G9a Histone Methyltransferase Contributes to Imprinting in the Mouse Placenta

REFERENCES

• Arima, T., K. Hata, S. Tanaka, M. Kusumi, E. Li, K. Kato, K. Shiota, H. Sasaki, and N. Wake. 2006. Loss of maternal imprint in Dnmt3Lmat−/− mice leads to a differentiation defect in the extraembryonic tissue. Dev. Biol. 297:361–373.
   PubMedGoogle Scholar
• Arnaud, P., K. Hata, M. Kaneda, E. Li, H. Sasaki, R. Feil, and G. Kelsey. 2006. Stochastic imprinting in the progeny of Dnmt3L−/− females. Hum. Mol. Genet. 15:589–598.
   PubMedGoogle Scholar
• Bourc'his, D., G. L. Xu, C. S. Lin, B. Bolman, and T. H. Bestor. 2001. Dnmt3L and the establishment of maternal genomic imprints. Science 294:2536–2539.
   PubMed Web of Science ®Google Scholar
• Csankovszki, G., A. Nagy, and R. Jaenisch. 2001. Synergism of Xist RNA, DNA methylation, and histone hypoacetylation in maintaining X chromosome inactivation. J. Cell Biol. 153:773–784.
   PubMed Web of Science ®Google Scholar
• Dean, W., L. Bowden, A. Aitchison, J. Klose, T. Moore, J. J. Meneses, W. Reik, and R. Feil. 1998. Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: association with aberrant phenotypes. Development 125:2273–2282.
   PubMed Web of Science ®Google Scholar
• Delaval, K., J. Govin, F. Cerqueira, S. Rousseaux, S. Khochbin, and R. Feil. 2007. Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO J. 26:720–729.
   PubMed Web of Science ®Google Scholar
• Delaval, K., and R. Feil. 2004. Epigenetic regulation of mammalian genomic imprinting. Curr. Opin. Genet. Dev. 14:188–195.
   PubMed Web of Science ®Google Scholar
• Duan, Z., A. Zarebski, D. Montoya-Durango, H. L. Grimes, and M. Horwitz. 2005. Gfl1 coordinates epigenetic repression of the P21Cip/WAF1 by recruitment of histone lysine methyltransferase G9a and histone deacetylase 1. Mol. Cell. Biol. 25:10338–10351.
   PubMed Web of Science ®Google Scholar
• Edwards, C. A., and A. C. Ferguson-Smith. 2007. Mechanisms regulating imprinted genes in clusters. Curr. Opin. Cell Biol. 19:1–9.
   Google Scholar
• Estève, P. O., H. G. Chin, A. Smallwood, G. R. Feehery, O. Gangisetty, A. R. Karpf, M. F. Carey, and S. Pradhan. 2006. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev. 20:3089–3103.
   PubMed Web of Science ®Google Scholar
• Feil, R., J. Walter, N. D. Allen, and W. Reik. 1994. Developmental control of allelic methylation in the imprinted mouse Igf2 and H19 genes. Development 120:2933–2943.
   PubMed Web of Science ®Google Scholar
• Feldman, N., A. Gerson, J. Fang, E. li, Y. Zhang, Y. Shinkai, H. Cedar, and Y. Bergman. 2006. G9A-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat. Cell Biol. 8:188–194.
   PubMed Web of Science ®Google Scholar
• Fitzpatrick, G. V., P. D. Soloway, and M. J. Higgins. 2002. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat. Genet. 32:426–431.
   PubMed Web of Science ®Google Scholar
• Fitzpatrick, G. V., E. M. Pugacheva, J.-Y. Shin, Z. Abdullaev, Y. Yang, K. Khatod, V. V. Lobanenkov, and M. J. Higgins. 2007. Allele-specific binding of CTCF to the multipartite imprinting control region KvDMR1. Mol. Cell. Biol. 27:2636–2647.
   PubMed Web of Science ®Google Scholar
• Hata, K., M. Okano, H. Lei, and E. Li. 2002. Dnmt3L cooperates with the Dnmt3 family of de novo methyltransferases to establish maternal imprints in mice. Development 129:1983–1993.
   PubMed Web of Science ®Google Scholar
• Hatada, I., K. Kitagawa, T. Yamaoka, X. Wang, Y. Arai, K. Hashido, S. Ohishi, J. Masuda, J. Ogata, and T. Mukai. 1995. Allele-specific methylation and expression of an imprinted U2af1-rs1 (SP2) gene. Nucleic Acids Res. 23:36–41.
   PubMedGoogle Scholar
• Howell, C. Y., T. H. Bestor, F. Ding, K. E. Latham, C. Mertineit, J. M. Trasler, and J. R. Chaillet. 2001. Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104:829–838.
   PubMed Web of Science ®Google Scholar
• Jenuwein, T. 2006. The epigenetic magic of histone lysine methylation. FEBS J. 273:3121–3135.
   PubMed Web of Science ®Google Scholar
• Kanduri, C., G. Fitzpatrick, R. Mukhopadhyay, M. Kanduri, V. Lobanenkov, and R. Ohlsson. 2002. A differentially methylated imprinting control region within the Kcnq1 locus harbors a methylation-sensitive chromatin insulator. J. Biol. Chem. 277:18106–18110.
   PubMedGoogle Scholar
• Kaneda, M., M. Okano, K. Hata, T. Sado, N. Tsujimoro, E. Li, and H. Sasaki. 2004. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429:900–903.
   PubMed Web of Science ®Google Scholar
• Kent, J. W. 2002. BLAT: the BLAST-like alignment tool. Genome Res. 12:656–664.
   PubMed Web of Science ®Google Scholar
• Kent, J. W., C. W. Sugnet, T. S. Furey, K. M. Roskin, T. H. Pringle, A. M. Zahler, and D. Haussler. 2002. The Human Genome Browser at UCSC. Genome Res. 12:996–1006.
   PubMed Web of Science ®Google Scholar
• Kubicek, S., R. J. O'Sullivan, E. M. August, E. R. Hickey, Q. Zhang, M. L. Teodoro, S. Rea, K. Mechtler, J. A. Kowalski, C. A. Homon, T. A. Kelly, and T. Jenuwein. 2007. Reversal of H3K9me2 by a small-molecule inhibitor for the G9a histone methyltransferase. Mol. Cell 25:473–481.
   PubMed Web of Science ®Google Scholar
• Lehnertz, B., Y. Ueda, A. A. Derijck, U. Braunschweig, L. Perez-Burgos, S. Kubicek, T. Chen, E. Li, T. Jenuwein, and A. H. Peters. 2003. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 13:1192–1200.
   PubMed Web of Science ®Google Scholar
• Lewis, A., K. Mitsuya, D. Umlauf, P. Smith, W. Dean, J. Walter, M. Higgins, R. Feil, and W. Reik. 2004. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat. Genet. 36:1291–1295.
   PubMed Web of Science ®Google Scholar
• Lewis, A., and W. Reik. 2006. How imprinting centres work. Cytogenet. Genome Res. 113:81–89.
   PubMed Web of Science ®Google Scholar
• Lewis, A., K. Green, C. Dawson, L. Redrup, K. D. Huyn, J. T. Lee, M. Hemberger, and W. Reik. 2006. Epigenetic dynamics of the Kcnq1 domain in the early embryo. Development 133:4203–4210.
   PubMedGoogle Scholar
• Li, E., C. Beard, and R. Jaenisch. 1993. Role of DNA methylation in genomic imprinting. Nature 366:362–365.
   PubMed Web of Science ®Google Scholar
• Li, H., T. Rauch, Z. X. Chen, P. E. Szabo, A. D. Riggs, and G. P. Pfeifer. 2006. The histone methyltransferase SETDB1 and the DNA methyltransferase DNMT3A interact directly and localize to promoters silenced in cancer cells. J. Biol. Chem. 281:19489–19500.
   PubMed Web of Science ®Google Scholar
• Mager, J., N. D. Montgomery, F. P. de Villena, and T. Magnuson. 2003. Genome imprinting regulated by the mouse Polycomb group protein Eed. Nat. Genet. 33:502–507.
   PubMed Web of Science ®Google Scholar
• Mancini-Dinardo, D., S. J. Steele, J. M. Levorse, R. S. Ingram, and S. M. Tilghman. 2006. Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes. Genes Dev. 20:1268–1282.
   PubMed Web of Science ®Google Scholar
• Mann, M. R., S. S. Lee, A. S. Doherty, R. I. Verona, L. D. Nolen, R. M. Schultz, and M. S. Bartolomei. 2004. Selective loss of imprinting in the placenta following preimplantation development in culture. Development 131:3727–3735.
   PubMed Web of Science ®Google Scholar
• Morison, I. M., J. P. Ramsay, and H. G. Spencer. 2005. A census of mammalian imprinting. Trends Genet. 21:457–465.
   PubMed Web of Science ®Google Scholar
• Neumann, B., and D. P. Barlow. 1996. Multiple roles for DNA methylation in gametic imprinting. Curr. Opin. Genet. Dev. 6:159–163.
   PubMedGoogle Scholar
• Ogawa, H., K. Ishiguro, S. Gaubatz, D. M. Livingston, and Y. Nakatani. 2002. A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in G0 cells. Science 296:1132–1136.
   PubMed Web of Science ®Google Scholar
• Ohhata, T., M. Tachibana, M. Tada, T. Tada, H. Sasaki, Y. Shinkai, and T. Sado. 2004. X-inactivation is stably maintained in mouse embryos deficient for histone methyl transferase G9a. Genesis 40:151–156.
   PubMedGoogle Scholar
• Okamoto, I., and E. Heard. 2006. The dynamics of imprinted X inactivation during preimplantation development in mice. Cytogenet. Genome Res. 113:318–324.
   PubMedGoogle Scholar
• Paulsen, M., K. R. Davies, L. M. Bowden, A. J. Villar, O. Franck, M. Fuermann, W. L. Dean, T. F. Moore, N. Rodrigues, K. E. Davies, R. J. Hu, A. P. Feinberg, E. R. Maher, W. Reik, and J. Walter. 1998. Syntenic organisaton of the mouse distal chromosome 7 imprinting cluster and the Beckwith-Wiedemann syndrome region in chromosome 11p15.5. Hum. Mol. Genet. 7:1149–1159.
   PubMedGoogle Scholar
• Peters, A. H., S. Kubicek, K. Mechter, R. J. O'Sullivan, A. A. Derijck, L. Perez-Burgos, A. Kohlmaier, S. Opravil, M. Tachibana, Y. Shinkai, J. H. Martens, and T. Jenuwein. 2003. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 12:1577–1589.
   PubMed Web of Science ®Google Scholar
• Regda, K., M. A. Sloane, R. Huang, F. M. Pauler, K. E. Warczok, B. Melikant, M. Radolf, J. H. Martens, G. Schotta, T. Jenuwein, and D. P. Barlow. 2007. Active and repressive chromatin are interspersed without spreading in an imprinted gene cluster in the mammalian genome. Mol. Cell 27:353–366.
   PubMedGoogle Scholar
• Rice, J. C., S. D. Briggs, B. Ueberheide, C. M. Barber, J. Shabanowitz, D. F. Hunt, Y. Shinkai, and C. D. Allis. 2003. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol. Cell 12:1591–1598.
   PubMed Web of Science ®Google Scholar
• Rivera, R. M., P. Stein, J. R. Weaver, J. Mager, R. M. Schultz, and M. S. Bartolomei. 27 September 2007, posting date. Manipulations of mouse embryos prior to implantation result in aberrant expression of imprinted genes on day 9.5 of development. Hum. Mol. Gen. [Epub ahead of print.]
   PubMedGoogle Scholar
• Sarraf, S. A., and I. Stancheva. 2004. Methyl-CpG binding protein MBD1 couples H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol. Cell 15:595–605.
   PubMed Web of Science ®Google Scholar
• Sasaki, H., A. C. Ferguson-Smith, A. S. Shum, S. C. Barton, and M. A. Surani. 1995. Temporal and spatial regulation of H19 imprinting in normal and uniparental mouse embryos. Development 121:4195–4202.
   PubMedGoogle Scholar
• Schulz, R., T. R. Menheniott, K. Woodfine, A. J. Wood, J. D. Choi, and R. J. Oakey. 2006. Chromosome-wide identification of novel imprinted genes using microarrays and uniparental disomies. Nucleic Acids Res. 34:e88.
   PubMedGoogle Scholar
• Smilinich, N. J., C. D. Day, G. V. Fitzpatrick, G. M. Caldwell, A. C. Lossie, P. R. Cooper, A. C. Smallwood, J. A. Joyce, P. N. Schofield, W. Reik, R. D. Nicholls, R. Weksberg, D. J. Driscoll, E. R. Maher, T. B. Shows, and M. J. Higgins. 1999. A maternally methylated CpG island in KvLQT1 is associated with an antisense paternal transcript and loss of imprinting in Beckwith-Wiedemann syndrome. Proc. Natl. Acad. Sci. USA 96:8064–8069.
   PubMed Web of Science ®Google Scholar
• Sutherland, H. G., G. K. Mumford, K. Newton, L. V. Ford, R. Farrall, G. Dellaire, J. F. Caceres, and W. A. Bickmore. 2001. Large-scale identification of mammalian proteins localized to nuclear sub-compartments. Hum. Mol. Genet. 10:1995–2011.
   PubMed Web of Science ®Google Scholar
• Tachibana, M., K. Sugimoto, M. Nozaki, J. Ueda, T. Ohta, M. Ohki, M. Fukuda, N. Takeda, H. Niida, H. Kato, and Y. Shinkai. 2002. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16:1779–1791.
   PubMed Web of Science ®Google Scholar
• Tachibana, M., J. Ueda, M. Fukuda, N. Takeda, T. Ohta, H. Iwanari, T. Sakihama, T. Kodama, T. Hamakubo, and Y. Shinkai. 2005. Histone methyltransferase G9a and Glp form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev. 19:815–826.
   PubMed Web of Science ®Google Scholar
• Tanaka, M., M. Puchyr, M. Gerstenstein, K. Harpal, R. Jaenisch, J. Rossant, and A. Nagy. 1999. Parental origin-specific expression of Mash2 is established at the time of implantation with its imprinting mechanism highly resistant to genome-wide demethylation. Mech. Dev. 87:129–142.
   PubMed Web of Science ®Google Scholar
• Ueda, J., M. Tachibana, T. Ikura, and Y. Shinkai. 2006. Zinc finger protein Wiz links G9a/Glp histone methyltransferases to the co-repressor molecule CtBP. J. Biol. Chem. 281:20120–20128.
   PubMedGoogle Scholar
• Uejima, H., M. P. Lee, H. Cui, and A. P. Feinberg. 2000. Hot-stop PCR: a simple and general assay for linear quantitation of allele ratios. Nat. Genet. 25:375–376.
   PubMedGoogle Scholar
• Umlauf, D., Y. Goto, R. Cao, F. Cerqueira, A. Wagschal, Y. Zhang, and R. Feil. 2004. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat. Genet. 36:1296–1300.
   PubMed Web of Science ®Google Scholar
• Verona, R. I., M. R. Mann, and M. S. Bartolomei. 2003. Genomic imprinting: intricacies of epigenetic regulation in clusters. Annu. Rev. Cell Dev. Biol. 19:237–259.
   PubMed Web of Science ®Google Scholar
• Wagschal, A., and R. Feil. 2006. Genomic imprinting in the placenta. Cytogen. Genome Res. 113:90–98.
   PubMed Web of Science ®Google Scholar
• Wu, M.-Y., T.-F. Tsai, and A. L. Beaudet. 2006. Deficiency of Rbp1/Arid4a and Rbbp1l1/Arid4b alters epigenetic modifications and suppresses an imprinting defect in the PWS/AS domain. Genes Dev. 20:2859–2870.
   PubMed Web of Science ®Google Scholar
• Xin, Z., M. Tachibana, M. Guggiari, E. Heard, Y. Shinkai, and J. Wagstaff. 2003. Role of histone methyltransferase G9a in CpG methylation of the Prader-Willi syndrome imprinting center. J. Biol. Chem. 278:14996–15000.
   PubMedGoogle Scholar
• Yang, Y., T. Li, T. H. Vu, G. A. Ulaner, J. F. Hu, and A. R. Hoffman. 2003. The histone code regulating expression of the imprinted mouse Igf2r gene. Endocrinology 144:5658–5670.
   PubMedGoogle Scholar
• Zvetkova, I., A. Apedaile, B. Ramsahoye, J. Mermoud, L. Crompton, R. John, R. Feil, and N. Brockdorff. 2005. Global hypomethylation of the genome in XX ES cells. Nat. Genet. 37:1274–1279.
   PubMedGoogle Scholar