Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse

Human Molecular Genetics

Volumn 16, Issue 19, 2007, Pages 2272-2280

  Kato, Yuzuru ^a   Kaneda, Masahiro ^a,f   Hata, Kenichiro ^a   Kumaki, Kenji ^a   Hisano, Mizue ^b   Kohara, Yuji ^a,c   Okano, Masaki ^d   Li, En ^e   Nozaki, Masami ^b   Sasaki, Hiroyuki ^a  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF GENETICS   (Japan)

^d RIKEN Center for Biosystems Dynamics Research   (Japan)

^e NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DLK1 PROTEIN; DNA; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 3 LIKE PROTEIN; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; GTL2 PROTEIN; ONCOPROTEIN; PROTEIN DERIVATIVE; RASGRF1 PROTEIN; RNA H19; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DNA METHYLATION; DNA MODIFICATION; ENZYME SPECIFICITY; EPIGENETICS; FETUS; FETUS DEVELOPMENT; GERM CELL; GERM LINE; IN VIVO STUDY; INTERSPERSED REPEAT; KNOCKOUT MOUSE; MALE; MOUSE; NEWBORN; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SPERMATOGONIUM; TESTIS DEVELOPMENT;

ANIMALS; ANIMALS, NEWBORN; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA, SATELLITE; FEMALE; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; INTERSPERSED REPETITIVE SEQUENCES; MALE; REPETITIVE SEQUENCES, NUCLEIC ACID; SPERMATOGENESIS;

INTRACISTERNAL A-PARTICLES; MUS;

EID: 34548705374     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddm179     Document Type: Article

References (50)

1. Reik, W., Dean, W. and Walter, J. (2001) Epigenetic reprogramming in mammalian development. Science, 293, 1089-1093.
2. Bird, A. (2002) DNA methylation patterns and epigenetic memory. Genes Dev., 16, 6-21.
3. Gruenbaum, Y., Cedar, H. and Razin, A. (1982) Substrate and sequence specificity of a eukaryotic DNA methylase. Nature, 295, 620-622.
4. Bestor, T.H. and Ingram, V.M. (1983) Two DNA methyltransferases from murine erythroleukemia cells: Purification, sequence specificity, and mode of interaction with DNA. Proc. Natl Acad. Sci. USA, 80, 5559-5563.
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. Li, E., Bestor, T.H. and Jaenisch, R. (1992) Targeted Mutation of the DNA methyltransferase gene results in embryonic lethality. Cell, 69, 915-926.
7. 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.
8. Li, E., Beard, C. and Jaenisch, R. (1993) Role for DNA methylation in genomic imprinting. Nature, 366, 362-365.
9. Kaneda, M., Okano, M., Hata, K., Sado, T., Tsujimoto, N., Li, E. and Sasaki, H. (2004) Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature, 429, 900-903.
10. Wutz, A., Smrzka, O.W., Schweifer, N., Schellander, K., Wagner, E.F. and Barlow, D.P. (1997) Imprinted expression of the Igf2r gene depends on an intronic CpG island. Nature, 389, 745-749.
11. Thorvaldsen, J.L., Duran, K.L. and Bartolomei, M.S. (1998) Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev., 12, 3693-3702.
12. Fitzpatrick, G.V., Soloway, P.D. and Higgins, M.J. (2002) Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat. Genet., 32, 426-431.
13. Lin, S.-P., Youngson, N., Takada, S., Seitz, H., Reik, W., Paulsen, M., Cavaille, J. and Ferguson-Smith, A.C. (2003) Asymmetric regulation of imprinting on the maternal and paternal chromosomes at the Dlk1-Gtl2 imprinted cluster on mouse chromosome 12. Nat. Genet., 35 97-102.
14. Williamson, C.M., Ball, S.T., Nottingham, W.T., Skinner, J.A., Plagge, A., Turner, M.D., Powles, N., Hough, T., Papworth, D., Fraser, W.D. et al. (2004) A cis-acting control region is required exclusively for the tissue-specific imprinting of Gnas. Nat. Genet. 36, 894-899.
15. Liu, J., Chen, M., Deng, C., Bourc'his, D., Nealon, J.G., Erlichman, B., Bestor, T.H. and Weinstein, L.S. (2005) Identification of the control region for tissue-specific imprinting of the stimulatory G protein α-subunit. Proc. Natl Acad. Sci. USA, 102, 5513-5518.
16. Lee, J., Inoue, K., Ono, R., Ogonuki, N., Kohda, T., Kaneko-Ishino, T., Ogura, A. and Ishino, F. (2002) Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development, 129, 1807-1817.
17. Hajkova, P., Erhardt, S., Lane, N., Haaf, T., El-Maarri, O., Reik, W., Walter, J. and Surani, M.A. (2002) Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev., 117, 15-23.
18. Li, J.-Y., Lees-Murdock, D.J., Xu, G.-L. and Walsh, C.P. (2004) Timing of establishment of paternal methylation imprints in the mouse. Genomics, 84, 952-960.
19. Lucifero, D., Mertineit, C., Clarke, H.J., Bestor, T.H. and Trasler, J.M. (2002) Methylation dynamics of imprinted genes in mouse germ cells. Genomics, 79, 530-538.
20. Lucifero, D., Mann, M.R.W., Bartolomei, M.S. and Trasler, J.M. (2004) Gene-specific timing and epigenetic memory in oocyte imprinting. Hum. Mol. Genet., 13, 839-849.
21. Hiura, H., Obata, Y., Komiyama, J., Shirai, M. and Kono, T. (2006) Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells, 11, 353-361.
22. Davis, T.L., Trasler, J.M., Moss, S.B., Yang, G.J. and Bartolomei, M.S. (1999) Acquisition of the H19 methylation imprint occurs differentially on the parental alleles during spermatogenesis. Genomics, 58, 18-28.
23. Davis, T.L., Yang, G.J., McCarrey, J.R. and Bartolomei, M.S. (2000) The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum. Mol. Genet., 9, 2885-2894.
24. Ueda, T., Abe, K., Miura, A., Yuzuriha, M., Zubair, M., Noguchi, M., Niwa, K., Kawase, Y., Kono, T., Matsuda, Y. et al. (2000) The paternal methylation imprint of the mouse H19 locus is acquired in the gonocyte stage during foetal testis development. Genes Cells, 5, 649-659.
25. 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.
26. 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.
27. Bourc'his, D. and Bestor, T.H. (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature, 431, 96-99.
28. Webster, K., O'Bryan, M.K., Fletcher, S., Crewther, P.E., Aapola, U., Craig, J., Harrison, D.K., Aung, H., Phutikanit, N., Lyle, R. et al. (2005) Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc. Natl Acad. Sci. USA, 102, 4068-4073.
29. Lees-Murdock, D.J., De Felici, M. and Walsh, C.P. (2003) Methylation dynamics of repetitive DNA elements in the mouse germ cell lineage. Genomics, 82, 230-237.
30. Hata, K., Kusumi, M., Yokomine, T., Li, E. and Sasaki, H. (2006) Meiotic and epigenetic aberrations in Dnmt3L-deficient male germ cells. Mol. Reprod. Dev., 73, 116-122.
31. 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.
32. 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.
33. Lees-Murdock, D.J., Shovlin, T.C., Gardiner, T., De Felici, M. and Walsh, C.P. (2005) DNA methyltransferase expression in the mouse germ line during periods of de novo methylation. Dev. Dyn., 232, 992-1002.
34. 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.
35. Sakai, Y., Suetake, I., Shinozaki, F., Yamashina, S. and Tajima, S. (2004) Co-expression of de novo DNA methyltransferases Dnmt3a2 and Dnmt3L in gonocytes of mouse embryos. Gene Exp. Patterns, 5, 231-237.
36. Chedin, F., Lieber, M.R. and Hsieh, L. (2002) The DNA methyltransferase-like protein DNMT3L stimulates de novo methylation by Dnmt3a. Proc. Natl Acad. Sci. USA, 99, 16916-16921.
37. Suetake, I., Shinozaki, 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.
38. 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.
39. Kareta, M.S., Botello, Z.M., Ennis, J.J., Chou, C. and Chedin, F. (2006) Reconstitution and mechanism of the stimulation of de novo methylation by human DNMT3L. J. Biol. Chem., 281, 25893-25902.
40. - females. Hum. Mol. Genet., 15, 589-598.
41. Koide, T., Moriwaki, K., Uchida, K., Mita, A., Sagai, T., Yonekawa, H., Katoh, H., Miyashita, N., Tsuchiya, K., Nielsen, T.J. et al. (1998) A new inbred strain JF1 established from Japanese fancy mouse carrying the classic piebald allele. Mamm. Genome, 9, 15-19.
42. Dodge, J.E., Okano, M., Dick, F., Tsujimoto, N., Chen, T., Wang, S., Ueda, Y., Dyson, N. and Li, E. (2005) Inactivation of Dnmt3b in mouse embryonic fibroblasts results in DNA hypomethylation, chromosomal instability, and spontaneous immortalization. J. Biol. Chem., 280, 17986-17991.
43. Lomeli, H., Ramos-Mejia, V., Gertsenstein, M., Lobe, C.G. and Nagy, A. (2000) Targeted insertion of Cre recombinase into the TNAP gene: excision in primordial gem cells. Genesis, 26, 116-117.
44. De Felici, M. and Mclaren, A. (1982) Isolation of mouse primordial germ cells. Exp. Cell Res., 142, 476-482.
45. Enders, G.C. and May, J.J., II (1994) Developmentally regulated expression of a mouse germ cell nuclear antigen examined from embryonic day 11 to adult in male and female mice. Dev. Biol., 163, 331-340.
46. Grabske, R.J., Lake, S., Gledhill, B.L. and Meistrich, M.L. (1975) Centrifugal elutriation: Separation of spermatogenic cells on the basis of sedimentation velocity. J. Cell. Physiol., 86, 177-190.
47. Kobayashi, H., Suda, C., Abe, T., Kohara, Y., Ikemura, T. and Sasaki, H. (2006) Bisulfite sequencing and dinucleotide content analysis of 15 imprinted mouse differentially methylated regions (DMRs): Paternally methylated DMRs contain less CpGs than maternally methylated DMRs. Cytogenet. Genome Res., 113, 130-137.
48. Vassetzky, N.S., Ten, O.A. and Kramerov, D.A. (2003) B1 and related SINEs in mammalian genomes. Gene, 319, 149-160.
49. Lehnertz, B., Ueda, Y., Derijck, A.A.H.A., Braunschweig, U., Perez-Burgos, L., Kubicek, S., Chen, T., Li, E., Jenuwein, T. and Peters, A.H.F.M. (2003) Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol., 13, 1192-1200.
50. Lane, N., Dean, W., Erhardt, S., Hajkova, P., Surani, A., Walter, J. and Reik, W. (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35, 88-93.