The Role of the Epigenetic Signal, DNA Methylation, in Gene Regulation During Erythroid Development

Current Topics in Developmental Biology

Volumn 82, Issue , 2008, Pages 85-116

  Ginder, Gordon D ^a   Gnanapragasam, Merlin N ^a   Mian, Omar Y ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLOBIN;

ANIMAL; CYTOLOGY; DNA METHYLATION; ERYTHROID CELL; ERYTHROPOIESIS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HUMAN; METABOLISM; REVIEW;

ANIMALS; DNA METHYLATION; EPIGENESIS, GENETIC; ERYTHROID CELLS; ERYTHROPOIESIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLOBINS; HUMANS;

EID: 39049132485     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0070-2153(07)00004-X     Document Type: Review

References (138)

1. Amaravadi L., and Klemsz M.J. DNA methylation and chromatin structure regulate PU.1 expression. DNA Cell Biol. 18 12 (1999) 875-884
2. Ballestar E., and Wolffe A. Methyl-CpG-binding proteins: Targeting specific gene repression. Eur. J. Biochem. 268 (2001) 1-6
3. Barbour V.M., Tufarelli C., Sharpe J.A., Smith Z.E., Ayyub H., Heinlein C.A., Sloane-Stanley J., Indrak K., Wood W.G., and Higgs D.R. Alpha-thalassemia resulting from a negative chromosomal position effect. Blood 96 3 (2000) 800-807
4. Barreto G., Schafer A., Marhold J., Stach D., Swaminathan S.K., Handa V., Doderlein G., Maltry N., Wu W., Lyko F., and Niehrs C. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445 7128 (2007) 671-675
5. Barrie P.A., Jeffreys A.J., and Scott A.F. Evolution of the beta-globin gene cluster in man and the primates. J. Mol. Biol. 149 3 (1981) 319-336
6. Baylin S.B. DNA methylation and gene silencing in cancer. Nat. Clin. Pract. Oncol. 2 Suppl. 1 (2005) S4-S11
7. Bellacosa A., Cicchillitti L., Schepis F., Riccio A., Yeung A.T., Matsumoto Y., Golemis E.A., Genuardi M., and Neri G. MED1, a novel human methyl-CpG-binding endonuclease, interacts with DNA mismatch repair protein MLH1. Proc. Natl. Acad. Sci. USA 96 7 (1999) 3969-3974
8. Bhattacharya S.K., Ramchandani S., Cervoni N., and Szyf M. A mammalian protein with specific demethylase activity for mCpG DNA. Nature 397 6720 (1999) 579-583
9. Bird A.P. DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res. 8 7 (1980) 1499-1504
10. Bird A.P., Taggart M.H., Nicholls R.D., and Higgs D.R. Non-methylated CpG-rich islands at the human alpha-globin locus: Implications for evolution of the alpha-globin pseudogene. EMBO J. 6 4 (1987) 999-1004
11. Bowen N., Fujita N., Kajita M., and Wade P. Mi-2/NuRD: Multiple complexes for many purposes. Biochemica et Biophysica Acta 1677 (2004) 52-57
12. Boyes J., and Bird A. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 64 6 (1991) 1123-1134
13. Brenner C., Deplus R., Didelot C., Loriot A., Vire E., De Smet C., Gutierrez A., Danovi D., Bernard D., Boon T., Pelicci P.G., Amati B., et al. Myc represses transcription through recruitment of DNA methyltransferase corepressor. EMBO J. 24 2 (2005) 336-346
14. Brinkman A.B., Pennings S.W., Braliou G.G., Rietveld L.E., and Stunnenberg H.G. DNA methylation immediately adjacent to active histone marking does not silence transcription. Nucleic Acids Res. 35 3 (2007) 801-811
15. Burns L.J., Glauber J.G., and Ginder G.D. Butyrate induces selective transcriptional activation of a hypomethylated embryonic globin gene in adult erythroid cells. Blood 72 5 (1988) 1536-1542
16. Cantor A.B., and Orkin S.H. Hematopoietic development: A balancing act. Curr. Opin. Genet. Dev. 11 5 (2001) 513-519
17. Chan L., Weidmann M., and Ingram V. Regulation of specific gene expression during embryonic development: Synthesis of globin messenger RNA during red cell formation in chick embryos. Dev. Biol. 40 1 (1974) 174-185
18. Charache S., Dover G.J., Smith K., Talbot Jr. C.C., Moyer M., and Boyer S. Treatment of sickle cell anemia with 5-azacytidine results in increased fetal hemoglobin production and is associated with nonrandom hypomethylation of DNA around the gamma-delta-beta-globin gene complex. Proc. Natl. Acad. Sci. USA 80 15 (1983) 4842-4846
19. Chihara Y., Sugano K., Kobayashi A., Kanai Y., Yamamoto H., Nakazono M., Fujimoto H., Kakizoe T., Fujimoto K., Hirohashi S., and Hirao Y. Loss of blood group A antigen expression in bladder cancer caused by allelic loss and/or methylation of the ABO gene. Lab. Invest. 85 7 (2005) 895-907
20. Daniel J.M., and Reynolds A.B. The catenin p120(ctn) interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor. Mol. Cell. Biol. 19 5 (1999) 3614-3623
21. DeSimone J., and Mueller A.L. Fetal hemoglobin synthesis in baboons (Papio cynocephalus). J. Lab. Clin. Med. 91 6 (1978) 862-871
22. DeSimone J., Heller P., Hall L., and Zwiers D. 5-Azacytidine stimulates fetal hemoglobin synthesis in anemic baboons. Proc. Natl. Acad. Sci. USA 79 14 (1982) 4428-4431
23. Di Croce L., Raker V.A., Corsaro M., Fazi F., Fanelli M., Faretta M., Fuks F., Lo C.F., Kouzarides T., Nervi C., Minucci S., and Pelicci P.G. Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor. Science 295 5557 (2002) 1079-1082
24. Eckhardt F., Lewin J., Cortese R., Rakyan V.K., Attwood J., Burger M., Burton J., Cox T.V., Davies R., Down T.A., Haefliger C., Horton R., et al. DNA methylation profiling of human chromosomes 6, 20 and 22. Nat. Genet. 38 12 (2006) 1378-1385
25. Egger G., Liang G., Aparicio A., and Jones P. Epigenetics in human disease and prospects for epigenetic therapy. Nature 429 6990 (2004) 457-463
26. Ehrlich M. The controversial denouement of vertebrate DNA methylation research. Biochemistry (Mosc.) 70 5 (2005) 568-575
27. Enver T., Zhang J.W., Papayannopoulou T., and Stamatoyannopoulos G. DNA methylation: A secondary event in globin gene switching?. Genes Dev. 2 6 (1988) 698-706
28. Feng Q., and Zhang Y. The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev. 15 7 (2001) 827-832
29. Feng Q., and Zhang Y. The NuRD complex: Linking histone modification to nucleosome remodeling. Curr. Top. Microbiol. Immunol. 274 (2003) 269-290
30. Filion G.J., Zhenilo S., Salozhin S., Yamada D., Prokhortchouk E., and Defossez P.A. A family of human zinc finger proteins that bind methylated DNA and repress transcription. Mol. Cell. Biol. 26 1 (2006) 169-181
31. Fujita N., Shimotake N., Ohki I., Chiba T., Saya H., Shirakawa M., and Nakao M. Mechanism of transcriptional regulation by methyl-CpG binding protein MBD1. Mol. Cell. Biol. 20 14 (2000) 5107-5118
32. Fuks F., Hurd P.J., Wolf D., Nan X., Bird A.P., and Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 278 6 (2003) 4035-4040
33. Gao S., Worm J., Guldberg P., Eiberg H., Krogdahl A., Liu C.J., Reibel J., and Dabelsteen E. Genetic and epigenetic alterations of the blood group ABO gene in oral squamous cell carcinoma. Int. J. Cancer 109 2 (2004) 230-237
34. Ge Y.Z., Pu M.T., Gowher H., Wu H.P., Ding J.P., Jeltsch A., and Xu G.L. Chromatin targeting of de novo DNA methyltransferases by the PWWP domain. J. Biol. Chem. 279 24 (2004) 25447-25454
35. Gibbons R.J., Picketts D.J., Villard L., and Higgs D.R. Mutations in a putative global transcriptional regulator cause X-linked mental retardation with alpha-thalassemia (ATR-X syndrome). Cell 80 6 (1995) 837-845
36. Gibbons R.J., McDowell T.L., Raman S., O'Rourke D.M., Garrick D., Ayyub H., and Higgs D.R. Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nat. Genet. 24 4 (2000) 368-371
37. Gibbons R.J., Pellagatti A., Garrick D., Wood W.G., Malik N., Ayyub H., Langford C., Boultwood J., Wainscoat J.S., and Higgs D.R. Identification of acquired somatic mutations in the gene encoding chromatin-remodeling factor ATRX in the alpha-thalassemia myelodysplasia syndrome (ATMDS). Nat. Genet. 34 4 (2003) 446-449
38. Ginder G.D., and McGhee J.D. DNA methylation in the chicken adult beta-globin gene: A relationship with gene expression. "Organization and Expression of Globin Genes," (1981), Liss, New York 191
39. Ginder G.D., Whitters M.J., and Pohlman J.K. Activation of a chicken embryonic globin gene in adult erythroid cells by 5-azacytidine and sodium butyrate. Proc. Natl. Acad. Sci. USA 81 13 (1984) 3954-3958
40. Groudine M., Peretz M., and Weintraub H. Transcriptional regulation of hemoglobin switching in chicken embryos. Mol. Cell. Biol. 1 3 (1981) 281-288
41. Haigh L.S., Owens B.B., Hellewell O.S., and Ingram V.M. DNA methylation in chicken alpha-globin gene expression. Proc. Natl. Acad. Sci. USA 79 17 (1982) 5332-5336
42. Harikrishnan K., Chow M., Baker E.P.S., Bassal S., Brasacchio D., Wang L., Craig J., Jones P., Sif S., and El-Osta A. Brahma links the SWI/SNF chromatin-remodeling complex with MeCP2-dependent transcriptional silencing. Nat. Genet. 37 3 (2005) 254-264
43. Hendrich B., and Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell. Biol. 18 11 (1998) 6538-6547
44. Hendrich B., and Tweedie S. The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet. 19 5 (2003) 269-277
45. Hendrich B., Hardeland U., Ng H.H., Jiricny J., and Bird A. The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature 401 6750 (1999) 301-304
46. Hendrich B., Guy J., Ramsahoye B., Wilson V.A., and Bird A. Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development. Genes Dev. 15 6 (2001) 710-723
47. Higgs D.R., Garrick D., Anguita E., De Gobbi M., Hughes J., Muers M., Vernimmen D., Lower K., Law M., Argentaro A., Deville M.A., and Gibbons R. Understanding alpha-globin gene regulation: Aiming to improve the management of thalassemia. Ann. NY Acad. Sci. 1054 (2005) 92-102
48. Holliday R., and Pugh J.E. DNA modification mechanisms and gene activity during development. Science 187 4173 (1975) 226-232
49. Hsu M., Mabaera R., Lowrey C.H., Martin D.I., and Fiering S. CpG hypomethylation in a large domain encompassing the embryonic {beta}-like globin genes in primitive erythrocytes. Mol. Cell. Biol. 27 13 (2007) 5047-5054
50. Hu K., Nan X., Bird A., and Wang W. Testing for association between MeCP2 and the brahma-associated SWI/SNF chromatin-remodeling complex. Nat. Genet. 38 9 (2006) 962-964
51. Hu M., Krause D., Greaves M., Sharkis S., Dexter M., Heyworth C., and Enver T. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev. 11 6 (1997) 774-785
52. Hutchins A.S., Mullen A.C., Lee H.W., Sykes K.J., High F.A., Hendrich B.D., Bird A.P., and Reiner S.L. Gene silencing quantitatively controls the function of a developmental trans-activator. Mol. Cell 10 1 (2002) 81-91
53. Hutchins A.S., Artis D., Hendrich B.D., Bird A.P., Scott P., and Reiner S.L. Cutting edge: A critical role for gene silencing in preventing excessive type 1 immunity. J. Immunol. 175 9 (2005) 5606-5610
54. Iwasaki H., Mizuno S., Arinobu Y., Ozawa H., Mori Y., Shigematsu H., Takatsu K., Tenen D.G., and Akashi K. The order of expression of transcription factors directs hierarchical specification of hematopoietic lineages. Genes Dev. 20 21 (2006) 3010-3021
55. Jackson J.P., Lindroth A.M., Cao X., and Jacobsen S.E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416 6880 (2002) 556-560
56. Jaenisch R., and Bird A. Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nat. Genet. 33 Suppl (2003) 245-254
57. Jiang C.-L., Jin S.-G., and Pfeifer G. MBD3L1 is a transcriptional repressor that interacts with methyl-CpG-binding protein 2 (MBD2) and components of the NuRD complex. J. Biol. Chem. 279 80 (2004) 51456-52464
58. Jin S.G., Jiang C.L., Rauch T., Li H., and Pfeifer G.P. MBD3L2 interacts with MBD3 and components of the NuRD complex and can oppose MBD2-MeCP1-mediated methylation silencing. J. Biol. Chem. 280 13 (2005) 12700-12709
59. Johnson L.M., Bostick M., Zhang X., Kraft E., Henderson I., Callis J., and Jacobsen S.E. The SRA methyl cytosine binding domain links DNA and histone methylation. Curr. Biol. 17 4 (2007) 379-384
60. Jones P.A. DNA methylation and cancer. Oncogene 21 35 (2002) 5358-5360
61. Jones P.A., and Baylin S.B. The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 3 6 (2002) 415-428
62. Jost J.P. Nuclear extracts of chicken embryos promote an active demethylation of DNA by excision repair of 5-methyldeoxycytidine. Proc. Natl. Acad. Sci. USA 90 10 (1993) 4684-4688
63. Jost J.P., Siegmann M., Sun L., and Leung R. Mechanisms of DNA demethylation in chicken embryos. Purification and properties of a 5-methylcytosine-DNA glycosylase. J. Biol. Chem. 270 17 (1995) 9734-9739
64. Jost J.P., Oakeley E.J., Zhu B., Benjamin D., Thiry S., Siegmann M., and Jost Y.C. 5-Methylcytosine DNA glycosylase participates in the genome-wide loss of DNA methylation occurring during mouse myoblast differentiation. Nucleic Acids Res. 29 21 (2001) 4452-4461
65. Kafri T., Ariel M., Brandeis M., Shemer R., Urven L., McCarrey J., Cedar H., and Razin A. Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev. 6 5 (1992) 705-714
66. Kanellopoulou C., Muljo S.A., Kung A.L., Ganesan S., Drapkin R., Jenuwein T., Livingston D.M., and Rajewsky K. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19 4 (2005) 489-501
67. Klochkov D., Rincon-Arano H., Ioudinkova E.S., Valadez-Graham V., Gavrilov A., Recillas-Targa F., and Razin S.V. A CTCF-dependent silencer located in the differentially methylated area may regulate expression of a housekeeping gene overlapping a tissue-specific gene domain. Mol. Cell. Biol. 26 5 (2006) 1589-1597
68. Klose R.J., and Bird A.P. Genomic DNA methylation: The mark and its mediators. Trends Biochem. Sci. 31 2 (2006) 89-97
69. Kominato Y., Hata Y., Takizawa H., Tsuchiya T., Tsukada J., and Yamamoto F. Expression of human histo-blood group ABO genes is dependent upon DNA methylation of the promoter region. J. Biol. Chem. 274 52 (1999) 37240-37250
70. Kominato Y., Hata Y., Takizawa H., Matsumoto K., Yasui K., Tsukada J., and Yamamoto F. Alternative promoter identified between a hypermethylated upstream region of repetitive elements and a CpG island in human ABO histo-blood group genes. J. Biol. Chem. 277 40 (2002) 37936-37948
71. Kondo E., Gu Z., Horii A., and Fukushige S. The thymine DNA glycosylase MBD4 represses transcription and is associated with methylated p16(INK4a) and hMLH1 genes. Mol. Cell. Biol. 25 11 (2005) 4388-4396
72. Kransdorf E.P., Wang S.Z., Zhu S.Z., Langston T.B., Rupon J.W., and Ginder G.D. MBD2 is a critical component of a methyl cytosine binding protein complex isolated from primary erythroid cells. Blood 108 8 (2006) 2836-2845
73. Kuo M.T., Mandel J.L., and Chambon P. DNA methylation: Correlation with DNase I sensitivity of chicken ovalbumin and conalbumin chromatin. Nucleic Acids Res. 7 8 (1979) 2105-2113
74. Laslo P., Spooner C.J., Warmflash A., Lancki D.W., Lee H.J., Sciammas R., Gantner B.N., Dinner A.R., and Singh H. Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 126 4 (2006) 755-766
75. Lavelle D., Vaitkus K., Hankewych M., Singh M., and De Simone J. Developmental changes in DNA methylation and covalent histone modifications of chromatin associated with the epsilon-, gamma-, and beta-globin gene promoters in Papio anubis. Blood Cells Mol. Dis. 36 2 (2006) 269-278
76. Lavelle D., Vaitkus K., Hankewych M., Singh M., and DeSimone J. Effect of 5-aza-2′-deoxycytidine (Dacogen) on covalent histone modifications of chromatin associated with the epsilon-, gamma-, and beta-globin promoters in Papio anubis. Exp. Hematol. 34 3 (2006) 339-347
77. LeGuezennec X., Vermeulen M., Brinkman A.B., Hoeijmakers W.A., Cohen A., Lasonder E., and Stunnenberg H.G. MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol. Cell. Biol. 26 3 (2006) 843-851
78. + thalassemia. N. Engl. J. Med. 307 24 (1982) 1469-1475
79. Ley T.J., Chiang Y.L., Haidaris D., Anagnou N.P., Wilson V.L., and Anderson W.F. DNA methylation and regulation of the human beta-globin-like genes in mouse erythroleukemia cells containing human chromosome 11. Proc. Natl. Acad. Sci. USA 81 21 (1984) 6618-6622
80. Li E., Bestor T.H., and Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69 6 (1992) 915-926
81. Mabaera R.H., Richardson C.A., Johnson K.J., Hsu M., Fiering S.H., and Lowrey C.H. Developmental and differentiation-specific patterns of human {gamma} and {beta}-globin promoter DNA methylation. Blood 110 (2007) 1343-1352
82. Matzke M.A., and Birchler J.A. RNAi-mediated pathways in the nucleus. Nat. Rev. Genet. 6 1 (2005) 24-35
83. McGhee J.D., and Ginder G.D. Specific DNA methylation sites in the vicinity of the chicken beta-globin genes. Nature 280 5721 (1979) 419-420
84. Meehan R.R., Lewis J.D., McKay S., Kleiner E.L., and Bird A.P. Identification of a mammalian protein that binds specifically to DNA containing methylated CpGs. Cell 58 3 (1989) 499-507
85. Mellon P., Parker V., Gluzman Y., and Maniatis T. Identification of DNA sequences required for transcription of the human alpha 1-globin gene in a new SV40 host-vector system. Cell 27 2 Pt 1 (1981) 279-288
86. Monk M., Boubelik M., and Lehnert S. Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 99 3 (1987) 371-382
87. Morris K.V., Chan S.W., Jacobsen S.E., and Looney D.J. Small interfering RNA-induced transcriptional gene silencing in human cells. Science 305 5688 (2004) 1289-1292
88. Murchison E.P., Partridge J.F., Tam O.H., Cheloufi S., and Hannon G.J. Characterization of Dicer-deficient murine embryonic stem cells. Proc. Natl. Acad. Sci. USA 102 34 (2005) 12135-12140
89. Mutskov V.J., Farrell C.M., Wade P.A., Wolffe A.P., and Felsenfeld G. The barrier function of an insulator couples high histone acetylation levels with specific protection of promoter DNA from methylation. Genes Dev. 16 12 (2002) 1540-1554
90. Nan X., Ng H.H., Johnson C.A., Laherty C.D., Turner B.M., Eisenman R.N., and Bird A. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393 6683 (1998) 386-389
91. Ng H.H., Zhang Y., Hendrich B., Johnson C.A., Turner B.M., Erdjument-Bromage H., Tempst P., Reinberg D., and Bird A. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 23 1 (1999) 58-61
92. Ohm J.E., McGarvey K.M., Yu X., Cheng L., Schuebel K.E., Cope L., Mohammad H.P., Chen W., Daniel V.C., Yu W., Berman D.M., Jenuwein T., et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat. Genet. 39 2 (2007) 237-242
93. Okano M., Bell D.W., Haber D.A., and Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99 3 (1999) 247-257
94. Okitsu C.Y., and Hsieh C.-L. DNA methylation dictates histone H3K4 methylation. Mol. Cell. Biol. 27 7 (2007) 2746-2757
95. Pace B., Li Q., Peterson K., and Stamatoyannopoulos G. Alpha-amino butyric acid cannot reactivate the silenced gamma gene of the beta locus YAC transgenic mouse. Blood 84 12 (1994) 4344-4353
96. Peschle C., Mavilio F., Care A., Migliaccio G., Migliaccio A.R., Salvo G., Samoggia P., Petti S., Guerriero R., Marinucci M., Lazzaro D., and Russo G. Haemoglobin switching in human embryos: Asynchrony of zeta-alpha and epsilon-gamma-globin switches in primitive and definite erythropoietic lineage. Nature 313 5999 (1985) 235-238
97. Pikaart M.J., Recillas-Targa F., and Felsenfeld G. Loss of transcriptional activity of a transgene is accompanied by DNA methylation and histone deacetylation and is prevented by insulators. Genes Dev. 12 18 (1998) 2852-2862
98. Prokhortchouk A., Hendrich B., Jorgensen H., Ruzov A., Wilm M., Georgiev G., Bird A., and Prokhortchouk E. The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor. Genes Dev. 15 13 (2001) 1613-1618
99. Prokhortchouk A., Sansom O., Selfridge J., Caballero I.M., Salozhin S., Aithozhina D., Cerchietti L., Meng F.G., Augenlicht L.H., Mariadason J.M., Hendrich B., Melnick A., et al. Kaiso-deficient mice show resistance to intestinal cancer. Mol. Cell. Biol. 26 1 (2006) 199-208
100. Qiu C., Sawada K., Zhang X., and Cheng X. The PWWP domain of mammalian DNA methyltransferase Dnmt3b defines a new family of DNA-binding folds. Nat. Struct. Biol. 9 3 (2002) 217-224
101. Ramachandran K., Wert J.V., Gopisetty G., and Singal R. Developmentally regulated demethylase activity targeting the beta(A)-globin gene in primary avian erythroid cells. Biochemistry 46 11 (2007) 3416-3422
102. Razin A., and Riggs A.D. DNA methylation and gene function. Science 210 4470 (1980) 604-610
103. Razin S.V., Ioudinkova E.S., and Scherrer K. Extensive methylation of a part of the CpG island located 3.0-4.5 kbp upstream to the chicken alpha-globin gene cluster may contribute to silencing the globin genes in non-erythroid cells. J. Mol. Biol. 299 4 (2000) 845-852
104. Reese B.E., Bachman K.E., Baylin S.B., and Rountree M.R. The methyl-CpG binding protein MBD1 interacts with the p150 subunit of chromatin assembly factor 1. Mol. Cell. Biol. 23 9 (2003) 3226-3236
105. Reik W., and Walter J. Genomic imprinting: Parental influence on the genome. Nat. Rev. Genet. 2 1 (2001) 21-32
106. Riggs A.D. X inactivation, differentiation, and DNA methylation. Cytogenet. Cell Genet. 14 1 (1975) 9-25
107. Rupon J.W., Wang S.Z., Gaensler K., Lloyd J., and Ginder G.D. Methyl binding domain protein 2 mediates {gamma}-globin gene silencing in adult human betaYAC transgenic mice. Proc. Natl. Acad. Sci. USA 103 17 (2006) 6617-6622
108. Ruzov A., Dunican D.S., Prokhortchouk A., Pennings S., Stancheva I., Prokhortchouk E., and Meehan R.R. Kaiso is a genome-wide repressor of transcription that is essential for amphibian development. Development 131 24 (2004) 6185-6194
109. Santos-Rosa H., Schneider R., Bannister A.J., Sherriff J., Bernstein B.E., Emre N.C., Schreiber S.L., Mellor J., and Kouzarides T. Active genes are tri-methylated at K4 of histone H3. Nature 419 6905 (2002) 407-411
110. Sarraf S.A., and Stancheva I. Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol. Cell 15 4 (2004) 595-605
111. Scarano E., Iaccarino M., Grippo P., and Parisi E. The heterogeneity of thymine methyl group origin in DNA pyrimidine isostichs of developing sea urchin embryos. Proc. Natl. Acad. Sci. USA 57 5 (1967) 1394-1400
112. Schlesinger Y., Straussman R., Keshet I., Farkash S., Hecht M., Zimmerman J., Eden E., Yakhini Z., Ben Shushan E., Reubinoff B.E., Bergman Y., Simon I., et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat. Genet. 39 2 (2007) 232-236
113. Schuetze S., Stenberg P.E., and Kabat D. The Ets-related transcription factor PU.1 immortalizes erythroblasts. Mol. Cell. Biol. 13 9 (1993) 5670-5678
114. Sharpe J.A., Wells D.J., Whitelaw E., Vyas P., Higgs D.R., and Wood W.G. Analysis of the human alpha-globin gene cluster in transgenic mice. Proc. Natl. Acad. Sci. USA 90 23 (1993) 11262-11266
115. Shen C.K., and Maniatis T. Tissue-specific DNA methylation in a cluster of rabbit beta-like globin genes. Proc. Natl. Acad. Sci. USA 77 11 (1980) 6634-6638
116. Singal R., and vanWert J.M. De novo methylation of an embryonic globin gene during normal development is strand specific and spreads from the proximal transcribed region. Blood 98 12 (2001) 3441-3446
117. Singal R., Ferris R., Little J.A., Wang S.Z., and Ginder G.D. Methylation of the minimal promoter of an embryonic globin gene silences transcription in primary erythroid cells. Proc. Natl. Acad. Sci. USA 94 25 (1997) 13724-13729
118. Singal R., vanWert J., and Ferdinand Jr. L. Methylation of alpha-type embryonic globin gene alpha-pi represses transcription in primary erythroid cells. Blood 100 12 (2002) 4217-4222
119. Singal R., Wang S.Z., Sargent T., Zhu S.Z., and Ginder G.D. Methylation of promoter proximal-transcribed sequences of an embryonic globin gene inhibits transcription in primary erythroid cells and promotes formation of a cell type-specific methyl cytosine binding complex. J. Biol. Chem. 277 3 (2002) 1897-1905
120. Singh M., Lavelle D., Vaitkus K., Mahmud N., Hankewych M., and DeSimone J. The gamma-globin gene promoter progressively demethylates as the hematopoietic stem progenitor cells differentiate along the erythroid lineage in baboon fetal liver and adult bone marrow. Exp. Hematol. 35 1 (2007) 48-55
121. Sjakste N., Iarovaia O.V., Razin S.V., Linares-Cruz G., Sjakste T., Le Gac V., Zhao Z., and Scherrer K. A novel gene is transcribed in the chicken alpha-globin gene domain in the direction opposite to the globin genes. Mol. Gen. Genet. 262 6 (2000) 1012-1021
122. Song F., Smith J.F., Kimura M.T., Morrow A.D., Matsuyama T., Nagase H., and Held W.A. Association of tissue-specific differentially methylated regions (TDMs) with differential gene expression. Proc. Natl. Acad. Sci. USA 102 9 (2005) 3336-3341
123. Soppe W.J., Jasencakova Z., Houben A., Kakutani T., Meister A., Huang M.S., Jacobsen S.E., Schubert I., and Fransz P.F. DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J. 21 23 (2002) 6549-6559
124. Stamatoyannopoulos G. Control of globin gene expression during development and erythroid differentiation. Exp. Hematol. 33 3 (2005) 259-271
125. Svoboda P., Stein P., Filipowicz W., and Schultz R.M. Lack of homologous sequence-specific DNA methylation in response to stable dsRNA expression in mouse oocytes. Nucleic Acids Res. 32 12 (2004) 3601-3606
126. Swisher J.F., Rand E., Cedar H., and Marie P.A. Analysis of putative RNase sensitivity and protease insensitivity of demethylation activity in extracts from rat myoblasts. Nucleic Acids Res. 26 24 (1998) 5573-5580
127. Tagoh H., Melnik S., Lefevre P., Chong S., Riggs A.D., and Bonifer C. Dynamic reorganization of chromatin structure and selective DNA demethylation prior to stable enhancer complex formation during differentiation of primary hematopoietic cells in vitro. Blood 103 8 (2004) 2950-2955
128. Tamaru H., Zhang X., McMillen D., Singh P.B., Nakayama J., Grewal S.I., Allis C.D., Cheng X., and Selker E.U. Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat.Genet. 34 1 (2003) 75-79
129. Tate P.H., and Bird A.P. Effects of DNA methylation on DNA-binding proteins and gene expression. Curr. Opin. Genet. Dev. 3 2 (1993) 226-231
130. Ting A.H., Schuebel K.E., Herman J.G., and Baylin S.B. Short double-stranded RNA induces transcriptional gene silencing in human cancer cells in the absence of DNA methylation. Nat. Genet. 37 8 (2005) 906-910
131. van der Ploeg L.H., and Flavell R.A. DNA methylation in the human gamma delta beta-globin locus in erythroid and nonerythroid tissues. Cell 19 4 (1980) 947-958
132. Voso M.T., Burn T.C., Wulf G., Lim B., Leone G., and Tenen D.G. Inhibition of hematopoiesis by competitive binding of transcription factor PU.1. Proc. Natl. Acad. Sci. USA 91 17 (1994) 7932-7936
133. Wade P. Methyl CpG-binding proteins and transcriptional repression. BioEssays 23 12 (2001) 1131-1137
134. Walsh C.P., and Bestor T.H. Cytosine methylation and mammalian development. Genes Dev. 13 1 (1999) 26-34
135. Warnecke P.M., and Bestor T.H. Cytosine methylation and human cancer. Curr. Opin. Oncol. 12 1 (2000) 68-73
136. Wolffe A.P., Jones P.L., and Wade P.A. DNA demethylation. Proc. Natl. Acad. Sci. USA 96 11 (1999) 5894-5896
137. Yin H., and Blanchard K.L. DNA methylation represses the expression of the human erythropoietin gene by two different mechanisms. Blood 95 1 (2000) 111-119
138. Zhang P., Zhang X., Iwama A., Yu C., Smith K.A., Mueller B.U., Narravula S., Torbett B.E., Orkin S.H., and Tenen D.G. PU.1 inhibits GATA-1 function and erythroid differentiation by blocking GATA-1 DNA binding. Blood 96 8 (2000) 2641-2648