Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-26T21:08:53.492Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of volume of oocyte cytoplasm on embryo development after parthenogenetic activation, intracytoplasmic sperm injection, or somatic cell nuclear transfer

Published online by Cambridge University Press:  01 August 2008

Wakayama Sayaka ,
Kishigami Satoshi ,
Nguyen Van Thuan ,
Ohta Hiroshi ,
Hikichi Takafusa ,
Mizutani Eiji ,
Bui Hong Thuy ,
Miyake Masashi  and
Wakayama Teruhiko
Wakayama Sayaka
Affiliation:
Laboratory for Genomic Reprogramming, Center for Developmental Biology, RIKEN Kobe, Japan.
Kishigami Satoshi
Affiliation:
Laboratory for Genomic Reprogramming, Center for Developmental Biology, RIKEN Kobe, Japan.
Nguyen Van Thuan
Affiliation:
Laboratory for Genomic Reprogramming, Center for Developmental Biology, RIKEN Kobe, Japan.
Ohta Hiroshi
Affiliation:
Laboratory for Genomic Reprogramming, Center for Developmental Biology, RIKEN Kobe, Japan.
Hikichi Takafusa
Affiliation:
Laboratory for Genomic Reprogramming, Center for Developmental Biology, RIKEN Kobe, Japan.
Mizutani Eiji
Affiliation:
Laboratory for Genomic Reprogramming, Center for Developmental Biology, RIKEN Kobe, Japan.
Bui Hong Thuy
Affiliation:
Laboratory for Genomic Reprogramming, Center for Developmental Biology, RIKEN Kobe, Japan.
Miyake Masashi
Affiliation:
Department of Life Science, Graduate School of Science and Technology, Kobe University, Kobe 657–8501, Japan.
Wakayama Teruhiko*
Affiliation:
Laboratory for Genomic Reprogramming, Center for Developmental Biology, RIKEN Kobe, 2–2–3 Minatojima-minamimachi Chuo-ku, Kobe 650–0047, Japan. Laboratory for Genomic Reprogramming, Center for Developmental Biology, RIKEN Kobe, Japan.
*
All correspondence to: Wakayama Teruhiko. Laboratory for Genomic Reprogramming, Center for Developmental Biology, RIKEN Kobe, 2–2–3 Minatojima-minamimachi Chuo-ku, Kobe 650–0047, Japan. Tel: +81 78 306 3049. Fax: +81 78 306 0101. e-mail [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Animal cloning methods are now well described and are becoming routine. Yet, the frequency at which live cloned offspring are produced remains below 5%, irrespective of the nuclear donor species or cell type. One possible explanation is that the reprogramming factor(s) of each oocyte is insufficient or not properly adapted for the receipt of a somatic cell nucleus, because it is naturally prepared only for the receipt of a gamete. Here, we have increased the oocyte volume by oocyte fusion and examined its subsequent development. We constructed oocytes with volumes two to nine times greater than the normal volume by the electrofusion or mechanical fusion of intact and enucleated oocytes. We examined their in vitro and in vivo developmental potential after parthenogenetic activation, intracytoplasmic sperm injection (ICSI) and somatic cell nuclear transfer (SCNT). When the fused oocytes were activated parthenogenetically, most developed to morulae or blastocysts, regardless of their original size. Diploid fused oocytes were fertilized by ICSI and developed normally and after embryo transfer, we obtained 12 (4–15%) healthy and fertile offspring. However, enucleated fused oocytes could not support the development of mice cloned by SCNT. These results suggest that double fused oocytes have normal potential for development after fertilization, but oocytes with extra cytoplasm do not have enhanced reprogramming potential.

Keywords

Giant oocyteFertilizationICSINuclear transferParthenogenesis
Type
Research Article
Information
Zygote , Volume 16 , Issue 3 , August 2008 , pp. 211 - 222
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Austin, C.R. (1960). Anomalies of fertilization leading to triploidy. J. Cell. Comp. Physiol. 56 (Suppl 1), 1–15.CrossRefGoogle Scholar
Austin, C.R. & Braden, A.W. (1954). Anomalies in rat, mouse and rabbit eggs. Aust. J. Biol. Sci. 7, 537–42.CrossRefGoogle ScholarPubMed
Balakier, H., Bouman, D., Sojecki, A., Librach, C. & Squire, J.A. (2002). Morphological and cytogenetic analysis of human giant oocytes and giant embryos. Hum. Reprod. 17, 2394–401.CrossRefGoogle ScholarPubMed
Boiani, M., Eckardt, S., Leu, N.A., Scholer, H.R. & McLaughlin, K.J. (2003). Pluripotency deficit in clones overcome by clone–clone aggregation: epigenetic complementation? EMBO J. 22, 5304–12.CrossRefGoogle ScholarPubMed
Bos-Mikich, A., Whittingham, D.G. & Jones, K.T. (1997). Meiotic and mitotic Ca2+ oscillations affect cell composition in resulting blastocysts. Dev. Biol. 182, 172–9.CrossRefGoogle ScholarPubMed
Chatot, C.L., Lewis, J.L., Torres, I. & Ziomek, C.A. (1990). Development of 1-cell embryos from different strains of mice in CZB medium. Biol. Reprod. 42, 432–40.CrossRefGoogle ScholarPubMed
Clarke, H.J. & Masui, Y. (1987). Dose-dependent relationship between oocyte cytoplasmic volume and transformation of sperm nuclei to metaphase chromosomes. J. Cell. Biol. 104, 831–40.CrossRefGoogle ScholarPubMed
Cohen, J., Scott, R., Alikani, M., Schimmel, T., Munne, S., Levron, J., Wu, L., Brenner, C., Warner, C. & Willadsen, S. (1998). Ooplasmic transfer in mature human oocytes. Mol. Hum. Reprod. 4, 269–80.CrossRefGoogle ScholarPubMed
Eglitis, M.A. (1980). Formation of tetraploid mouse blastocysts following blastomere fusion with polyethylene glycol. J. Exp. Zool. 213, 309–13.CrossRefGoogle ScholarPubMed
Fulka, H. (2004). Distribution of mitochondria in reconstructed mouse oocytes. Reproduction 127, 195–200.CrossRefGoogle ScholarPubMed
FulkaJ., Jr. J., Jr., Flechon, B. & Flechon, J.E. (1989). Fusion of mammalian oocytes: SEM observations of surface changes. Reprod. Nutr. Dev. 29, 551–7.CrossRefGoogle ScholarPubMed
FulkaJ., Jr. J., Jr., Notarianni, E., Passoni, L. & Moor, R.M. (1993). Early changes in embryonic nuclei fused to chemically enucleated mouse oocytes. Int. J. Dev. Biol. 37, 433–9.Google ScholarPubMed
FulkaJ., Jr. J., Jr., Kalab, P., First, N.L. & Moor, R.M. (1997). Damaged chromatin does not prevent the exit from metaphase I in fused mouse oocytes. Hum. Reprod. 12, 2473–6.CrossRefGoogle Scholar
Funaki, K. & Mikamo, K. (1980). Giant diploid oocytes as a cause of digynic triploidy in mammals. Cytogenet. Cell. Genet. 28, 158–68.CrossRefGoogle ScholarPubMed
Gordo, A. C., Rodrigues, P., Kurokawa, M., Jellerette, T., Exley, G. E., Warner, C. & Fissore, R. (2002). Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs. Biol. Reprod. 66, 1828–37.CrossRefGoogle ScholarPubMed
Gulyas, B.J., Wood, M. & Whittingham, D. G. (1984). Fusion of oocytes and development of oocyte fusion products in the mouse. Dev. Biol. 101, 246–50.CrossRefGoogle ScholarPubMed
Henery, C.C. & Kaufman, M.H. (1993). The cleavage rate of digynic triploid mouse embryos during the preimplantation period. Mol. Reprod. Dev. 34, 272–9.CrossRefGoogle ScholarPubMed
Karnikova, L., Jacquet, P. & FulkaJ., Jr. J., Jr. (2000). Preimplantation development of giant triploid zygotes in the mouse. Folia Biol. (Praha), 46, 83–6.Google ScholarPubMed
Kimura, Y. & Yanagimachi, R. (1995). Intracytoplasmic sperm injection in the mouse. Biol. Reprod. 52, 709–20.CrossRefGoogle ScholarPubMed
Kishigami, S., Mizutani, E., Ohta, H., Hikichi, T., Thuan, N.V., Wakayama, S., Bui, H.T. & Wakayama, T. (2006a). Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem. Biophys. Res. Commun. 340, 183–9.CrossRefGoogle ScholarPubMed
Kishigami, S., Wakayama, S., Thuan, N.V., Ohta, H., Mizutani, E., Hikichi, T., Bui, H.T., Balbach, S., Ogura, A., Boiani, M. & Wakayama, T. (2006b). Production of cloned mice by somatic cell nuclear transfer. Nature Protocols 1, 125–38.CrossRefGoogle ScholarPubMed
Kishigami, S., Bui, H.T., Wakayama, S., Tokunaga, K., Van Thuan, N., Hikichi, T., Mizutani, E., Ohta, H., Suetsugu, R., Sata, T. & Wakayama, T. (2007). Successful mouse cloning of an outbred strain by trichostatin A treatment after somatic nuclear transfer. J. Reprod. Dev. 53, 165–70.CrossRefGoogle ScholarPubMed
Krukowska, A., Wielkopolska, E., Czolowska, R., Maleszewski, M. & Tarkowski, A.K. (1998). Mouse oocytes and parthenogenetic eggs lose the ability to be penetrated by spermatozoa after fusion with zygotes. Zygote 6, 321–8.CrossRefGoogle ScholarPubMed
Kusakabe, H., Szczygiel, M.A., Whittingham, D.G. & Yanagimachi, R. (2001). Maintenance of genetic integrity in frozen and freeze-dried mouse spermatozoa. Proc. Natl. Acad. Sci. U S A 98, 13501–6.CrossRefGoogle ScholarPubMed
McGrath, J. & Solter, D. (1984). Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37, 179–83.CrossRefGoogle ScholarPubMed
Mizutani, E., Ohta, H., Kishigami, S., Van Thuan, N., Hikichi, T., Wakayama, S., Kosaka, M., Sato, E. & Wakayama, T. (2006). Developmental ability of cloned embryos from neural stem cells. Reproduction 132, 849–57.CrossRefGoogle ScholarPubMed
Nagy, A., Gertsenstein, M., Vintersten, K. & Behringer, R. (2003). Manipulating the Mouse Embryo; A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.Google Scholar
Naito, K., Toyoda, Y. & Yanagimachi, R. (1992). Production of normal mice from oocytes fertilized and developed without zonae pellucidae. Hum. Reprod. 7, 281–5.CrossRefGoogle ScholarPubMed
Ogura, A., Ogonuki, N., Takano, K. & Inoue, K. (2001). Microinsemination, nuclear transfer and cytoplasmic transfer: the application of new reproductive engineering techniques to mouse genetics. Mamm. Genome 12, 803–12.CrossRefGoogle ScholarPubMed
Peura, T.T., Lewis, I. M. & Trounson, A.O. (1998). The effect of recipient oocyte volume on nuclear transfer in cattle. Mol. Reprod. Dev. 50, 185–91.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Ribas, R., Oback, B., Ritchie, W., Chebotareva, T., Ferrier, P., Clarke, C., Taylor, J., Gallagher, E.J., Mauricio, A.C., Sousa, M. & Wilmut, I. (2005). Development of a zona-free method of nuclear transfer in the mouse. Cloning Stem Cells 7, 126–38.CrossRefGoogle ScholarPubMed
Rosenbusch, B. & Schneider, M. (1998). Maturation of a binuclear oocyte from the germinal vesicle stage to metaphase II: formation of two polar bodies and two haploid chromosome sets. Hum. Reprod. 13, 1653–5.CrossRefGoogle ScholarPubMed
Sherard, J., Bean, C., Bove, B., DelDucaV., Jr. V., Jr., Esterly, K.L., Karcsh, H.J., Munshi, G., Reamer, J. F., Suazo, G., Wilmoth, D. et al. (1986). Long survival in a 69,XXY triploid male. Am. J. Med. Genet. 25, 307–12.CrossRefGoogle Scholar
Snow, M.H. (1975). Embryonic development of tetraploid mice during the second half of gestation. J. Embryol Exp. Morphol. 34, 707–21.Google ScholarPubMed
Soupart, P. (1980). Initiation of mouse embryonic development by oocyte fusion. Arch. Androl. 5, 55–7.Google Scholar
Surani, M.A., Barton, S.C. & Norris, M.L. (1984). Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308, 548–50.CrossRefGoogle ScholarPubMed
Suzuki, H., Togashi, M., Adachi, J. & Toyoda, Y. (1995). Developmental ability of zona-free mouse embryos is influenced by cell association at the 4-cell stage. Biol. Reprod. 53, 78–83.CrossRefGoogle Scholar
Tarkowski, A.K. & Balakier, H. (1980). Nucleo-cytoplasmic interactions in cell hybrids between mouse oocytes, blastomeres and somatic cells. J. Embryol. Exp. Morphol. 55, 319–30.Google ScholarPubMed
Tecirlioglu, R.T., French, A.J., Lewis, I.M., Vajta, G., Korfiatis, N.A., Hall, V.J., Ruddock, N.T., Cooney, M.A. & Trounson, A.O. (2004). Birth of a cloned calf derived from a vitrified hand-made cloned embryo. Reprod. Fertil. Dev. 15, 361–6.CrossRefGoogle Scholar
Tesarik, J. & Testart, J. (1994). Treatment of sperm-injected human oocytes with Ca2+ ionophore supports the development of Ca2+ oscillations. Biol. Reprod. 51, 385–91.CrossRefGoogle ScholarPubMed
Tesarik, J., Nagy, Z.P., Mendoza, C. & Greco, E. (2000). Chemically and mechanically induced membrane fusion: nonactivating methods for nuclear transfer in mature human oocytes. Hum. Reprod. 15, 1149–54.CrossRefGoogle ScholarPubMed
Toyoda, Y., Yokoyama, M. & Hoshi, T. (1971). Studies on the fertilization of mouse eggs in vitro. Jpn J. Anim. Reprod. 16, 152–7.CrossRefGoogle Scholar
Vajta, G., Lewis, I.M., Trounson, A.O., Purup, S., Maddox-Hyttel, P., Schmidt, M., Pedersen, H.G., Greve, T. & Callesen, H. (2003). Handmade somatic cell cloning in cattle: analysis of factors contributing to high efficiency in vitro. Biol. Reprod. 68, 571–8.CrossRefGoogle ScholarPubMed
Van Thuan, N., Wakayama, S., Kishigami, S. & Wakayama, T. (2006). Donor centrosome regulation of initial spindle formation in mouse somatic cell nuclear transfer: roles of gamma-tubulin and nuclear mitotic apparatus protein 1. Biol. Reprod. 74, 777–87.CrossRefGoogle ScholarPubMed
Vassetzky, S. G. & Sekirina, G. G. (1985). Induced fusion of female gametes and embryonic cells. Cell Differ. 16, 77–82.CrossRefGoogle ScholarPubMed
Wakayama, S., Mizutani, E., Kishigami, S., Thuan, N.V., Ohta, H., Hikichi, T., Bui, H.T., Miyake, M. & Wakayama, T. (2005). Mice cloned by nuclear transfer from somatic and ntES cells derived from the same individuals. J. Reprod. Dev. 51, 765–72.CrossRefGoogle ScholarPubMed
Wakayama, T. (2007). Production of cloned mice and ES cells from adult somatic cells by nuclear transfer: how to improve cloning efficiency? J. Reprod. Dev. 53, 13–26.CrossRefGoogle ScholarPubMed
Wakayama, T. & Yanagimachi, R. (1998). Fertilisability and developmental ability of mouse oocytes with reduced amounts of cytoplasm. Zygote 6, 341–6.CrossRefGoogle ScholarPubMed
Wakayama, T. & Yanagimachi, R. (1999). Cloning of male mice from adult tail-tip cells. Nat. Genet. 22, 127–8.CrossRefGoogle ScholarPubMed
Wakayama, T. & Yanagimachi, R. (2001a). Effect of cytokinesis inhibitors, DMSO and the timing of oocyte activation on mouse cloning using cumulus cell nuclei. Reproduction 122, 49–60.CrossRefGoogle ScholarPubMed
Wakayama, T. & Yanagimachi, R. (2001b). Mouse cloning with nucleus donor cells of different age and type. Mol. Reprod. Dev. 58, 376–83.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Wakayama, T., Perry, A.C., Zuccotti, M., Johnson, K. R. & Yanagimachi, R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394, 369–74.CrossRefGoogle ScholarPubMed
Wakayama, T., Tabar, V., Rodriguez, I., Perry, A. C., Studer, L. & Mombaerts, P. (2001). Differentiation of embryonic stem cell lines generated from adult somatic cells by nuclear transfer. Science 292, 740–3.CrossRefGoogle ScholarPubMed
Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J. & Campbell, K.H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–13.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (1998). Intracytoplasmic sperm injection experiments using the mouse as a model. Hum. Reprod. 13 (Suppl 1), 87–98.CrossRefGoogle ScholarPubMed