Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes

Development

Volumn 138, Issue 5, 2011, Pages 811-820

  Tomizawa, Shin Ichi ^a,b,c   Kobayashi, Hisato ^a,b,g   Watanabe, Toshiaki ^a,b,h   Andrews, Simon ^c   Hata, Kenichiro ^d   Kelsey, Gavin ^c,e   Sasaki, Hiroyuki ^a,b,f  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c BABRAHAM INSTITUTE   (United Kingdom)

^d NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f KYUSHU UNIVERSITY   (Japan)

^g TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^h YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Differentially methylated region (DMR); DNA methylation; Genomic imprinting; Mouse; Non CpG methylation; Oocyte; Sperm

Indexed keywords

ALLELE; ANIMAL CELL; ARTICLE; BLASTOCYST; CONTROLLED STUDY; CPG ISLAND; DIFFERENTIALLY METHYLATED REGION; EMBRYO; EMBRYONIC STEM CELL; EPIGENETICS; FEMALE; GENOME IMPRINTING; GERM LINE; GERMLINE MICRONUCLEUS; MALE; MAMMAL; METHYLATION; MOLECULAR DYNAMICS; MOUSE; MOUSE EMBRYO; NONHUMAN; ONTOGENY; OOCYTE; OOCYTE DEVELOPMENT; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; SPERM;

ANIMALS; CPG ISLANDS; DNA METHYLATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; GENOME; GENOMIC IMPRINTING; MALE; MICE; OOCYTES; SPERMATOZOA;

MAMMALIA; MUS;

EID: 79951529848     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.061416     Document Type: Article

References (52)

1. Aoki, A., Suetake, I., Miyagawa, J., Fujio, T., Chijiwa, T., Sasaki, H. and Tajima, S. (2001). Enzymatic properties of de novo-type mouse DNA (cytosine-5) methyltransferases. Nucleic Acids Res. 29, 3506-3512. (Pubitemid 32898764)
2. Blackledge, N. P., Zhou, J. C., Tolstorukov, M. Y., Farcas, A. M., Park, P. J. and Klose, R. J. (2010). CpG islands recruit a histone H3 lysine 36 demethylase. Mol. Cell 38, 179-190.
3. Bourc'his, D. and Bestor, T. H. (2004). Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96-99.
4. Brandeis, M., Kafri, T., Ariel, M., Chaillet, J. R., McCarrey, J., Razin, A. and Cedar, H. (1993). The ontogeny of allele-specific methylation associated with imprinted genes in the mouse. EMBO J. 12, 3669-3677. (Pubitemid 23256454)
5. Chotalia, M., Smallwood, S. A., Ruf, N., Dawson, C., Lucifero, D., Frontera, M., James, K., Dean, W. and Kelsey, G. (2009). Transcription is required for establishment of germline methylation marks at imprinted genes. Genes Dev. 23, 105-117.
6. Ciccone, D. N., Su, H., Hevi, S., Gay, F., Lei, H., Bajko, J., Xu, G., Li, E. and Chen, T. (2009). KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 461, 415-418.
7. Crooks, G. E., Hon, G., Chandonia, J. M. and Brenner, S. E. (2004). WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190.
8. Dhayalan, A., Rajavelu, A., Rathert, P., Tamas, R., Jurkowska, R. Z., Ragozin, S. and Jeltsch, A. (2010). The Dnmt3a PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation. J. Biol. Chem. 285, 26114-26120.
9. Ferguson-Smith, A. C. and Greally, J. M. (2007). Epigenetics: perceptive enzymes. Nature 449, 148-149.
10. Ferguson-Smith, A. C., Sasaki, H., Cattanach, B. M. and Surani, M. A. (1993). Parental-origin-specific epigenetic modification of the mouse H19 gene. Nature 362, 751-755.
11. 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. (Pubitemid 35266120)
12. Greally, J. M. (2002). Short interspersed transposable elements (SINEs) are excluded from imprinted regions in the human genome. Proc. Natl. Acad. Sci. USA 99, 327-332.
13. Haines, T. R., Rodenhiser, D. I. and Ainsworth, P. J. (2001). Allele-specific non-CpG methylation of the Nf1 gene during early mouse development. Dev. Biol. 240, 585-598. (Pubitemid 34056513)
14. 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. (Pubitemid 34874213)
15. Hetzl, J., Foerster, A. M., Raidl, G. and Mittelsten Scheid, O. (2007). CyMATE: a new tool for methylation analysis of plant genomic DNA after bisulphite sequencing. Plant J. 51, 526-536. (Pubitemid 47106545)
16. Hirasawa, R., Chiba, H., Kaneda, M., Tajima, S., Li, E., Jaenisch, R. and Sasaki, H. (2008). Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev. 22, 1607-1616. (Pubitemid 351846841)
17. 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.
18. Hutter, B., Helms, V. and Paulsen, M. (2006). Tandem repeats in the CpG islands of imprinted genes. Genomics 88, 323-332. (Pubitemid 44294744)
19. Illingworth, R. S., Gruenewald-Schneider, U., Webb, S., Kerr, A. R., James, K. D., Turner, D. J., Smith, C., Harrison, D. J., Andrews, R. and Bird, A. P. (2010). Orphan CpG islands identify numerous conserved promoters in the mammalian genome. PLoS Genet. 6, e1001134.
20. Imamura, T., Kerjean, A., Heams, T., Kupiec, J. J., Thenevin, C. and Paldi, A. (2005). Dynamic CpG and non-CpG methylation of the Peg1/Mest gene in the mouse oocyte and preimplantation embryo. J. Biol. Chem. 280, 20171-20175. (Pubitemid 41379549)
21. Jia, D., Jurkowska, R. Z., Zhang, X., Jeltsch, A. and Cheng, X. (2007). Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449, 248-251. (Pubitemid 47402375)
22. 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. (Pubitemid 38843304)
23. Kaneda, M., Hirasawa, R., Chiba, H., Okano, M., Li, E. and Sasaki, H. (2010). Genetic evidence for Dnmt3a-dependent imprinting during oocyte growth obtained by conditional knockout with Zp3-Cre and complete exclusion of Dnmt3b by chimera formation. Genes Cells 15, 169-179.
24. 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. (Pubitemid 47423893)
25. Ke, X., Thomas, N. S., Robinson, D. O. and Collins, A. (2002). The distinguishing sequence characteristics of mouse imprinted genes. Mamm. Genome 13, 639-645. (Pubitemid 35398940)
26. 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.
27. Kobayashi, H., Yamada, K., Morita, S., Hiura, H., Fukuda, A., Kagami, M., Ogata, T., Hata, K., Sotomaru, Y. and Kono, T. (2009). Identification of the mouse paternally expressed imprinted gene Zdbf2 on chromosome 1 and its imprinted human homolog ZDBF2 on chromosome 2. Genomics 93, 461-472.
28. 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. (Pubitemid 28158987)
29. 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.
30. Lindroth, A. M., Park, Y. J., McLean, C. M., Dokshin, G. A., Persson, J. M., Herman, H., Pasini, D., Miro, X., Donohoe, M. E., Lee, J. T. et al. (2008). Antagonism between DNA and H3K27 methylation at the imprinted Rasgrf1 locus. PLoS Genet. 4, e1000145.
31. Lister, R., Pelizzola, M., Dowen, R. H., Hawkins, R. D., Hon, G., Tonti-Filippini, J., Nery, J. R., Lee, L., Ye, Z., Ngo, Q. M. et al. (2009). Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462, 315-322.
32. Morgan, H. D., Santos, F., Green, K., Dean, W. and Reik, W. (2005). Epigenetic reprogramming in mammals. Hum. Mol. Genet. 14 Spec No 1, R47-R58. (Pubitemid 40542620)
33. Neumann, B., Kubicka, P. and Barlow, D. P. (1995). Characteristics of imprinted genes. Nat. Genet. 9, 12-13.
34. 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. (Pubitemid 28309328)
35. 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. (Pubitemid 47236857)
36. Ramsahoye, B. H., Biniszkiewicz, D., Lyko, F., Clark, V., Bird, A. P. and Jaenisch, R. (2000). Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc. Natl. Acad. Sci. USA 97, 5237-5242. (Pubitemid 30313702)
37. Reik, W. and Walter, J. (2001). Genomic imprinting: parental influence on the genome. Nat. Rev. Genet. 2, 21-32. (Pubitemid 33674766)
38. Reik, W., Dean, W. and Walter, J. (2001). Epigenetic reprogramming in mammalian development. Science 293, 1089-1093. (Pubitemid 32758081)
39. Reinhart, B., Paoloni-Giacobino, A. and Chaillet, J. R. (2006). Specific differentially methylated domain sequences direct the maintenance of methylation at imprinted genes. Mol. Cell. Biol. 26, 8347-8356.
40. Rohde, C., Zhang, Y., Reinhardt, R. and Jeltsch, A. (2010). BISMA-fast and accurate bisulfite sequencing data analysis of individual clones from unique and repetitive sequences. BMC Bioinformatics 11, 230.
41. Sasaki, H. and Matsui, Y. (2008). Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat. Rev. Genet. 9, 129-140.
42. Shiura, H., Nakamura, K., Hikichi, T., Hino, T., Oda, K., Suzuki-Migishima, R., Kohda, T., Kaneko-ishino, T. and Ishino, F. (2009). Paternal deletion of Meg1/Grb10 DMR causes maternalization of the Meg1/Grb10 cluster in mouse proximal chromosome 11 leading to severe pre- and postnatal growth retardation. Hum. Mol. Genet. 18, 1424-1438.
43. Thomson, J. P., Skene, P. J., Selfridge, J., Clouaire, T., Guy, J., Webb, S., Kerr, A. R., Deaton, A., Andrews, R., James, K. D. et al. (2010). CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464, 1082-1086.
44. 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. (Pubitemid 29019650)
45. Tremblay, K. D., Saam, J. R., Ingram, R. S., Tilghman, S. M. and Bartolomei, M. S. (1995). A paternal-specific methylation imprint marks the alleles of the mouse H19 gene. Nat. Genet. 9, 407-413.
46. Tremblay, K. D., Duran, K. L. and Bartolomei, M. S. (1997). A 5′ 2-kilobase-pair region of the imprinted mouse H19 gene exhibits exclusive paternal methylation throughout development. Mol. Cell. Biol. 17, 4322-4329. (Pubitemid 27318108)
47. Vassena, R., Dee Schramm, R. and Latham, K. E. (2005). Species-dependent expression patterns of DNA methyltransferase genes in mammalian oocytes and preimplantation embryos. Mol. Reprod. Dev. 72, 430-436.
48. Walter, J., Hutter, B., Khare, T. and Paulsen, M. (2006). Repetitive elements in imprinted genes. Cytogenet. Genome Res. 113, 109-115.
49. Wienholz, B. L., Kareta, M. S., Moarefi, A. H., Gordon, C. A., Ginno, P. A. and Chedin, F. (2010). DNMT3L modulates significant and distinct flanking sequence preference for DNA methylation by DNMT3A and DNMT3B in vivo. PLoS Genet. 6, e1001106.
50. 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. (Pubitemid 39014110)
51. 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. (Pubitemid 27458963)
52. Yoon, B. J., Herman, H., Sikora, A., Smith, L. T., Plass, C. and Soloway, P. D. (2002). Regulation of DNA methylation of Rasgrf1. Nat. Genet. 30, 92-96.