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Development and imprinted gene expression in uniparental preimplantation mouse embryos in vitro

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Abstract

Increasing numbers of reports show that imprinted genes play a crucial role in fetal development, and uniparental embryos, which possess two paternally or two maternally derived pronuclei, are excellent tools for investigating the biological significance of imprinted genes. In the present study, to examine the in vitro developmental ability and expression pattern of eight imprinted genes in uniparental embryos, we produced androgenones, gynogenones, and parthenogenones using enucleation. Our data confirmed the previously observed restriction in haploid androgenetic development potential and first indicated that diploid androgenetic embryos were arrested in the 3/4-cell stage. Some imprinted genes were expressed in androgenetic, gynogenetic, and parthenogenetic blastocysts, suggesting that they were unable to maintain their imprinted expression status in uniparental embryos and that both paternal and maternal alleles are required for the specific expression of some imprinted genes.

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References

  1. McGrath J, Solter D (1983) Nuclear transplantation in the mouse embryo by microsurgery and cell fusion. Science 220:1300–1302

    Article  CAS  PubMed  Google Scholar 

  2. Barton SC, Surani MA, Norris ML (1984) Role of paternal and maternal genomes in mouse development. Nature 311:374–376

    Article  CAS  PubMed  Google Scholar 

  3. McGrath J, Solter D (1984) Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37:179–183

    Article  CAS  PubMed  Google Scholar 

  4. Surani MA, Barton SC, Norris ML (1984) Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308:548–550

    Article  CAS  PubMed  Google Scholar 

  5. Hoppe PC, Illmensee K (1977) Microsurgically produced homozygous-diploid uniparental mice. Proc Natl Acad Sci USA 74:5657–5661

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Hoppe PC, Illmensee K (1982) Full-term development after transplantation of parthenogenetic embryonic nuclei into fertilized mouse eggs. Proc Natl Acad Sci USA 79:1912–1916

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Modlinski JA (1980) Preimplantation development of microsurgically obtained haploid and homozygous diploid mouse embryos and effects of pretreatment with Cytochalasin B on enucleated eggs. J Embryol Exp Morphol 60:153–161

    CAS  PubMed  Google Scholar 

  8. Markert CL (1982) Parthenogenesis, homozygosity, and cloning in mammals. J Hered 73:390–397

    CAS  PubMed  Google Scholar 

  9. Kaufman MH, Barton SC, Surani MA (1977) Normal postimplantation development of mouse parthenogenetic embryos to the forelimb bud stage. Nature 265:53–55

    Article  CAS  PubMed  Google Scholar 

  10. Barton SC, Adams CA, Norris ML et al (1985) Development of gynogenetic and parthenogenetic inner cell mass and trophectoderm tissues in reconstituted blastocysts in the mouse. J Embryol Exp Morphol 90:267–285

    CAS  PubMed  Google Scholar 

  11. Nakao M, Sasaki H (1996) Genomic imprinting: significance in development and diseases and the molecular mechanisms. J Biochem 120:467–473

    Article  CAS  PubMed  Google Scholar 

  12. Kajii T, Ohama K (1977) Androgenetic origin of hydatidiform mole. Nature 268:633–634

    Article  CAS  PubMed  Google Scholar 

  13. Kaplan CG, Askin FB, Benirschke K (1979) Cytogenetics of extragonadal tumors. Teratology 19:261–266

    Article  CAS  PubMed  Google Scholar 

  14. Feinberg AP (2000) DNA methylation, genomic imprinting and cancer. Curr Top Microbiol Immunol 249:87–99

    CAS  PubMed  Google Scholar 

  15. Skuse DH, James RS, Bishop DV et al (1997) Evidence from Turner’s syndrome of an imprinted X-linked locus affecting cognitive function. Nature 387:705–708

    Article  CAS  PubMed  Google Scholar 

  16. Nicholls RD (2000) The impact of genomic imprinting for neurobehavioral and developmental disorders. J Clin Invest 105:413–418

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Zhan A, Bao Z, Hu X et al (2008) Accurate methods of DNA extraction and PCR-based genotyping for single scallop embryos/larvae long preserved in ethanol. Mol Ecol Resour 8:790–795

    Article  CAS  PubMed  Google Scholar 

  18. Kay GF, Barton SC, Surani MA et al (1994) Imprinting and X chromosome counting mechanisms determine Xist expression in early mouse development. Cell 77:639–650

    Article  CAS  PubMed  Google Scholar 

  19. Zuccotti M, Monk M (1995) Methylation of the mouse Xist gene in sperm and eggs correlates with imprinted Xist expression and paternal X-inactivation. Nat Genet 9:316–320

    Article  CAS  PubMed  Google Scholar 

  20. Edwards RG (1957) The experimental induction of gynogenesis in the mouse. I. Irradiation of the sperm by x-rays. Proc R Soc Lond B Biol Sci 146:469–487

    Article  CAS  PubMed  Google Scholar 

  21. Edwards RG (1957) The experimental induction of gynogenesis in the mouse. II. Ultra-violet irradiation of the sperm. Proc R Soc Lond B Biol Sci 146:488–504

    Article  CAS  PubMed  Google Scholar 

  22. Edwards RG (1958) The experimental induction of gynogenesis in the mouse. III. Treatment of sperm with trypaflavine, toluidine blue, or nitrogen mustard. Proc R Soc Lond B Biol Sci 149:117–129

    Article  CAS  PubMed  Google Scholar 

  23. Edwards RG (1958) Colchicine-induced heteroploidy in the mouse. I. The induction of triploidy by treatment of the gametes. J Exp Zool 137:317–347

    Article  CAS  PubMed  Google Scholar 

  24. McGaughey RW, Chang MC (1969) Inhibition of fertilization and production of heteroploidy in eggs of mice treated with colchicine. J Exp Zool 171:465–480

    Article  CAS  PubMed  Google Scholar 

  25. Marston JH, Chang MC (1964) The fertilizable life of ova and their morphology following delayed insemination in mature and immature mice. J Exp Zool 155:237–251

    Article  CAS  PubMed  Google Scholar 

  26. Edwards RG, Sirlin JL (1959) Identification of C14-labelled male chromatin at fertilization in colchicine-treated mouse eggs. J Exp Zool 140:19–27

    Article  CAS  PubMed  Google Scholar 

  27. Tarkowski AK, Rossant J (1976) Haploid mouse blastocysts developed from bisected zygotes. Nature 259:663–665

    Article  CAS  PubMed  Google Scholar 

  28. Tarkowki AK (1977) In vitro development of haploid mouse embryos produced by bisection of one-cell fertilized eggs. J Embryol Exp Morphol 38:187–202

    CAS  PubMed  Google Scholar 

  29. Modlinski JA (1975) Haploid mouse embryos obtained by microsurgical removal of one pronucleus. J Embryol Exp Morphol 33:897–905

    CAS  PubMed  Google Scholar 

  30. Hiramoto Y (1962) An analysis of the mechanism of fertilation by means of enucleation of sea urchin eggs. Exp Cell Res 28:323–334

    Article  CAS  PubMed  Google Scholar 

  31. Kono T, Sotomaru Y, Sato Y et al (1993) Development of androgenetic mouse embryos produced by in vitro fertilization of enucleated oocytes. Mol Reprod Dev 34:43–46

    Article  CAS  PubMed  Google Scholar 

  32. Latham KE, Akutsu H, Patel B et al (2002) Comparison of gene expression during preimplantation development between diploid and haploid mouse embryos. Biol Reprod 67:386–392

    Article  CAS  PubMed  Google Scholar 

  33. Cuthbertson KS, Whittingham DG, Cobbold PH (1981) Free Ca2 + increases in exponential phases during mouse oocyte activation. Nature 294:754–757

    Article  CAS  PubMed  Google Scholar 

  34. Szollosi MS, Kubiak JZ, Debey P et al (1993) Inhibition of protein kinases by 6-dimethylaminopurine accelerates the transition to interphase in activated mouse oocytes. J Cell Sci 104(Pt 3):861–872

    CAS  PubMed  Google Scholar 

  35. Surani MA, Barton SC, Norris ML (1986) Nuclear transplantation in the mouse: heritable differences between parental genomes after activation of the embryonic genome. Cell 45:127–136

    Article  CAS  PubMed  Google Scholar 

  36. Obata Y, Ono Y, Akuzawa H et al (2000) Post-implantation development of mouse androgenetic embryos produced by in vitro fertilization of enucleated oocytes. Hum Reprod 15:874–880

    Article  CAS  PubMed  Google Scholar 

  37. Morris T (1968) The XO and OY chromosome constitutions in the mouse. Genet Res 12:125–137

    Article  CAS  PubMed  Google Scholar 

  38. Latham KE, Solter D (1991) Effect of egg composition on the developmental capacity of androgenetic mouse embryos. Development 113:561–568

    CAS  PubMed  Google Scholar 

  39. Hagemann LJ, First NL (1992) Embryonic cytoplasmic extracts rescue murine androgenones to the blastocyst stage. Development 114:997–1001

    CAS  PubMed  Google Scholar 

  40. Latham KE, Doherty AS, Scott CD et al (1994) Igf2r and Igf2 gene expression in androgenetic, gynogenetic, and parthenogenetic preimplantation mouse embryos: absence of regulation by genomic imprinting. Genes Dev 8:290–299

    Article  CAS  PubMed  Google Scholar 

  41. Sotomaru Y, Katsuzawa Y, Hatada I et al (2002) Unregulated expression of the imprinted genes H19 and Igf2r in mouse uniparental fetuses. J Biol Chem 277:12474–12478

    Article  CAS  PubMed  Google Scholar 

  42. Ogawa H, Wu Q, Komiyama J et al (2006) Disruption of parental-specific expression of imprinted genes in uniparental fetuses. FEBS Lett 580:5377–5384

    Article  CAS  PubMed  Google Scholar 

  43. Ruf N, Dunzinger U, Brinckmann A et al (2006) Expression profiling of uniparental mouse embryos is inefficient in identifying novel imprinted genes. Genomics 87:509–519

    Article  CAS  PubMed  Google Scholar 

  44. Cruz NT, Wilson KJ, Cooney MA et al (2008) Putative imprinted gene expression in uniparental bovine embryo models. Reprod Fertil Dev 20:589–597

    Article  PubMed  Google Scholar 

  45. Thurston A, Taylor J, Gardner J et al (2008) Monoallelic expression of nine imprinted genes in the sheep embryo occurs after the blastocyst stage. Reproduction 135:29–40

    Article  CAS  PubMed  Google Scholar 

  46. Arnaud P, Monk D, Hitchins M et al (2003) Conserved methylation imprints in the human and mouse GRB10 genes with divergent allelic expression suggests differential reading of the same mark. Hum Mol Genet 12:1005–1019

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the National Basic Research and Development Program of China (973 Program) (No.2011CB944202, 2010CB945001 and 2009CB941601) and the National Science Supporting Plan of China (2011BAD19B03). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors are grateful to the anonymous reviewers for their comments that helped to improve the earlier versions of this manuscript.

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Authors and Affiliations

  1. Agricultural Animal Genomics and Molecular Breeding Key Lab of Guangdong Province, College of Animal Science, South China Agricultural University, Guangzhou, 510642, China

    Minhua Hu, Li-Chi TuanMu, Hengxi Wei, Fenglei Gao, Li Li & Shouquan Zhang

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  1. Minhua Hu
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  2. Li-Chi TuanMu
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  3. Hengxi Wei
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Correspondence to Shouquan Zhang.

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Hu, M., TuanMu, LC., Wei, H. et al. Development and imprinted gene expression in uniparental preimplantation mouse embryos in vitro. Mol Biol Rep 42, 345–353 (2015). https://doi.org/10.1007/s11033-014-3774-5

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  • DOI: https://doi.org/10.1007/s11033-014-3774-5

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