Gamete imprinting: setting epigenetic patterns for the next generation
Jacquetta M. Trasler
+ Author Affiliations
- Author Affiliations
McGill University-Montreal Children’s Hospital Research Institute and the Departments of Pediatrics, Human Genetics and Pharmacology and Therapeutics, McGill University, Montreal, Quebec, Canada. Email: jacquetta.trasler@mcgill.ca
Reproduction, Fertility and Development 18(2) 63-69 https://doi.org/10.1071/RD05118
Submitted: 21 September 2005 Accepted: 21 September 2005 Published: 14 December 2005
Abstract
The acquisition of genomic DNA methylation patterns, including those important for development, begins in the germ line. In particular, imprinted genes are differentially marked in the developing male and female germ cells to ensure parent-of-origin-specific expression in the offspring. Abnormalities in imprints are associated with perturbations in growth, placental function, neurobehavioural processes and carcinogenesis. Based, for the most part, on data from the well-characterised mouse model, the present review will describe recent studies on the timing and mechanisms underlying the acquisition and maintenance of DNA methylation patterns in gametes and early embryos, as well as the consequences of altering these patterns.
Extra keywords: assisted reproductive technologies, DNA methylation, embryogenesis, genomic imprinting, germ cells, human, mouse, oogenesis, spermatogenesis.
Acknowledgments
JMT is a William Dawson Scholar of McGill University and a Scholar of the Fonds de la recherche en santé du Québec. This work was supported by grants from the Canadian Institutes of Health Research and the National Institutes of Health (USA).
References
Aapola, U. , Lyle, R. , Krohn, K. , Antonarakis, S. E. , and Peterson, P. (2001). Isolation and initial characterization of the mouse Dnmt3l gene. Cytogenet. Cell Genet. 92, 122–126.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Allegrucci, C. , Denning, C. , Priddle, H. , and Young, L. (2004). Stem-cell consequences of embryo epigenetic defects. Lancet 364, 206–208.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Anway, M. , Cupp, A. S. , Uzuncu, M. , and Skinner, M. K. (2005). Epigenetic transgenerational actions of endocrine disruptors and male infertility. Science 308, 1466–1469.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bao, S. , Obata, Y. , Carroll, J. , Domecki, I. , and Kono, T. (2000). Epigenetic modifications necessary for normal development are established during oocyte growth in mice. Biol. Reprod. 62, 616–621.
| PubMed |
Bestor, T. , Laudano, A. , and Mattaliano, R. (1988). Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J. Mol. Biol. 203, 971–983.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bourc’his, D. , and Bestor, T. H. (2004). Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96–99.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brandeis, M. , Ariel, M. , and Cedar, H. (1993). Dynamics of DNA methylation during development. Bioessays 15, 709–713.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chaillet, J. R. , Vogt, T. F. , Beier, D. R. , and Leder, P. (1991). Parental-specific methylation of an imprinted transgene is established during gametogenesis and progressively changes during embryogenesis. Cell 66, 77–83.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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, 16 916–16 921.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Clark, S. J. , Harrison, J. , Paul, C. L. , and Frommer, M. (1994). High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 22, 2990–2997.
| PubMed |
Coffigny, H. , Bourgeois, C. , Ricoul, M. , Bernardino, J. , Vilain, A. , Niveleau, A. , Malfoy, B. , and Dutrillaux, B. (1999). Alterations of DNA methylation patterns in germ cells and Sertoli cells from developing mouse testis. Cytogenet. Cell Genet. 87, 175–181.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cox, G. F. , Burger, J. , Lip, V. , Mau, U. A. , Sperling, K. , Wu, B. L. , and Horsthemke, B. (2002). Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am. J. Hum. Genet. 71, 162–164.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dean, W. , Bowden, L. , Aitchison, A. , Klose, J. , Moore, T. , Meneses, J. J. , Reik, W. , and Feil, R. (1998). Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: association with aberrant phenotypes. Development 125, 2273–2282.
| PubMed |
DeBaun, M. R. , Niemitz, E. L. , and Feinberg, A. P. (2003). Association of in vitro fertilization with Beckwith–Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am. J. Hum. Genet. 72, 156–160.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Doherty, A. S. , Mann, M. R. , Tremblay, K. D. , Bartolomei, M. S. , and Schultz, R. M. (2000). Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol. Reprod. 62, 1526–1535.
| PubMed |
Egger, G. , Liang, G. , Aparico, A. , and Jones, P. A. (2004). Epigenetics in human disease and prospects for epigenetic therapy. Nature 429, 457–463.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
El Maarri, O. , Seoud, M. , Coullin, P. , Herbiniaux, U. , Oldenburg, J. , Rouleau, G. , and Slim, R. (2003). Maternal alleles acquiring paternal methylation patterns in biparental complete hydatidiform moles. Hum. Mol. Genet. 12, 1405–1413.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gicquel, C. , Gaston, V. , Mandelbaum, J. , Siffroi, J. P. , Flahault, A. , and Le Bouc, Y. (2003). In vitro fertilization may increase the risk of Beckwith–Wiedemann syndrome related to the abnormal imprinting of the KCNQ1OT1 gene. Am. J. Hum. Genet. 72, 1338–1341.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Goll, M. G. , and Bestor, T. H. (2005). Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem. 74, 481–514.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Halliday, J. , Oke, K. , Breheny, S. , Algar, E. , and Amor, D. J. (2004). Beckwith–Wiedemann syndrome and IVF: a case-control study. Am. J. Hum. Genet. 75, 526–528.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hanel, M. L. , and Wevrick, R. (2001). Establishment and maintenance of DNA methylation patterns in mouse Ndn: implications for maintenance of imprinting in target genes of the imprinting center. Mol. Cell. Biol. 21, 2384–2392.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| PubMed |
Hayward, B. E. , De Vos, M. , Judson, H. , Hodge, D. , Huntriss, J. , Picton, H. M. , Sheridan, E. , and Bonthron, D. T. (2003). Lack of involvement of known DNA methyltransferases in familial hydatidiform mole implies the involvement of other factors in establishment of imprinting in the human female germline. BMC Genet. 4, 2.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Helwani, M. N. , Seoud, M. , Zahed, L. , Zaatari, G. , Khalil, A. , and Slim, R. (1999). A familial case of recurrent hydatidiform molar pregnancies with biparental genomic contribution. Hum. Genet. 105, 112–115.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Howell, C. Y. , Bestor, T. H. , Ding, F. , Latham, K. E. , Mertineit, C. , Trasler, J. M. , and Chaillet, J. R. (2001). Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104, 829–838.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Howlett, S. K. , and Reik, W. (1991). Methylation levels of maternal and paternal genomes during preimplantation development. Development 113, 119–127.
| PubMed |
Humpherys, D. , Eggan, K. , Akutsu, H. , Hochedlinger, K. , Rideout, W. M. , Biniszkiewicz, D. , Yanigimachi, R. , and Jaenisch, R. (2001). Epigenetic instability in ES cells and cloned mice. Science 293, 95–97.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Judson, H. , Hayward, B. E. , Sheridan, E. , and Bonthron, D. T. (2002). A global disorder of imprinting in the human female germ line. Nature 416, 539–542.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jue, K. , Bestor, T. H. , and Trasler, J. M. (1995). Regulated synthesis and localization of DNA methyltransferase during spermatogenesis. Biol. Reprod. 53, 561–569.
| PubMed |
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.
| PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Khosla, S. , Dean, W. , Brown, D. , Reik, W. , and Feil, R. (2001). Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol. Reprod. 64, 918–926.
| PubMed |
Kono, T. , Obata, Y. , Yoshimzu, T. , Nakahara, T. , and Carroll, J. (1996). Epigenetic modifications during oocyte growth correlates with extended parthenogenetic development in the mouse. Nat. Genet. 13, 91–94.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lucifero, D. , Mann, M. R. , Bartolomei, M. S. , and Trasler, J. M. (2004a). Gene-specific timing and epigenetic memory in oocyte imprinting. Hum. Mol. Genet. 13, 839–849.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lucifero, D. , Chaillet, J. R. , and Trasler, J. M. (2004b). Potential significance of genomic imprinting defects for reproduction and assisted reproductive technology. Hum. Reprod. Update 10, 3–18.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ludwig, M. , Katalinic, A. , Gross, S. , Sutcliffe, A. , Varon, R. , and Horsthemke, B. (2005). Increased prevalence of imprinting defects in patients with Angelman syndrome born to subfertile couples. J. Med. Genet. 42, 289–291.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
MacLean, J. A. , and Wilkinson, M. F. (2005). Gene regulation in spermatogenesis. Curr. Top. Dev. Biol. ,in press.
Maher, E. R. , Brueton, L. A. , Bowdin, S. C. , Luharia, A. , and Cooper, W. , et al. (2003). Beckwith–Wiedemann syndrome and assisted reproduction technology (ART). J. Med. Genet. 40, 62–64.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Maitra, A. , Arking, D. E. , Shivapurkar, N. , Ikeda, M. , and Stastny, V. , et al. (2005). Genomic alterations in cultured human embryonic stem cells. Nat. Genet. ,in press.
| PubMed |
Marques, C. J. , Carvalho, F. , Sousa, M. , and Barros, A. (2004). Genomic imprinting in disruptive spermatogenesis. Lancet 363, 1700–1702.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mayer, W. , Niveleau, A. , Walter, J. , Fundele, R. , and Haaf, T. (2000). Demethylation of the zygotic paternal genome. Nature 403, 501–502.
| PubMed |
Mertineit, C. , Yoder, J. A. , Taketo, T. , Laird, D. W. , Trasler, J. M. , and Bestor, T. H. (1998). Sex-specific exons control DNA methyltransferase in mammalian germ cells. Development 125, 889–897.
| PubMed |
Moglabey, Y. B. , Kircheisen, R. , Seoud, M. , El Mogharbel, N. , Van den Veyrer, I. , and Slim, R. (1999). Genetic mapping of a maternal locus responsible for familial hydatidiform moles. Hum. Mol. Genet. 8, 667–671.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| PubMed |
Morgan, H. D. , Sutherland, H. G. , Martin, D. I. , and Whitelaw, E. (1999). Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 23, 314–318.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nikaido, I. , Saito, C. , Mizuno, Y. , Meguro, M. , and Bono, H. , et al. (2003). Discovery of imprinted transcripts in the mouse transcriptome using large-scale expression profiling. Genome Res. 13, 1402–1409.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Obata, Y. , and Kono, T. (2002). Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J. Biol. Chem. 277, 5285–5289.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Olek, A. , and Walter, J. (1997). The pre-implantation ontogeny of the H19 methylation imprint. Nat. Genet. 17, 275–276.
| PubMed |
Orstavik, K. H. , Eiklid, K. , van der Hagen, C. B. , Spetalen, S. , Kierulf, K. , Skjeldal, O. , and Buiting, K. (2003). Another case of imprinting defect in a girl with Angelman syndrome who was conceived by intracytoplasmic semen injection. Am. J. Hum. Genet. 72, 218–219.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ratnam, S. , Mertineit, C. , Ding, F. , Howell, C. Y. , Clarke, H. J. , Bestor, T. H. , Chaillet, J. R. , and Trasler, J. M. (2002). Dynamics of Dnmt1 methyltransferase expression and intracellular localization during oogenesis and preimplantation development. Dev. Biol. 245, 304–314.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Reik, W. , and Walter, J. (2001). Genomic imprinting: parental influence on the genome. Nat. Rev. Genet. 2, 21–32.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rougier, N. , Bourc'his, D. , Gomes, D. M. , Niveleau, A. , Plachot, M. , Paldi, A. , and Viegas-Pequignot, E. (1998). Chromosome methylation patterns during mammalian preimplantation development. Genes Dev. 12, 2108–2113.
| PubMed |
Rugg-Gunn, P. J. , Ferguson-Smith, A. C. , and Pedersen, R. A. (2005). Epigenetic status of human embryonic stem cells. Nat. Genet. 37, 585–587.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sakai, Y. , Suetake, I. , Itoh, K. , Mizugaki, M. , Tajima, S. , and Yamashima, S. (2001). Expression of DNA methyltransferase (Dnmt1) in testicular germ cells during development of mouse embryo. Cell Struct. Funct. 26, 685–691.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 Expr. Patterns 5, 231–237.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Santos, F. , and Dean, W. (2004). Epigenetic reprogramming during early development in mammals. Reproduction 127, 643–651.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shamanski, F. L. , Kimura, Y. , Lavoir, M. C. , Pedersen, R. , and Yanagimachi, R. (1999). Status of genomic imprinting in mouse spermatids. Hum. Reprod. 14, 1050–1056.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stoger, R. , Kubicka, P. , Liu, C. G. , Kafri, T. , Razin, A. , Cedar, H. , and Barlow, D. P. (1993). Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal. Cell 73, 61–71.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Szabo, P. E. , Hubner, K. , Scholer, H. , and Mann, J. R. (2002). Allele-specific expression of imprinted genes in mouse migratory primordial germ cells. Mech. Dev. 115, 157–160.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Takada, S. , Paulsen, M. , Tevendale, M. , Tsai, C. E. , Kelsey, G. , Cattanach, B. M. , and Ferguson-Smith, A. C. (2002). Epigenetic analysis of the Dlk1-Gtl2 imprinted domain on mouse chromosome 12: implications for imprinting control from comparison with Igf2–H19. Hum. Mol. Genet. 11, 77–86.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| PubMed |
Tycko, B. , and Morison, I. M. (2002). Physiological functions of imprinted genes. J. Cell. Physiol. 192, 245–258.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ueda, T. , Yamazaki, K. , Suzuki, R. , Fujimoto, H. , Sasaki, H. , Sakaki, Y. , and Higashinakagawa, T. (1992). Parental methylation patterns of a transgenic locus in adult somatic tissues are imprinted during gametogenesis. Development 116, 831–839.
| PubMed |
Ueda, T. , Abe, K. , Miura, A. , Yuzuriha, M. , and Zubair, M. , 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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Walsh, C. P. , Chaillet, J. R. , and Bestor, T. H. (1998). Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20, 116–117.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Webster, K. E. , O'Bryan, M. K. , Fletcher, S. , Crewther, P. E. , and Aapola, U. , et al. (2005). Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc. Natl Acad. Sci. USA 102, 4068–4073.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yamazaki, Y. , Mann, M. R. , Lee, S. S. , Marh, J. , McCarrey, J. R. , Yanagimachi, R. , and Bartolomei, M. S. (2003). Reprogramming of primordial germ cells begins before migration into the genital ridge, making these cells inadequate donors for reproductive cloning. Proc. Natl Acad. Sci. USA 100, 12 207–12 212.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yoder, J. A. , and Bestor, T. H. (1998). A candidate mammalian DNA methyltransferase related to pmt1p of fission yeast. Hum. Mol. Genet. 7, 279–284.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Young, L. E. , Fernandes, K. , McEvoy, T. G. , Butterswith, S. C. , Gutierrez, C. G. , Carolan, C. , Broadbent, P. J. , Robinson, J. J. , Wilmut, I. , and Sinclair, K. D. (2001). Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27, 153–154.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
