. Acad. Sci. U.S.A. 101: 7763-7768.
56. Meehan, R.R., Lewis, J.D., McKay, S., Kleiner, E.L., and Bird, A.P. 1989. Identification of a mammalian protein that binds specifically to DNA containing methylated CpGs. Cell, 58: 499-507.
57. Merlo, A., Herman, J.G., Mao, L., Lee, D.J., Gabrielson, E., Burger, P.C. et al. 1995. 5′ CpG island methylation is associated with transcriptional silencing of the tumour suppressor p16/ CDKN2/MTS1 in human cancers. Nat. Med. 1: 686-692.
58. Millar, C.B., Guy, J., Sansom, O. J., Selfridge, J., MacDougall, E., Hendrich, B. et al. 2002. Enhanced CpG mutability and tumorigenesis in MBD4-deficient mice. Science (Wash.), 297: 403-405.
59. Miller, O.J., Schnedl, W., Allen, J., and Erlanger, B.F. 1974. 5-Methylcytosine localised in mammalian constitutive heterochromatin. Nature (London), 251: 636-637.
60. Muller, H.M., Fiegl, H., Goebel, G., Hubalek, M.M., Widschwendter, A., Muller-Holzner, E. et al. 2003. MeCP2 and MBD2 expression in human neoplastic and non-neoplastic breast tissue and its association with oestrogen receptor status. Br. J. Cancer, 89: 1934-1939.
61. Nakayama, J., Rice, J.C., Strahl, B.D., Allis, C.D., and Grewal, S.I. 2001. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science (Wash.), 292: 110-113.
62. Nan, X., Ng, H.H., Johnson, C.A., Laherty, C.D., Turner, B.M., Eisenman, R.N. et al. 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature (London), 393: 386-389.
63. Nan, X., Campoy, F.J., and Bird, A. 1997. MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell, 88: 471-481.
64. 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.
65. Ng, H.H., Zhang, Y., Hendrich, B., Johnson, C.A., Turner, B.M., Erdjument-Bromage, H. et al. 1999. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 23: 58-61.
66. 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.
67. Ohki, I., Shimotake, N., Fujita, N., Jee, J., Ikegami, T., Nakao, M. et al. 2001. Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell, 105: 487-497.
68. Prokhortchouk, A., Hendrich, B., Jorgensen, H., Ruzov, A., Wilm, M., Georgiev, G. et al. 2001. The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor. Genes Dev. 15: 1613-1618.
69. Reik, W., Collick, A., Norris, M.L., Barton, S.C., and Surani, M.A. 1987. Genomic imprinting determines methylation of parental alleles in transgenic mice. Nature (London), 328: 248-251.
70. Riccio, A., Aaltonen, L.A., Godwin, A.K., Loukola, A., Percesepe, A., Salovaara, R. et al. 1999. The DNA repair gene MBD4 (MED1) is mutated in human carcinomas with microsatellite instability. Nat. Genet. 23: 266-268.
71. Roloff, T.C., Ropers, H.H., and Nuber, U.A. 2003. Comparative study of methyl-CpG-binding domain proteins. BMC Genomics, 4: 1-9.
72. Rundlett, S.E., Carmen, A.A., Suka, N., Turner, B.M., and Grunstein, M. 1998. Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3. Nature (London), 392: 831-835.
73. Sakai, H., Urano, T., Ookata, K., Kim, M.H., Hirai, Y., Saito, M. et al. 2002. MBD3 and HDAC1, two components of the NuRD complex, are localized at Aurora-A-positive centrosomes in M phase. J. Biol. Chem. 277: 48714-48723.
74. Saito, Y., Kanai, Y., Sakamoto, M., Saito, H., Ishii, H., and Hirohashi, S. 2001. Expression of mRNA for DNA methyltransferases and methyl-CpG-binding proteins and DNA methylation status on CpG islands and pericentromeric satellite regions during human hepatocarcinogenesis. Hepatology, 33: 561-568.
75. Sansom, O.J., Berger, J., Bishop, S.M., Hendrich, B., Bird, A., and Clarke, A.R. 2003. Deficiency of Mbd2 suppresses intestinal tumorigenesis. Nat. Genet. 34: 145-147.
76. Santoro, R., and Grummt, I. 2001. Molecular mechanisms mediating methylation-dependent silencing of ribosomal gene transcription. Mol. Cell, 8: 719-725.
77. Santoro, R., Li, J., and Grummt, I. 2002. The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat. Genet. 32: 393-396.
78. Santos-Rosa, H., Schneider, R., Bannister, A.J., Sherriff, J., Bernstein, B.E., Emre, N.C. et al. 2002. Active genes are tri-methylated at K4 of histone H3. Nature (London), 419: 407-411.
79. Sato, M., Horio, Y., Sekido, Y., Minna, J.D., Shimokata, K., and Hasegawa, Y. 2002. The expression of DNA methyltransferases and methyl-CpG-binding proteins is not associated with the methylation status of p14(ARF), p16(INK4a) and RASSF1A in human lung cancer cell lines. Oncogene, 21: 4822-489.
80. Schroeder, M.D., Symowicz, J., and Schuler, L.A. 2002. PRL modulates cell cycle regulators in mammary tumor epithelial cells. Mol. Endocrinol. 16: 45-57.
81. Sekimata, M., and Homma, Y. 2004. Sequence-specific transcriptional repression by an MBD2-interacting zinc finger protein MIZF. Nucleic Acids Res. 32: 590-597.
82. Sekimata, M., Takahashi, A., Murakami-Sekimata, A., and Homma, Y. 2001. Involvement of a novel zinc finger protein, MIZF, in transcriptional repression by interacting with a methyl-CpG-binding protein, MBD2. J. Biol. Chem. 276: 42632-42638.
83. Schotta, G., Lachner, M., Sarma, K., Ebert, A., Sengupta, R., Reuter, G. et al. 2004. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18: 1251-1262.
84. Schultz, D.C., Ayyanathan, K., Negorev, D., Maul, G.G., and Rauscher, F.J. 3rd. 2002. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 16: 919-932.
85. Shen, C.K., and Maniatis, T. 1980. Tissue-specific DNA methylation in a cluster of rabbit beta-like globin genes. Proc. Natl. Acad. Sci. U.S.A. 77: 6634-6638.
86. Takizawa, T., Nakashima, K., Namihira, M., Ochiai, W., Uemura, A., Yanagisawa, M. et al. 2001. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev. Cell, 1: 749-758.
87. Tate, P.H., and Bird, A.P. 1993. Effects of DNA methylation on DNA-binding proteins and gene expression. Curr. Opin. Genet. Dev. 3: 226-231.
88. Tudor, M., Akbarian, S., Chen, R.Z., and Jaenisch, R. 2002. Transcriptional profiling of a mouse model for Rett syndrome reveals subtle transcriptional changes in the brain. Proc Natl Acad Sci U.S.A. 99: 15536-15541.
89. 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.
90. Wade, P.A. 2001. Methyl CpG-binding proteins and transcriptional repression. Bioessays, 23: 1131-1137.
91. Wakefield, R.I., Smith, B.O., Nan, X., Free, A., Soteriou, A., Uhrin, D. et al. 1999. The solution structure of the domain from MeCP2 that binds to methylated DNA. J. Mol. Biol. 291: 1055-1065.
92. Walsh, C.P., Chaillet, J.R., and Bestor, T.H. 1998. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20: 116-117.
93. Wang, Y., Fischle, W., Cheung, W., Jacobs, S., Khorasanizadeh, S., and Allis, C.D. 2004. Beyond the double helix: writing and reading the histone code. Novartis Found. Symp. 259: 3-17.
94. Watanabe, S., Ichimura, T., Fujita, N., Tsuruzoe, S., Ohki, I., Shirakawa, M. et al. 2003. Methylated DNA-binding domain 1 and methylpurine-DNA glycosylase link transcriptional repression and DNA repair in chromatin. Proc. Natl. Acad. Sci. U.S.A. 100: 12859-12564.
95. 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.
96. Welsch, C.W. 1978. Prolactin and the development and progression of early neoplastic mammary gland lesions. Cancer Res. 38: 4054-4058.
97. Wolf, S.F., and Migeon, B.R. 1982. Studies of X chromosome DNA methylation in normal human cells. Nature, 295: 667-671.
98. Xu, G.L., Bestor, T.H., Bourc'his, D., Hsieh, C.L., Tommerup, N., Bugge, M. et al. 1999. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature (London), 402: 187-191.
99. Yoon, H.G., Chan, D.W., Reynolds, A.B., Qin, J., and Wong, J. 2003. N-CoR mediates DNA methylation-dependent repression through a methyl CpG binding protein Kaiso. Mol. Cell, 12: 723-734.
100. Zhao, X., Ueba, T., Christie, B.R., Barkho, B., McConnell, M.J., Nakashima, K. et al. 2003. Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc. Natl. Acad. Sci. U.S.A. 100: 6777-6782.