Genetic modification for bimaternal embryo development
Tomohiro Kono
+ Author Affiliations
- Author Affiliations
Department of BioScience, Tokyo University of Agriculture, Setagaya-ku, Tokyo 156-8502, Japan. Email: tomohiro@nodai.ac.jp
Reproduction, Fertility and Development 21(1) 31-36 https://doi.org/10.1071/RD08213
Published: 9 December 2008
Abstract
Full mammalian development typically requires genomes from both the oocyte and spermatozoon. Biparental reproduction is necessary because of parent-specific epigenetic modification of the genome during gametogenesis; that is, a maternal methylation imprint imposed during the oocyte growth period and a paternal methylation imprint imposed in pregonadal gonocytes. This leads to unequivalent expression of imprinted genes from the maternal and paternal alleles in embryos and individuals. It is possible to hypothesise that the maternal methylation imprint is necessary to prevent parthenogenesis, which extinguishes the opportunity for having descendents, whereas the paternal methylation imprint prevents parthenogenesis, ensuring that a paternal contribution is obligatory for any descendants. To date, there are several lines of direct evidence that the epigenetic modifications that occur during oocyte growth have a decisive effect on mammalian development. Using bimaternal embryos with two sets of maternal genomes, the present paper illustrates how parental methylation imprints are an obstacle to the progression of parthenogenesis.
Additional keywords: DNA methylation, embryogenesis, gametogenesis, genomic imprinting, mammals, mouse, parthenogenesis.
Acknowledgements
The author’s work described herein was supported by Grants-in-Aid for Scientific Research on Priority Area, and for Scientific Research A from the Ministry of Education, Science, Culture and Sports of Japan (to T.K.).
References
Abu-Amero, S. , Monk, D. , Apostolidou, S. , Stanier, P. , and Moore, G. (2006). Imprinted genes and their role in human fetal growth. Cytogenet. Genome Res. 113, 262–270.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Allegrucci, C. , Thurston, A. , Lucas, E. , and Young, L. (2005). Epigenetics and the germline. Reproduction 129, 137–149.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Bao, S. , Obata, Y. , Carroll, J. , Domeki, I. , and Kono, T. (2000). Epigenetic modifications necessary for normal development are established during oocyte growth in mice. Biol. Reprod. 62, 616–621.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Bao, S. , Obata, Y. , Ono, Y. , Futatsumata, N. , Niimura, S. , and Kono, T. (2002). Nuclear competence for maturation and pronuclear formation in mouse oocytes. Hum. Reprod. 17, 1311–1316.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bao, S. , Ushijima, H. , Hirose, A. , Aono, F. , Ono, Y. , and Kono, T. (2003). Development of bovine oocytes reconstructed with a nucleus from growing stage oocytes after fertilization in vitro. Theriogenology 59, 1231–1239.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bartolomei, M. S. (2003). Epigenetics: role of germ cell imprinting. Adv. Exp. Med. Biol. 518, 239–245.
| PubMed | CAS |
Bestor, T. H. (2000). The DNA methyltransferases of mammals. Hum. Mol. Genet. 9, 2395–2402.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Branco, M. R. , Oda, M. , and Reik, W. (2008). Safeguarding parental identity: Dnmt1 maintains imprints during epigenetic reprogramming in early embryogenesis. Genes Dev. 22, 1567–1571.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Cassidy, S. B. , Dykens, E. , and Williams, C. A. (2000). Prader–Willi and Angelman syndromes: sister imprinted disorders. Am. J. Med. Genet. 97, 136–146.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Charalambous, M. , Smith, F. M. , Bennett, W. R. , Crew, T. E. , Mackenzie, F. , and Ward, A. (2003). Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proc. Natl Acad. Sci. USA 100, 8292–8297.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Cohen, M. M. (1994). Wiedemann–Beckwith syndrome, imprinting, IGF2, and H19: implications for hemihyperplasia, associated neoplasms, and overgrowth. Am. J. Med. Genet. 52, 233–234.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Costa, F. F. (2008). Non-coding RNAs, epigenetics and complexity. Gene 410, 9–17.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Delaval, K. , and Feil, R. (2004). Epigenetic regulation of mammalian genomic imprinting. Curr. Opin. Genet. Dev. 14, 188–195.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Feil, R. , and Berger, F. (2007). Convergent evolution of genomic imprinting in plants and mammals. Trends Genet. 23, 192–199.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Ferguson-Smith, A. , Lin, S. P. , Tsai, C. E. , Youngson, N. , and Tevendale, M. (2003). Genomic imprinting: insights from studies in mice. Semin. Cell Dev. Biol. 14, 43–49.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Fowden, A. L. , Sibley, C. , Reik, W. , and Constancia, M. (2006). Imprinted genes, placental development and fetal growth. Horm. Res. 65((Suppl. 3)), 50–58.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Georgiades, P. , Watkins, M. , Surani, M. A. , and Ferguson-Smith, A. C. (2000). Parental origin-specific developmental defects in mice with uniparental disomy for chromosome 12. Development 127, 4719–4728.
| PubMed | CAS |
Guillemot, F. , Caspary, T. , Tilghman, S. M. , Copeland, N. G. , Gilbert, D. J. , Jenkins, N. A. , Anderson, D. J. , Joyner, A. L. , Rossant, J. , and Nagy, A. (1995). Genomic imprinting of Mash2, a mouse gene required for trophoblast development. Nat. Genet. 9, 235–242.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
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 | CAS |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kagami, M. , Nagai, T. , Fukami, M. , Yamazawa, K. , and Ogata, T. (2007). Silver–Russell syndrome in a girl born after in vitro fertilization: partial hypermethylation at the differentially methylated region of PEG1/MEST. J. Assist. Reprod. Genet. 24, 131–136.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kagami, M. , Sekita, Y. , Nishimura, G. , Irie, M. , and Kato, F. , et al. (2008). Deletions and epimutations affecting the human 14q32.2 imprinted region in individuals with paternal and maternal upd(14)-like phenotypes. Nat. Genet. 40, 237–242.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
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 | CAS |
Kantor, B. , Shemer, R. , and Razin, A. (2006). The Prader–Willi/Angelman imprinted domain and its control center. Cytogenet. Genome Res. 113, 300–305.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kawahara, M. , Wu, Q. , Yaguchi, Y. , Ferguson-Smith, A. C. , and Kono, T. (2006). Complementary roles of genes regulated by two paternally methylated imprinted regions on chromosomes 7 and 12 in mouse placentation. Hum. Mol. Genet. 15, 2869–2879.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kawahara, M. , Wu, Q. , Ferguson-Smith, A. C. , and Kono, T. (2007a). Appropriate expression of imprinted genes on mouse chromosome 12 extends development of bi-maternal embryos to term. FEBS Lett. 581, 5178–5184.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kawahara, M. , Wu, Q. , Takahashi, N. , Morita, S. , Yamada, K. , Ito, M. , Ferguson-Smith, A. C. , and Kono, T. (2007b). High-frequency generation of viable mice from engineered bi-maternal embryos. Nat. Biotechnol. 25, 1045–1050.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kawahara, M. , Obata, Y. , Sotomaru, Y. , Shimozawa, N. , Bao, S. , Tsukadaira, T. , Fukuda, A. , and Kono, T. (2008). Protocol for the production of viable bimaternal mouse embryos. Nat. Protoc. 3, 197–209.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
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 | CAS |
Kono, T. , Sotomaru, Y. , Katsuzawa, Y. , and Dandolo, L. (2002). Mouse parthenogenetic embryos with monoallelic H19 expression can develop to day 17.5 of gestation. Dev. Biol. 243, 294–300.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kono, T. , Obata, Y. , Wu, Q. , Niwa, K. , Ono, Y. , Yamamoto, Y. , Park, E. S. , Seo, J. S. , and Ogawa, H. (2004). Birth of parthenogenetic mice that can develop to adulthood. Nature 428, 860–864.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lalande, M. , and Calciano, M. A. (2007). Molecular epigenetics of Angelman syndrome. Cell. Mol. Life Sci. 64, 947–960.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Li, E. , Beard, C. , and Jaenisch, R. (1993). Role for DNA methylation in genomic imprinting. Nature 366, 362–365.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
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 | CAS |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lopes, S. , Lewis, A. , Hajkova, P. , Dean, W. , and Oswald, J. , et al. (2003). Epigenetic modifications in an imprinting cluster are controlled by a hierarchy of DMRs suggesting long-range chromatin interactions. Hum. Mol. Genet. 12, 295–305.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lucifero, D. , Chaillet, J. R. , and Trasler, J. M. (2004a). Potential significance of genomic imprinting defects for reproduction and assisted reproductive technology. Hum. Reprod. Update 10, 3–18.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lucifero, D. , Mann, M. , Bartolomei, M. , and Trasler, J. (2004b). Gene-specific timing and epigenetic memory in oocyte imprinting. Hum. Mol. Genet. 13, 839–849.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
McGrath, J. , and Solter, D. (1984). Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37, 179–183.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Moon, Y. S. , Smas, C. M. , Lee, K. , Villena, J. A. , Kim, K. H. , Yun, E. J. , and Sul, H. S. (2002). Mice lacking paternally expressed Pref-1/Dlk1 display growth retardation and accelerated adiposity. Mol. Cell. Biol. 22, 5585–5592.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Moore, T. , and Haig, D. (1991). Genomic imprinting in mamalian development: a parental tug-of-war. Trends Genet. 7, 45–49.
| PubMed | CAS |
Moore, T. , and Mills, W. (2008). Evolutionary theories of imprinting: enough already! Adv. Exp. Med. Biol. 626, 116–122.
| PubMed |
Nicholls, R. D. , and Knepper, J. L. (2001). Genome organization, function, and imprinting in Prader–Willi and Angelman syndromes. Annu. Rev. Genomics Hum. Genet. 2, 153–175.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
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 | CAS |
Obata, Y. , Kaneko-Ishino, T. , Koide, T. , Takai, Y. , Ueda, T. , Domeki, I. , Shiroishi, T. , Ishino, F. , and Kono, T. (1998). Disruption of primary imprinting during oocyte growth leads to the modified expression of imprinted genes during embryogenesis. Development 125, 1553–1560.
| PubMed | CAS |
Obata, Y. , Kono, T. , and Hatada, I. (2002). Oogenesis: maturation of mouse fetal germ cells in vitro. Nature 418, 497–498.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Ono, R. , Nakamura, K. , Inoue, K. , Naruse, M. , and Usami, T. , et al. (2006). Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat. Genet. 38, 101–106.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Reik, W. , and Dean, W. (2001). DNA methylation and mammalian epigenetics. Electrophoresis 22, 2838–2843.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Reik, W. , and Walter, J. (2001). Genomic imprinting: parental influence on the genome. Nat. Rev. Genet. 2, 21–32.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Reik, W. , Santos, F. , and Dean, W. (2003). Mammalian epigenomics: reprogramming the genome for development and therapy. Theriogenology 59, 21–32.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Reinhart, B. , and Chaillet, J. R. (2005). Genomic imprinting: cis-acting sequences and regional control. Int. Rev. Cytol. 243, 173–213.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Ripoche, M. A. , Kress, C. , Poirier, F. , and Dandolo, L. (1997). Deletion of the H19 transcription unit reveals the existence of a putative imprinting control element. Genes Dev. 11, 1596–1604.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Royo, H. , and Cavaille, J. (2008). Non-coding RNAs in imprinted gene clusters. Biol. Cell 100, 149–166.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sarvella, P. (1974). Environmental effects on a parthenogenetic line of chickens. Poult. Sci. 53, 273–279.
| PubMed | CAS |
Surani, M. A. (2007). Germ cells: the eternal link between generations. C. R. Biol. 330, 474–478.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Surani, M. A. H. , Barton, S. C. , and Norris, N. L. (1984). Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308, 548–550.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Suzuki, S. , Renfree, M. B. , Pask, A. J. , Shaw, G. , Kobayashi, S. , Kohda, T. , Kaneko-Ishino, T. , and Ishino, F. (2005). Genomic imprinting of IGF2, p57(KIP2) and PEG1/MEST in a marsupial, the tammar wallaby. Mech. Dev. 122, 213–222.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wagschal, A. , and Feil, R. (2006). Genomic imprinting in the placenta. Cytogenet. Genome Res. 113, 90–98.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Walter, J. , and Paulsen, M. (2003). Imprinting and disease. Semin. Cell Dev. Biol. 14, 101–110.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Watanabe, T. , Totoki, Y. , Toyoda, A. , Kaneda, M. , and Kuramochi-Miyagawa, S. , et al. (2008). Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453, 539–543.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wood, A. J. , and Oakey, R. J. (2006). Genomic imprinting in mammals: emerging themes and established theories. PLoS Genet. 2, e147.
| 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 | CAS |
Zhou, Q. Y. , Huang, J. N. , Xiong, Y. Z. , and Zhao, S. H. (2007). Imprinting analyses of the porcine GATM and PEG10 genes in placentas on Days 75 and 90 of gestation. Genes Genet. Syst. 82, 265–269.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
