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DNA synthesis and epigenetic modification during mouse oocyte fertilization by human or hamster sperm injection

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Abstract

Purpose

To evaluate DNA synthesis and epigenetic modification in mouse oocytes during the first cell cycle following the injection of human or hamster sperm.

Methods

Mouse oocytes following the injection of human and hamster sperm and cultured in M16 medium.

Results

Male and female pronucleus formation, DNA synthesis, histone protein modification, and heterochromatin formation were similar in mouse oocytes injected with human or hamster sperm. However, DNA methylation patterns were altered in mouse oocytes following human sperm injection. Immunocytochemical staining with a histone H3-MeK9 antibody revealed that human and hamster sperm chromatin associated normally with female mouse chromatin, then entered into the metaphase and formed normal, two-cell stage embryos.

Conclusions

Although differences in epigenetic modification of DNA were observed, fertilization and cleavage occurred in a species non-specific manner in mouse oocytes.

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References

  1. Yanagimachi R. Intracytoplasmic injection of spermatozoa and spermatogenic cells: its biology and application in human and animals. Reprod Biomed Online. 2005;10:247–88.

    Article  PubMed  Google Scholar 

  2. Yamazaki T, Yamagata K, Baba T. Time-lapse and retrospective analysis of DNA methylation on mouse preimplantation embryos by live cell imaging. Dev Biol. 2007;304:409–19.

    Article  PubMed  CAS  Google Scholar 

  3. Morozumi K, Yanagimachi R. Incorporation of the acrosome into the oocyte during intracytoplasmic sperm injection could be potentially hazardous to embryo development. Proc Natl Acad Sci USA. 2005;102:14209–14.

    Article  PubMed  CAS  Google Scholar 

  4. Aoki E, Schultz RM. DNA replication in the 1-cell mouse embryo: stimulatory effect of histone acetylation. Zygote. 1999;7:165–72.

    Article  PubMed  CAS  Google Scholar 

  5. Akira K, Kwon OY, Tatsuo N, Tomohiro K. DNA synthesis in mouse 1-cell embryos containing transferred nuclei. J Reprod Dev. 1998;44:113–20.

    Article  Google Scholar 

  6. Tesarík J, Kopecný V. Nucleic acid synthesis and development of human male pronucleus. J Reprod Fert. 1989;86:549–58.

    Article  Google Scholar 

  7. Probst AV, Santos F, Reik W, Almouzni G, Dean W. Structural differences in centromeric heterochromatin are spatially reconciled on fertilization in the mouse zygote. Chromosoma. 2007;116:403–15.

    Article  PubMed  Google Scholar 

  8. Shoukir Y, Campana A, Farley T, Sakkas D. Early cleavage of in-vitro fertilized human embryos to the 2-cell stage: a novel indicator of embryo quality and viability. Hum Reprod. 1997;12:1531–6.

    Article  PubMed  CAS  Google Scholar 

  9. Beaujean N, Taylor JE, McGarry M, Gardner JO, Wilmut I, Loi P, et al. The effect of interspecific oocytes on demethylation of sperm DNA. Proc Natl Acad Sci USA. 2004;101:7636–40.

    Article  PubMed  CAS  Google Scholar 

  10. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet. 2002;3:662–73.

    Article  PubMed  CAS  Google Scholar 

  11. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature. 2007;447:425–32.

    Article  PubMed  CAS  Google Scholar 

  12. Kouzarides T. chromatin modifications and their function. Cell. 2007;128:693–705.

    Article  PubMed  CAS  Google Scholar 

  13. Klose RJ, Zhang Y. Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol. 2007;8:307–18.

    Article  PubMed  CAS  Google Scholar 

  14. Surani MA, Hayashi K, Hajkova P. Genetic and epigenetic regulators of pluripotency. Cell. 2007;128:747–62.

    Article  PubMed  CAS  Google Scholar 

  15. Jenuwein T, Allis CD. Translating the histone code. Science. 2001;293:1074–80.

    Article  PubMed  CAS  Google Scholar 

  16. Arney KL, Bao S, Bannister AJ, Kouzarides T, Surani MA. Histone methylation defines epigenetic asymmetry in the mouse zygote. Int J Dev Biol. 2002;46:317–20.

    PubMed  CAS  Google Scholar 

  17. Liu H, Kim JM, Aoki F. Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos. Development. 2004;131:2269–80.

    Article  PubMed  CAS  Google Scholar 

  18. Lepikhov K, Walter J. Differential dynamics of histone H3 methylation at positions K4 and K9 in the mouse zygote. BMC Dev Biol. 2004;4:12.

    Article  PubMed  Google Scholar 

  19. Santos S, Peters AH, Otte AP, Reik W, Dean W. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev Biol. 2005;280:225–36.

    Article  PubMed  CAS  Google Scholar 

  20. Yeo S, Lee KK, Han YM, Kang YK. Methylation changes of lysine 9 of histone H3 during preimplantation mouse development. Mol cells. 2005;20:423–8.

    PubMed  CAS  Google Scholar 

  21. Adenot PG, Mercier Y, Renard JP, Thompson EM. Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development. 1997;124:4615–25.

    PubMed  CAS  Google Scholar 

  22. Worrad DM, Turner BM, Schultz RM. Temporally restricted spatial localization of acetylated isoforms of histone H4 and RNA polymerase II in the 2cell mouse embryo. Development. 1995;121:2949–59.

    PubMed  CAS  Google Scholar 

  23. Yamazaki T. kobayakawa S, Yamagata K, Abe K, Baba T: Molecular dynamics of heterochromatin protein 1beta, HP1beta, during mouse preimplantation development. J Reprod Dev. 2007;53:1035–41.

    Article  PubMed  CAS  Google Scholar 

  24. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T. Demethylation of the zygotic paternal genome. Nature. 2000;403:501–2.

    Article  PubMed  CAS  Google Scholar 

  25. Oswald J, Engemann S, Lane N, Mayer W, Olek A, Fundele R, et al. Active demethylation of the paternal genome in the mouse zygote. Curr Biol. 2000;10:475–8.

    Article  PubMed  CAS  Google Scholar 

  26. Beaujean N, Hartshorne G, Cavilla J, Taylor J, Gardner J, Wilmut I, et al. Non-conservation of mammalian preimplantation methylation dynamics. Curr Biol. 2004;14(7):R266–7.

    Article  PubMed  CAS  Google Scholar 

  27. Shi W, Dirim F, Wolf E, Zakhartchenko V, Haaf T. Methylation reprogramming and chromosomal aneuploidy in in vivo fertilized and cloned rabbit preimplantation embryos. Biol Reprod. 2004;71:340–7.

    Article  PubMed  CAS  Google Scholar 

  28. Hou J, Lei TH, Liu L, Cui XH, An XR, Chen YF. DNA methylation patterns in in vitro-fertilised goat zygotes. Reprod Fert Dev. 2005;17:809–13.

    Article  CAS  Google Scholar 

  29. Schatten G. The centrosome and its mode of inheritance: The reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev Biol. 1994;165:299–335.

    Article  PubMed  CAS  Google Scholar 

  30. Long CR, Pinto-Correia C, Duby RT. Ponce de Leon FA, Boland MP, Roche JF, Robl JM: Chromatin and microtubule morphology during the first cell cycle in bovine zygotes. Mol Reprod Dev. 1993;36:23–32.

    Article  PubMed  CAS  Google Scholar 

  31. Navara CS, First NL, Schatten G. Microtubule organization in the cow during fertilization, polyspermy, parthenogenesis, and nuclear transfer: The role of the sperm aster. Dev Biol. 1994;162:29–40.

    Article  PubMed  CAS  Google Scholar 

  32. Kim N-H, Simerly C, Funahashi H, Schatten G, Day BN. Microtubule organization in porcine oocytes during fertilization and parthenogenesis. Biol Reprod. 1996;54:1397–404.

    Article  PubMed  CAS  Google Scholar 

  33. Kim N-H, Chung KS, Day BN. The role and distribution of microtubule and microfilaments during fertilization and parthenogenesis. J Reprod Fertil. 1997;111:143–9.

    Article  PubMed  CAS  Google Scholar 

  34. Kuretake S, Kimura Y, Hoshi K, Yanagimachi R. Fertilization and development of mouse oocytes injected with isolated sperm heads. Biol Reprod. 1996;55:789–95.

    Article  PubMed  CAS  Google Scholar 

  35. Keefer CL. Fertilization by sperm injection in the rabbit. Gamete Res. 1989;22:59–69.

    Article  PubMed  CAS  Google Scholar 

  36. Bourne H, Richings N, Liu DY, Clarke GN, Harari O, Baker HWG. Sperm preparation for intracytoplasmic injection: methods and relationship to fertilization results. Reprod Fert Dev. 1995;7:177–83.

    Article  CAS  Google Scholar 

  37. Mansour RT, Aboulghar MA, Serour GI, Salah I. Intracytoplasmic injection of sperm head only. J Assist Reprod Genet. 1995;12(suppl):193. abstract.

    Google Scholar 

  38. Kim N-H, Lee JW, Jun SH, Lee HT, Chung KS. Fertilization of porcine oocytes following intracytoplasmic spermatozoon or isolated sperm head injection. Mol Reprod Dev. 1998;51:436–44.

    Article  PubMed  CAS  Google Scholar 

  39. Nakamura S, Terada Y, Horiuchi T, Emuta C, Murakami T, Yaegashi N, et al. Human sperm aster formation and pronuclear decondensation in bovine eggs following intracytoplasmic sperm injection using a piezo-driven pipette: A novel assay for human sperm centrosomal function. Biol Reprod. 2001;65:1359–63.

    Article  PubMed  CAS  Google Scholar 

  40. Kimura Y, Yanagimachi R. Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development. 1995;121:2397–405.

    PubMed  CAS  Google Scholar 

  41. Kishigami S, Wakayama S, Thuan NV, Ohta H, Mizutani E, Hikichi T, et al. Production of cloned mice by somatic cell nuclear transfer. Nat Protoc. 2006;1:125–38.

    Article  PubMed  CAS  Google Scholar 

  42. Dean W, Santos F, Stojkovic M. zakhartchenko V, Walter J, Wolf E, Reik W: Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci USA. 2001;98:13734–8.

    Article  PubMed  CAS  Google Scholar 

  43. SAS. User’s Guide: statistics, version 5. Cary: SAS; 1985.

    Google Scholar 

  44. Steel RGD, Torrie JH. Principles and procedures of statistics. New York: McGraw Hill Nook Co; 1980.

    Google Scholar 

  45. Van Steirgehem AC, Nagy Z, Joris H, Liu J, Staessen C, Smitz J, et al. High fertilization and implantation rates after intracytoplasmic sperm injection. Hum Reprod. 1993;8:1061–6.

    Google Scholar 

  46. Bos-Mikichi A, Wood MJ, Candy CJ, Whittingham DG. Cytogenetical analysis and developmental potential of vitrified mouse oocytes. Biol Reprod. 1995;53:780–5.

    Article  Google Scholar 

  47. Che L, Lalonde A, Bordignon V. Chemical activation of parthenogenetic and nuclear transfer porcine oocytes using ionomycin and strontium chloride. Theriogenology. 2007;67:1297–304.

    Article  PubMed  CAS  Google Scholar 

  48. Méo SC, Leal CLV, Garcia JM. Activation and early parthenogenesis of bovine oocytes treated with ethanol and strontium. Ann Reprod Sci. 2004;81:35–46.

    Article  Google Scholar 

  49. Méo SC, Yamazaki W, Leal CLV, Oliveira JA, Garcia JM. Use of strontium for bovine oocyte activation. Theriogenology. 2005;63:2089–102.

    Article  PubMed  Google Scholar 

  50. Suganuma R, Walden CM, Butters TD, Platt FM, Dwek RA, Yanagimachi R, et al. Alkylated imino sugars, reversible male infertility-inducing agents, do not affect the genetic integrity of male mouse germ cells during short-term tre atment despite induction of sperm deformities. Biol Reprod. 2005;72:805–13.

    Article  PubMed  CAS  Google Scholar 

  51. Kim NH, Jun SH, Do JT, Uhm SJ, Lee HT, Chung KS. Intracytoplasmic injection of porcine, bovine, mouse or human spermatozoon into porcine oocytes. Mol Reprod Dev. 1999;53:84–91.

    Article  PubMed  CAS  Google Scholar 

  52. Kim BK, Cheon SH, Lee YJ, Choi SH, Cui XS, Kim NH. Pronucleus formation, DNA synthesis and metaphase entry in porcine oocytes following intracytoplasmic injection of murine spermatozoa. Zygote. 2003;11:261–70.

    Article  PubMed  CAS  Google Scholar 

  53. Fulka H, Barnetova I, Mosko T, Fulka Jr J. Epigenetic analysis of human spermatozoa after their injection into ovulated mouse oocytes. Hum Reprod. 2008;23:627–34.

    Article  PubMed  CAS  Google Scholar 

  54. Hou J, Liu L, Zhang J, Cui XH, Yan FX, Guan H, et al. Epigenetic modification of histone 3 at lysine 9 in sheep zygotes and its relationship with DNA methylation. BMC Dev Biol. 2008;8:60.

    Article  PubMed  Google Scholar 

  55. Zaitseva I, Zaitsev S, Alenina N, Bader M, Krivokharchenko A. Dynamics of DNA-demethylation in early mouse and rat embryos developed in vivo and In vitro. Mol Reprod Dev. 2007;74:1255–61.

    Article  PubMed  CAS  Google Scholar 

  56. Park JS, Jeong YS, Shin ST, Lee KK, Kang YK. Dynamic DNA methylation reprogramming: active demethylation and immediate remethylation in the male pronucleus of bovine zygotes. Dev Dyn. 2007;236:2523–33.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This study was supported financially by a grant from the BioGreen 21 program (201003010612240010400 and 201003010612240010500) and KOSEF (20100002070), Rural Development Administration (RDA), Republic of Korea.

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Correspondence to Nam-Hyung Kim.

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Capsule Using mouse oocytes as ICSI recipients for human and mamster sperm, embryonic cell cycle progression is observed despite the presence of altered epigenetic modifications in sperm chromatin.

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Xu, YN., Cui, XS., Tae, JC. et al. DNA synthesis and epigenetic modification during mouse oocyte fertilization by human or hamster sperm injection. J Assist Reprod Genet 28, 325–333 (2011). https://doi.org/10.1007/s10815-010-9509-1

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  • DOI: https://doi.org/10.1007/s10815-010-9509-1

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