De novo DNA methylation through the 5’-segment of the H19 ICR maintains its imprint during early embryogenesis

Development (Cambridge)

Volumn 142, Issue 22, 2015, Pages 3821-3832

  Matsuzaki, Hitomi ^a   Okamura, Eiichi ^a   Takahashi, Takuya ^a   Ushiki, Aki ^a   Nakamura, Toshinobu ^b   Nakano, Toru ^c   Hata, Kenichiro ^d   Fukamizu, Akiyoshi ^a   Tanimoto, Keiji ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

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

Author keywords

DNA methylation; Early embryogenesis; Genomic imprinting; Igf2 H19 locus

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 3; SMALL INTERFERING RNA; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA METHYLTRANSFERASE 3A; DNMT3L PROTEIN, MOUSE; H19 LONG NON-CODING RNA; IGF2 PROTEIN, MOUSE; LONG UNTRANSLATED RNA; PRIMER DNA; SOMATOMEDIN B;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; EMBRYO DEVELOPMENT; FOREBRAIN; IMMUNOHISTOCHEMISTRY; MESODERM; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; DNA METHYLATION; DNA SEQUENCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GENOME IMPRINTING; MALE; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; TRANSGENIC MOUSE;

ANIMALS; BASE SEQUENCE; BLOTTING, SOUTHERN; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA PRIMERS; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOMIC IMPRINTING; INSULIN-LIKE GROWTH FACTOR II; MALE; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, LONG NONCODING; SEQUENCE ANALYSIS, DNA;

EID: 84947483852     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.126003     Document Type: Article

References (47)

1. Arnaud, P., Hata, K., Kaneda, M., Li, E., Sasaki, H., Feil, R. and Kelsey, G. (2006). Stochastic imprinting in the progeny of Dnmt3L−/− females. Hum. Mol. Genet. 15, 589-598.
2. Bell, A. C. and Felsenfeld, G. (2000). Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405, 482-485.
3. Cheong, C. Y., Chng, K., Ng, S., Chew, S. B., Chan, L. and Ferguson-Smith, A. C. (2015). Germline and somatic imprinting in the nonhuman primate highlights species differences in oocyte methylation. Genome Res. 25, 611-623.
4. de Vries, W. N., Binns, L. T., Fancher, K. S., Dean, J., Moore, R., Kemler, R. and Knowles, B. B. (2000). Expression of Cre recombinase in mouse oocytes: a means to study maternal effect genes. Genesis 26, 110-112.
5. DeChiara, T. M., Robertson, E. J. and Efstratiadis, A. (1991). Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64, 849-859.
6. Dickson, J., Gowher, H., Strogantsev, R., Gaszner, M., Hair, A., Felsenfeld, G. and West, A. G. (2010). VEZF1 elements mediate protection from DNA methylation. PLoS Genet. 6, e1000804.
7. 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.
8. Ferguson-Smith, A. C. (2011). Genomic imprinting: the emergence of an epigenetic paradigm. Nat. Rev. Genet. 12, 565-575.
9. Gabory, A., Jammes, H. and Dandolo, L. (2010). The H19 locus: role of an imprinted non-coding RNA in growth and development. Bioessays 32, 473-480.
10. Gebert, C., Kunkel, D., Grinberg, A. and Pfeifer, K. (2010). H19 imprinting control region methylation requires an imprinted environment only in the male germ line. Mol. Cell. Biol. 30, 1108-1115.
11. Guenatri, M., Duffie, R., Iranzo, J., Fauque, P. and Bourc’his, D. (2013). Plasticity in Dnmt3L-dependent and -independent modes of de novo methylation in the developing mouse embryo. Development 140, 562-572.
12. Hammoud, S. S., Nix, D. A., Zhang, H., Purwar, J., Carrell, D. T. and Cairns, B. R. (2009). Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473-478.
13. Hark, A. T., Schoenherr, C. J., Katz, D. J., Ingram, R. S., Levorse, J. M. and Tilghman, S. M. (2000). CTCF mediates methylation-sensitive enhancerblocking activity at the H19/Igf2 locus. Nature 405, 486-489.
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.
15. Henckel, A., Nakabayashi, K., Sanz, L. A., Feil, R., Hata, K. and Arnaud, P. (2009). Histone methylation is mechanistically linked to DNA methylation at imprinting control regions in mammals. Hum. Mol. Genet. 18, 3375-3383.
16. Henckel, A., Chebli, K., Kota, S. K., Arnaud, P. and Feil, R. (2012). Transcription and histone methylation changes correlate with imprint acquisition in male germ cells. EMBO J. 31, 606-615.
17. 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.
18. Hu, Y.-G., Hirasawa, R., Hu, J.-L., Hata, K., Li, C.-L., Jin, Y., Chen, T., Li, E., Rigolet, M., Viegas-Pequignot, E. et al. (2008). Regulation of DNA methylation activity through Dnmt3L promoter methylation by Dnmt3 enzymes in embryonic development. Hum. Mol. Genet. 17, 2654-2664.
19. 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.
20. Kelsey, G. and Feil, R. (2013). New insights into establishment and maintenance of DNA methylation imprints in mammals. Philos. Trans. R. Soc. B Biol. Sci. 368, 20110336.
21. Kobayashi, H., Sakurai, T., Imai, M., Takahashi, N., Fukuda, A., Yayoi, O., Sato, S., Nakabayashi, K., Hata, K., Sotomaru, Y. et al. (2012). Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet. 8, e1002440.
22. Li, X., Ito, M., Zhou, F., Youngson, N., Zuo, X., Leder, P. and Ferguson-Smith, A. C. (2008). A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev. Cell 15, 547-557.
23. Ma, P., Lin, S., Bartolomei, M. S. and Schultz, R. M. (2010). Metastasis tumor antigen 2 (MTA2) is involved in proper imprinted expression of H19 and Peg3 during mouse preimplantation development. Biol. Reprod. 83, 1027-1035.
24. Matsuzaki, H., Okamura, E., Shimotsuma, M., Fukamizu, A. and Tanimoto, K. (2009). A randomly integrated transgenic H19 imprinting control region acquires methylation imprinting independently of its establishment in germ cells. Mol. Cell. Biol. 29, 4595-4603.
25. Matsuzaki, H., Okamura, E., Fukamizu, A. and Tanimoto, K. (2010). CTCF binding is not the epigenetic mark that establishes post-fertilization methylation imprinting in the transgenic H19 ICR. Hum. Mol. Genet. 19, 1190-1198.
26. Messerschmidt, D. M., de Vries, W., Ito, M., Solter, D., Ferguson-Smith, A. and Knowles, B. B. (2012). Trim28 is required for epigenetic stability during mouse oocyte to embryo transition. Science 335, 1499-1502.
27. Miller, D., Brinkworth, M. and Iles, D. (2010). Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 139, 287-301.
28. Nakamura, T., Arai, Y., Umehara, H., Masuhara, M., Kimura, T., Taniguchi, H., Sekimoto, T., Ikawa, M., Yoneda, Y., Okabe, M. et al. (2007). PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat. Cell Biol. 9, 64-71.
29. Nakamura, T., Liu, Y.-J., Nakashima, H., Umehara, H., Inoue, K., Matoba, S., Tachibana, M., Ogura, A., Shinkai, Y. and Nakano, T. (2012). PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 486, 415-419.
30. Okamura, E., Matsuzaki, H., Fukamizu, A. and Tanimoto, K. (2013a). The chicken HS4 insulator element does not protect the H19 ICR from differential DNA methylation in yeast artificial chromosome transgenic mouse. PLoS ONE 8, e73925.
31. Okamura, E., Matsuzaki, H., Sakaguchi, R., Takahashi, T., Fukamizu, A. and Tanimoto, K. (2013b). The H19 imprinting control region mediates preimplantation imprinted methylation of nearby sequences in yeast artificial chromosome transgenic mice. Mol. Cell. Biol. 33, 858-871.
32. 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.
33. Park, K.-Y., Sellars, E. A., Grinberg, A., Huang, S.-P. and Pfeifer, K. (2004). The H19 differentially methylated region marks the parental origin of a heterologous locus without gametic DNA methylation. Mol. Cell. Biol. 24, 3588-3595.
34. Puget, N., Hirasawa, R., Hu, N.-S. N., Laviolette-Malirat, N., Feil, R. and Khamlichi, A. A. (2015). Insertion of an imprinted insulator into the IgH locus reveals developmentally regulated, transcription-dependent control of V(D)J recombination. Mol. Cell. Biol. 35, 529-543.
35. Quenneville, S., Verde, G., Corsinotti, A., Kapopoulou, A., Jakobsson, J., Offner, S., Baglivo, I., Pedone, P. V., Grimaldi, G., Riccio, A. et al. (2011). In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Mol. Cell 44, 361-372.
36. Reese, K. J., Lin, S., Verona, R. I., Schultz, R. M. and Bartolomei, M. S. (2007). Maintenance of paternal methylation and repression of the imprinted H19 gene requires MBD3. PLoS Genet. 3, e137.
37. Sakaguchi, R., Okamura, E., Matsuzaki, H., Fukamizu, A. and Tanimoto, K. (2013). Sox-Oct motifs contribute to maintenance of the unmethylated H19 ICR in YAC transgenic mice. Hum. Mol. Genet. 22, 4627-4637.
38. Schoenherr, C. J., Levorse, J. M. and Tilghman, S. M. (2003). CTCF maintains differential methylation at the Igf2/H19 locus. Nat. Genet. 33, 66-69.
39. Smallwood, S. A., Tomizawa, S.-i., Krueger, F., Ruf, N., Carli, N., Segonds-Pichon, A., Sato, S., Hata, K., Andrews, S. R. and Kelsey, G. (2011). Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat. Genet. 43, 811-814.
40. Srivastava, M., Hsieh, S., Grinberg, A., Williams-Simons, L., Huang, S. P. and Pfeifer, K. (2000). H19 and Igf2 monoallelic expression is regulated in two distinct ways by a shared cis acting regulatory region upstream of H19. Genes Dev. 14, 1186-1195.
41. Szabo, P. E., Tang, S. H., Reed, M. R., Silva, F. J., Tsark, W. M. and Mann, J. R. (2002). The chicken beta-globin insulator element conveys chromatin boundary activity but not imprinting at the mouse Igf2/H19 domain. Development 129, 897-904.
42. Tanimoto, K., Shimotsuma, M., Matsuzaki, H., Omori, A., Bungert, J., Engel, J. D. and Fukamizu, A. (2005). Genomic imprinting recapitulated in the human beta-globin locus. Proc. Natl. Acad. Sci. USA 102, 10250-10255.
43. Tanimoto, K., Sugiura, A., Kanafusa, S., Saito, T., Masui, N., Yanai, K. and Fukamizu, A. (2008). A single nucleotide mutation in the mouse renin promoter disrupts blood pressure regulation. J. Clin. Invest. 118, 1006-1016.
44. Tomizawa, S.-I. and Sasaki, H. (2012). Genomic imprinting and its relevance to congenital disease, infertility, molar pregnancy and induced pluripotent stem cell. J. Hum. Genet. 57, 84-91.
45. 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.
46. West, A. G., Huang, S., Gaszner, M., Litt, M. D. and Felsenfeld, G. (2004). Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Mol. Cell 16, 453-463.
47. Zimmerman, D. L., Boddy, C. S. and Schoenherr, C. S. (2013). Oct4/Sox2 binding sites contribute to maintaining hypomethylation of the maternal igf2/h19 imprinting control region. PLoS ONE 8, e81962.