Regulation of DNA methylation activity through Dnmt3L promoter methylation by Dnmt3 enzymes in embryonic development

Human Molecular Genetics

Volumn 17, Issue 17, 2008, Pages 2654-2664

  Hu, Ye Guang ^a   Hirasawa, Ryutaro ^b,c   Hu, Jia Lei ^a   Hata, Kenichiro ^d   Li, Chun Liang ^e   Jin, Ying ^e   Chen, Taiping ^f   Li, En ^f   Rigolet, Muriel ^g   Viegas Péquignot, Evani ^g   Sasaki, Hiroyuki ^b,c   Xu, Guo Liang ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^d NATIONAL CENTER FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^e SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^f NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^g INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; DNA METHYLTRANSFERASE 3L;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOREGULATION; CONTROLLED STUDY; DNA METHYLATION; DNA TRANSCRIPTION; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENZYME ACTIVITY; EPIGENETICS; GENE DISRUPTION; GENE REPRESSION; GENETIC ANALYSIS; GENETIC DISORDER; ICF SYNDROME; MOUSE; NONHUMAN; PATHOGENESIS; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM;

ANIMALS; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EMBRYO IMPLANTATION; EMBRYONIC STEM CELLS; HUMANS; IMMUNOLOGIC DEFICIENCY SYNDROMES; MICE; POINT MUTATION; PROMOTER REGIONS (GENETICS); TRANSCRIPTION, GENETIC;

EID: 49649120959     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn165     Document Type: Article

References (49)

1. Jones, P.A. and Baylin, S.B. (2007) The epigenomics of cancer. Cell 128, 683-692.
2. Feinberg, A.P. (2007) Phenotypic plasticity and the epigenetics of human disease. Nature, 447, 433-440.
3. Morgan, H.D., Santos, F., Green, K., Dean, W. and Reik, W. (2005) Epigenetic reprogramming in mammals. Hum. Mol. Genet., 14; R47-R58.
4. Bestor, T.H. (2000) The DNA methyltransferases of mammals. Hum. Mol. Genet., 9, 2395-2402.
5. Okano, M., Xie, S. and Li, E. (1998) Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat. Genet., 19, 219-220.
6. Okano, M., Bell, D.W., Haber, D.A. and Li, E. (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell, 99, 247-257.
7. Ko, Y.G., Nishino, K., Hattori, N., Arai, Y., Tanaka, S. and Shiota, K. (2005) Stage-by-stage change in DNA methylation status of Dmnt1 locus during mouse early development. J. Biol. Chem., 280, 9627-9634.
8. Chen, T., Ueda, Y., Xie, S. and Li, E. (2002) A novel Dnmt3a isoform produced from an alternative promoter localizes to euchromatin and its expression correlates with active de novo methylation. J. Biol. Chem. 277, 38746-38754.
9. Xu, G.L., Bestor, T.H., Bourc'his, D., Hsieh, C.L., Tommerup, N., Bugge, M., Hulten, M., Qu, X., Russo, J.J. and Viegas-Pequignot, E. (1999) Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature, 402, 187-191.
10. Hansen, R.S., Wijmenga, C., Luo, P., Stanek, A.M., Canfield, T.K., Weemaes, C.M. and Gartler, S.M. (1999) The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc. Natl Acad. Sci. USA, 96, 14412-14417.
11. Aapola, U., Shibuya, K., Scott, H.S., Ollila, J., Vihinen, M., Heino, M., Shintani, A., Kawasaki, K., Minoshima, S., Krohn, K. et al. (2000) Isolation and initial characterization of a novel zinc finger gene, DNMT3L, on 21q22.3, related to the cytosine-5-methyltransferase 3 gene family. Genomics, 65, 293-298.
12. Bourc'his, D. and Bestor, T.H. (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature, 431, 96-99.
13. La Salle, S., Mertineit, C., Taketo, T., Moens, P.B., Bestor, T.H. and Trasler, J.M. (2004) Windows for sex-specific methylation marked by DNA methyltransferase expression profiles in mouse germ cells. Dev. Biol. 268, 403-415.
14. Xie, Z.H., Huang, Y.N., Chen, Z.X., Riggs, A.D., Ding, J.P., Gowher, H., Jeltsch, A., Sasaki, H., Hata, K. and Xu, G.L. (2006) Mutations in DNA methyltransferase DNMT3B in ICF syndrome affect its regulation by DNMT3L. Hum. Mol. Genet., 15, 1375-1385.
15. Bourc'his, D., Xu, G.L., Lin, C.S., Bollman, B. and Bestor, T.H. (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294, 2536-2539.
16. Kato, Y., Kaneda, M., Hata, K., Kumaki, K., Hisano, M., Kohara, Y., Okano, M., Li, E., Nozaki, M. and Sasaki, H. (2007) Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum. Mol. Genet., 16, 2272-2280.
17. Webster, K.E., O'Bryan, M.K., Fletcher, S., Crewther, P.E., Aapola, U., Craig, J., Harrison, D.K., Aung, H., Phatikanit, N., Lyle, R. et al. (2005) Meiotic and epigerietic defects in Dnmt3L-knockout mouse spermatogenesis. Proc. Natl Acad. Sci. USA, 102, 4068-4073.
18. Hata, K., Okano, M., Lei, H. and Li, E. (2002) Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development, 129, 1983-1993.
19. Hata, K., Kusumi, M., Yokomine, T., Li, E. and Sasald, H. (2006) Meiotic and epigenetic aberrations in Dnmt3L-deficient male germ cells. Mol. Reprod Dev., 73, 116-122.
20. Chedin, F., Lieber, M.R. and Hsieh, C.L. (2002) The DNA methyltransferase-like protein DNMT3L stimulates de novo methylation by Dnmt3a. Proc. Natl Acad. Sci. USA, 99, 16916-16921.
21. Suetake, I., Shmozaki, F., Miyagawa, J., Takeshima, H. and Tajima, S. (2004) DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction. J. Biol. Chem., 279, 27816-27823.
22. Gowher, H., Liebert, K., Hermann, A., Xu, G. and Jeltsch, A. (2005) Mechanism of stimulation of catalytic activity of Dnmt3A and Dnmt3B DNA-(cytosine-C5)-methyltransferases by Dnmt3L. J. Biol. Chem., 280, 13341-13348.
23. Chen, Z.X., Mann, J.R., Hsieh, C.L., Riggs, A.D. and Chedin, F. (2005) Physical and functional interactions between the human DNMT3L protein and members of the de novo methyltransferase family. J. Cell. Biochem., 95, 902-917.
24. Aapola, U., Maenpaa, K., Kaipia, A. and Peterson, P. (2004) Epigenetic modifications affect Dnmt3L expression. Biochem. J., 390, 705-713.
25. Weitzer, G. (2006) Embryonic stem cell-derived embryoid bodies: An in vitro model of eutherian pregastrulation development and early gastrulation. Handbook of Experimental Pharmacology, 21-51.
26. Leahy, A., Xiong, J.W., Kuhnert, F. and Stuhlmann, H. (1999) Use of developmental marker genes to define temporal and spatial patterns of differentiation during embryoid body formation. J. Exp. Zool., 294, 67-81.
27. Ehrlich, M. (2003) The ICF syndrome, a DNA methyltransferase 3B deficiency and immunodeficiency disease. Clin. Immunol., 109 17-28.
28. Ueda, Y., Okano, M., Williams, C., Chen, T., Georgopoulos, K. and Li, E. (2006) Roles for Dnmt3b in mammalian development: A mouse model for the ICF syndrome. Development, 133, 1183-1192.
29. Monk, M., Boubelik, M. and Lehnert, S. (1987) Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development, 99 371-382.
30. Kafri, T., Ariel, M., Brandeis, M., Shemer, R., Urven, L., McCarrey, J., Cedar, H. and Razin, A. (1992) Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev., 6, 705-714.
31. Mayer, W., Niveleau, A., Walter, J., Fundele, R. and Haaf, T. (2000) Demethylation of the zygotic paternal genome. Nature, 403, 501-502.
32. Oswald, J., Engemann, S., Lane, N., Mayer, W., Olek, A., Fundele, R., Dean, W., Reik, W. and Walter, J. (2000) Active demethylation of the paternal genome in the mouse zygote. Curr. Biol., 10, 475-478.
33. Santos, F., Hendrich, B., Reik, W. and Dean, W. (2002) Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol., 241, 172-182.
34. Li, J.Y., Pu, M.T., Hirasawa, R., Li, B.Z., Huang, Y.N., Zeng, R., Jing, N.H., Chen, T., Li, E., Sasaki, H. et al. (2007) Synergistic function of DNA methyltransferases Dnmt3a and Dnmt3b in the methylation of Oct4 and Nanog. Mol. Cell. Biol., 27, 8748-8759.
35. Fuks, F., Burgers, W.A., Godin, N., Kasai, M. and Kouzarides, T. (2001) Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. EMBO J., 20, 2536-2544.
36. Bachman, K.E., Rountree, M.R. and Baylin, S.B. (2001) Dnmt3a and Dmnt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J. Biol. Chem., 276, 32282-32287.
37. Aapola, U., Liiv, I. and Peterson, P. (2002) Imprinting regulator DNMT3L is a transcriptional repressor associated with histone deacetylase activity. Nucleic Acids Res., 30, 3602-3608.
38. Ooi, S.K., Qiu, C., Bernstein, E., Li, K., Jia, D., Yang, Z., Erdjument-Bromage, H., Tempst, P., Lin, S.P., Allis, C.D. et al. (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature, 448, 714-717.
39. Jia, D., Jurkowska, R.Z., Zhang, X., Jeltsch, A. and Cheng, X. (2007) Structure of Dmnt3a bound to Dmnt3L suggests a model for de novo DNA methylation. Nature, 449, 248-251.
40. Shovlin, T.C., Bourc'his, D., La Salle, S., O'Doherty, A., Trasler, J.M., Bestor, T.H. and Walsh, C.P. (2007) Sex-specific promoters regulate Dnmt3L expression in mouse germ cells. Hum. Reprod., 22, 457-467.
41. Linhart, H.G., Lin, H., Yamada, Y., Moran, E., Steine, E.J., Gokhale, S., Lo, G., Cantu, E., Ehrich, M., He, T. et al. (2007) Dnmt3b promotes tumorigenesis in vivo by gene-specific de novo methylation and transcriptional silencing. Genes Dev., 21, 3110-3122.
42. Gokul, G., Gautami, B., Malathi, S., Sowjanya, A.P., Poli, U.R., Jain, M., Ramakrishna, G. and Khosla, S. (2007) DNA methylation profile at the DNMT3L promoter: A potential biomarker for cervical cancer. Epigenetics, 2, 80-85.
43. Shirohzu, H., Kubota, T., Kumazawa, A., Sado, T., Chijiwa, T., Inagaki, K., Suetake, I., Tajima, S., Wakui, K., Miki, Y. et al. (2002) Three novel DNMT3B mutations in Japanese patients with ICF syndrome. Am. J. Med. Genet., 112, 31-37.
44. Ge, Y.Z., Pu, M.T., Gowher, H., Wu, H.P., Ding, J.P., Jeltsch, A. and Xu, G.L. (2004) Chromatin targeting of de novo DNA methyltransferases by the PWWP domain. J. Biol. Chem., 279, 25447-25454.
45. Hajkova, P., el-Maarri, O., Engemann, S., Oswald, J., Olek, A. and Walter, J. (2002) DNA-methylation analysis by the bisulfite-assisted genomic sequencing method. Methods Mol. Biol., 200, 143-154.
46. Chen, T., Ueda, Y., Dodge, J.E., Wang, Z. and Li, E. (2003) Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol. Cell. Biol., 23 5594-5605.
47. Metzger, JM., Lin, W.I. and Samuelson, L.C. (1994) Transition in cardiac contractile sensitivity to calcium during the in vitro differentiation of mouse embryonic stem cells. J. Cell Biol., 126, 701-711.
48. Bustin, S.A. (2002) Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): Trends and problems. J. Mol. Endocrinol. 29, 23-39.
49. Yu, Q., Thieu, V.T. and Kaplan, M.H. (2007) Stat4 limits DNA methyltransferase recruitment and DNA methylation of the IL-18Ralpha gene during Th1 differentiation. EMBO J., 26, 2052-2060.