Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-06-01T04:38:14.428Z Has data issue: false hasContentIssue false
  • English
  • Français

Sperm head decondensation, pronuclear formation, cleavage and embryonic development following intracytoplasmic injection of mitochondria-damaged sperm in mammals

Published online by Cambridge University Press:  26 September 2008

Ali Ahmadi  and
Soon-Chye Ng
Ali Ahmadi
Affiliation:
Department of Obstetrics and Gynaecology, National University of Singapore, Singapore
Soon-Chye Ng*
Affiliation:
Department of Obstetrics and Gynaecology, National University of Singapore, Singapore
*
Soon-Chye Ng, Department of Obstetrics and Gynaecology, National University of Singapore, Lower Kent Ridge Road, Singapore 119074. Telephone: +65- 772 4261. Fax: +65-779 4753. e-mail: obgngsc@nus.sg.
Get access Rights & Permissions [Opens in a new window]

Summary

The objective of this study was to investigate the influence of sperm mitochondrial destruction on sperm head decondensation, male pronuclear formation, cleavage and embryonic development. In the study two models were used:heterologous (hamster ICSI assay: human sperm injected into a hamster oocyte) for evaluation of sperm head decondensation and pronuclear formation, and homologous (mouse model) for the study of fertilisation and development. Destruction of mitochondria of the sperm was achieved by exposure to cyanide, a respiratory poison. Rhodamine 123 was used to evaluate the functional integrity of mitochondria. Sperm head decondensation was found to be not statistically significantly affected by mitochondrial damage (p = 0.8), with 62.8% and 67.9% condensa tion in the experimental and control groups respectively. Male pronucleus formation was seen in 40.2% and 44.4% of the injected oocytes in the experimental and control groups respectively. In the mouse experiments 45.5% and 49.7% of the injected oocytes were fertilised in the mitochondria-damaged and live-intact sperm groups respectively(p = 0.53)Development to blastocyst was achieved in 53.5% and 59.4% of the experimental and control groups respectively; the difference was not significant (p = 0.71). Inner cell mass (ICM) cell number were 15.7 ± 4.02 and 43.1 ± 11.3 respectively in the mitochondria damaged group; the equivalent numbers were 14.12±4.12 and 39.3 ± 12.6 in the control group. However, the differences in ICM and total cell counts between these two groups were not significant. Of the blastocysts transferred to pseudopregnant mice, 51.3% (20/36) implanted and 33.4% (12/36) developed to live fetuses in the mitochondria-damaged group. These rates were 60.5% (23/38) and 39.5% (15/38) in the control group. In conclusion, this study shows that functional integrity of thesperm mitochondria is not necessary in the process of fertilisation and development when the sperm is deposited into the ooplasm. Fertilisation and development can be achieved by injection of sperm at the very early stage of necrosis in which only the mitochondria have been destroyed and the rest of the cell including the plasma membrane is still intact.

Keywords

CleavageDead spermDevelopmentMale pronuclear formationOocyteSpermmitochondria-damagedSperm head decondensation
Type
Article
Information
Zygote , Volume 5 , Issue 3 , August 1997 , pp. 247 - 253
Copyright
Copyright © Cambridge University Press 1997

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

Afzelius, B.A. (1959). Electron microscopy of the sperm tail: results obtained with a new fixative. J. Biophys. Biochem. Cytol. 5, 269–78.CrossRefGoogle ScholarPubMed
Ahmadi, A. & Ng, S.C. (1997). Single sperm curling test, a modified hypo-osmotic swelling test, as a potential technique for selection of viable sperm in intracytoplasmic sperm injection procedure. Fertil.Steril. 68, 346–50.CrossRefGoogle Scholar
Ahmadi, A., Ng, S.C., Liow, S.L., Ali, J., Bongso, A. & Ratnam, S.S. (1995). Intracytoplasmic sperm injection of mouse oocytes with 5mM Ca2+ at different intervals. Hum. Reprod. 10, 431–5.CrossRefGoogle Scholar
Ahmadi, A., Bongso, A. & Ng, S.C. (1996 a)Intracytoplasmic sperm injection of human sperm into frozen-thawedhamster oocytes. Med. Sci. Res. 24, 693–4.Google Scholar
Ahmadi, A., Bongso, A. & Ng, S.C. (1996 b) Intracytoplasmic sperm injection of human sperm into the hamster oocyte(hamster-ICSI assay): a test for fertilizing capacity of the severe male-factor sperm. I. Assist. Reprod.Genet. 13, 647–51.CrossRefGoogle ScholarPubMed
Ball, E.H. & Singer, S.J. (1982). Mitochondria are associated with microtubules and not with intermediate filaments in cultured fibroblasts. Proc. Natl. Acad. Sci. USA 79, 123–6.CrossRefGoogle Scholar
Bartoov, B. & Fisher, J. (1980). Uniqueness of sperm mtDNA as compared to somatic mtDNA in ram. Int. J. Androl. 3, 594–601.CrossRefGoogle ScholarPubMed
Becker, W.M. (1983). Aerobic production of ATP: electron transport. Biochemistry, ed. Zubay, G.L., pp. 363–407. Reading, Mass.: Addison-Wesley.Google Scholar
Dallman, P.R. & Goodman, G.R. (1970). Enlargement of mitochondrial compartment in iron and copper deficiency. Blood 35, 496–505.CrossRefGoogle ScholarPubMed
Dawid, I.B. & Blackler, A.W. (1972). Maternal and cytoplasmic inheritance of mitochondrial DNA in Xenopus. Dev. Biol. 29, 152–61.CrossRefGoogle ScholarPubMed
De Martino, C., Floridi, A., Marcante, M.L., Malroni, W., Scorza Barcellona, P., Belocci, M. & Silverstrini, B. (1979). Morphological, histochemical and biochemical studies on germ cell mitochondria of normal rats. Cell Tissue Res. 196, 1–22.CrossRefGoogle ScholarPubMed
Fawcett, D.W. (1970). A comparative view of sperm ultrastructure. Biol. Reprod. (Suppl.) 2, 90–127.CrossRefGoogle ScholarPubMed
Fawcett, D.W. (1975). The mammalian spermatozoon. Dev. Biol. 44, 394–436.CrossRefGoogle ScholarPubMed
Francisco, J.F. & Simpson, M.V. (1972). The occurrence of two types of mitochondria; DNA in rat populations as detected by Eco RI endonuclease analysis. FEBS Lett. 79, 291–4.CrossRefGoogle Scholar
Giles, R.E., Blanc, H., Cann, H.M. & Wallace, D.C. (1980). Maternal inheritance of human mitochondrial DNA. Proc. Natl. Acad. Sci. USA 77, 6715–19.CrossRefGoogle ScholarPubMed
Hackenbrock, C.R. (1968). Ultrastructure basis for metabolically linked mechanical activity of mitochondria.II. Electron transport linked ultrastructural transformations in mitochondria. J. Cell Biol. 37, 345–69.CrossRefGoogle Scholar
Handyside, A.H. & Hunter, S. (1984). A rapid procedure for visualising the inner cell mass and trophectoderm nuclei of mouse blastocyst in situ using polynucleotide-specific fluorochromes. J. Exp. Zool. 231, 429–34.CrossRefGoogle ScholarPubMed
Hecht, N.B. & Bradley, F.M. (1981). Changes in mitochondrial protein composition during testicular differentiation in mouse and bull. Gamete Res. 4, 433–49.CrossRefGoogle Scholar
Hecht, N.B., Liem, H., Kleene, K.C., Distel, R.J. & Ho, S.-M. (1984). Maternal inheritance of the mouse mitochondria genome is not mediated by a loss or gross alteration of the paternal mitochondrial DNA or by methylation of the oocyte mitochondria DNA. Dev. Biol. 102, 452–61.CrossRefGoogle ScholarPubMed
Hiraoka, J. & Hirao, Y. (1988). Fate of sperm tail components after incorporation into the hamster eggs. Gamete Res. 19, 369–80.CrossRefGoogle Scholar
Hutchison, C.A., Newbold, J.E., Potter, S.S. & Edgell, M.H. (1974). Maternal inheritance of mammalian mitochondrial DNA. Nature 251, 536–8.CrossRefGoogle ScholarPubMed
Kaneda, H., Hayashi, J.-I., Takahama, S., Taya, C. & Lindahl, K.F. (1995). Elimination of paternal mitochondria in intra specific crosses during early mouse embryogenesis. Proc. Natl. Acad. Sci. USA 92, 4542–6.CrossRefGoogle Scholar
Kroon, A.M., Devos, W.M. & Bakker, H. (1978). The heterogeneity of rat liver mitochondria DNA. Biochim.Biophys. Acta 519, 269–73.CrossRefGoogle Scholar
Kuretake, S., Kimura, Y., Hoshi, K. & Yanagimachi, R. (1996). Fertilization and development of mouse oocytes injected with isolated sperm heads. Biol. Reprod. 55, 789–95.CrossRefGoogle ScholarPubMed
Laipis, P., Choi, T., Jaenisch, R., Lindahl, K.F. & Loveland, B. (1990). J.Cell Biochem. (suppl.) 14A, 352.Google Scholar
Papaioannou, V.E. & Ebert, K.M. (1988). The preimplantation pig embryo: cell numberand allocation to trophectoderm and inner cell mass of the blastocyst in vivo and in vitro. Development 102, 793–803.CrossRefGoogle Scholar
Phillips, D.M. (1977). Mitochondrial disposition in mammalian spermatozoa. J. Ultrastruct. Res. 58, 144–54.CrossRefGoogle Scholar
Sacktor, B. & Shimada, Y. (1972). Degenerative changes in the mitochondria of flight muscle from aging blowflies. J. Cel Biol. 52, 465–77.CrossRefGoogle ScholarPubMed
Schnaitman, C. & Greenawalt, J.W. (1968). Enzymatic properties of the inner and outer membrane of rat liver mitochondria. J. Cell Biol. 38, 158–75.CrossRefGoogle ScholarPubMed
Shalgi, R., Magnus, A., Jones, R. & Phillips, D.M. (1994). Fate of sperm organelles during early embryogenesis in the rat. Mol. Reprod. Dev. 37, 264–71.CrossRefGoogle ScholarPubMed
Sutovsky, P., Navara, C.S. & Schatten, G. (1996). Fate of the sperm mitochondria, and the incorporation, conversion, and disassembly of the sperm tail structures during bovine fertilization. Biol. Reprod. 55, 1195–205.CrossRefGoogle ScholarPubMed
Tandler, B., Erlandson, R.A. & Wynder, E.L. (1968). Riboflavin and mouse hepatic cell structure and function.I. Ultrastructural alterations in simple deficiency. Am. I. Pathol. 52, 69–96.Google ScholarPubMed
Zamboni, L. (1992). Sperm structure and its relevance to infertility. Arch. Pathol. Lab. Med. 116, 325–44.Google ScholarPubMed