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Paternal Centrosomal Dynamics in Early Human Development and Infertility

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Abstract

Purpose: Our purpose was to demonstrate the dynamics of the human sperm centrosome during fertilization and cleavage.

Methods: Human gametes, fertilized oocytes, and preimplantation embryos were examined by transmission electron microscopy.

Results: The functional sperm centrosome containing a typical centriole (proximal) is inherited at fertilization and forms a sperm monoaster. It then replicates and is perpetuated during cleavage. It organizes the mitotic apparatus at each stage of cleavage up to the hatching blastocyst stage. Bipolar spindles are formed in all monospermic and most dispermic embryos. Occasionally, two sperm asters and tripolar spindles are formed in dispermic embryos. Centrioles are associated with pronuclei and nuclei at interphases when they duplicate and occupy pivotal positions at spindle poles during mitoses. The maternal centrosome is not functional.

Conclusions: The human embryo shows paternal centrosome inheritance and perpetuation like most other animals. Inheritance of defective centrosomes may lead to abnormal cleavage and contribute to infertility.

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REFERENCES

  1. Sathananthan AH, Kola I, Osborne J, Trounson A, Ng SC, Bongso A, Ratnam SS: Centrioles in the beginning of human development. Proc Natl Acad Sci USA 1991;88:4806–4810

    Google Scholar 

  2. 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

    Google Scholar 

  3. Boveri T: Ueber die “Befruchtung der Eier von Ascaris megalocephala.” Jena, Germany, Fischer, 1887

    Google Scholar 

  4. Boveri T: Zellen-Studien: Ueber die natur der centrosomen, IV. Jena, Germany, Fischer, 1901

    Google Scholar 

  5. Sathananthan AH, Ratnam SS, Ng SC, Tarin JJ, Gianaroli L, Trounson A: The sperm centriole: Its inheritance, replication and perpetuation in early human embryos. Hum Reprod 1996;11:345–356

    Google Scholar 

  6. Sathananthan AH: Mitosis in the human embryo: The vital role of the sperm centrosome (centriole). Histol Histopathol 1997;12:827–856

    Google Scholar 

  7. Sathananthan AH: Inheritance of paternal centrioles and male infertility. XIIIth World Congress of Obsterics and Gynaecology, Singapore, Abstr No. 1629

  8. Sathananthan AH: Centriole behavior during fertilization in humans. In Satellite Symposium on Inheritance Patterns During Fertilization, Society for Developmental Biology, Washington, USA

  9. Sathananthan AH: Functional competence of abnormal spermatozoa. In Bailliere's Clinical Obstetrics and Gynaecology—Micromanipulation techniques, S Fishel (ed). London, Bailliere Tindall, 1994, pp 141–156

    Google Scholar 

  10. Sathananthan AH: The paternal centrosome: Its role in human embryonic development and infertility (A recent discovery) In Current Issues in Obstetrics and Gynaecology, S Arulkumaran, S Ng (eds). Oxford, Oxford University Press, 1996, pp 101–115

    Google Scholar 

  11. Sathananthan AH: Ultrastructure of fertilization and embryo development. In A Trounson, DK Gardner (eds). Boca Raton, FL, CRC Press, 1993, pp 237–261

    Google Scholar 

  12. Simerly C, Wu GJ, Zoran S, Ord T, Rawlins R, Jones J, Navara C, Gerrity M, Rinehart J, Binor Z, Asch R, Schatten G: The paternal inheritance of the centrosome, the cell's microtubule—organizing centre, in humans, and the implications for infertility. Nature Med 1995;1:47–52

    Google Scholar 

  13. Holstein AF, Roosen-Runge EC: Atlas of Human Spermatogenesis. Berlin, Grosse Verlag

  14. de Kretser DM, Kerr JB: The cytology of the testis. In The Physiology of Reproduction, 2nd ed. E Knobil, JD Neill (eds). New York, Raven Press, 1994, pp 1177–1290

    Google Scholar 

  15. Wheatley DN: The Centriole: A Central Enigma of Cell Biology. Amsterdam, Elsevier, 1982

    Google Scholar 

  16. Brinkley BR: Microtubule organizing centers. Annu Rev Cell Biol 1985;1:145–172

    Google Scholar 

  17. Mazia D: The chromosome cycle and the centrosome cycle in the mitotic cycle. Int Rev Cytol 1987;100:49–92

    Google Scholar 

  18. Kalnins VI: The Centrosome. New York, Academic Press, 1992

    Google Scholar 

  19. Sathananthan AH: Ultrastructural changes during meiotic maturation in mammalian oocytes: Unique aspects of the human oocyte. Microsc Res Tech 1994;27:145–164

    Google Scholar 

  20. Sathananthan AH, Ng SC, Bongso A, Trounson A, Ratnam S: Visual Atlas of Early Human Development for Assisted Reproductive Technology. Singapore, Serono, 1993

    Google Scholar 

  21. Sathananthan AH, Kirby C, Trounson A, Philipatos D, Shaw J: The effects of cooling mouse oocytes. J Assist Reprod Genet 1992;9:139–148

    Google Scholar 

  22. Szöllösi D, Calarco PG, Donohue RP: Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J Cell Sci 1972;11:521–541

    Google Scholar 

  23. Sathananthan AH, Tatham B, Lewis L, Trounson A: Inheritance of sperm centrioles in bovine embryos. XIth Annual Meeting of the Fertility Society of Australia. Adelaide, 1992

  24. Le Guen P, Crozet N: Microtubule and centrosome distribution during sheep fertilization. Eur J Cell Biol 1989;48:239–249

    Google Scholar 

  25. Crozet N: Behavior of the sperm centriole during sheep oocyte fertilization. Eur J Cell Biol 1990;53:321–332

    Google Scholar 

  26. Long CR, Pinto-Correia C, Duby R, Ponce de Leon F, 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

    Google Scholar 

  27. Navara C, First N, 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

    Google Scholar 

  28. Breed W, Simerly C, Navara C, Vande Berg, Schatten G: Distribution of microtubules in eggs and early embryos of marsupial, Monodelphis domestica. Dev Biol 1994;164:230–240

    Google Scholar 

  29. Hewitson LC, Simerly C, Tengowski MW, Sutovsky P, Navara C, Haavisto A, Schatten G: Microtubule and DNA configurations during rhesus intracytoplasmic sperm injection: Successes and failures. Biol Reprod 1997 (in press)

  30. Sathananthan AH, Lyons G, Dharmawardena V, Tatham B, Pushett D, Trounson A: The paternal centriole: Its replication and perpetuation in early bovine embryos (in press)

  31. Paweletz N, Mazia D: The fine structure of the formation of mitotic poles in fertilized eggs. In The Cell Biology of Fertilization, H Schatten, G Schatten (eds). San Diego, Academic Press, 1989, pp 165–187

    Google Scholar 

  32. Zoran S, Simerly C, Schoff P, Stearns T, Salisbury J, Schatten G: Reconstitution of the human sperm centrosome, in vitro. Mol Biol Cell 1994;5:38a

    Google Scholar 

  33. Van Blerkom J, Davis P: Evolution of the sperm aster after microinjection of isolated human sperm centrosomes into meiotically mature human oocytes. Hum Reprod 1995;10:2179–2182

    Google Scholar 

  34. Van Blerkom J, Davis P, Merriam J, Sinclair J: Nuclear and cytoplasmic dynamics of sperm penetration, pronuclear formation and microtubule organization during fertilization and early preimplantation development in the human. Hum Reprod Update 1995;1:429–461

    Google Scholar 

  35. Winston N, Johnson M, Pickering S, Braude P: Parthenogenetic activation and development of fresh and aged human oocytes. Fertil Steril 1991;56:904–912

    Google Scholar 

  36. Palermo G, Munné S, Cohen J: The human zygote inherits its mitotic potential from the male gamete. Hum Reprod 1994;9:1220–1225

    Google Scholar 

  37. Plachot M: Cytogenetic analysis of oocytes and embryos. Ann Acad Med 1992;21:538–544

    Google Scholar 

  38. Sathananthan AH: Abnormal nuclear configurations encountered in human IVF and possible genetic implications. Assist Reprod Tech/Androl 1990;1:115–133

    Google Scholar 

  39. Sathananthan AH (Ed): Visual Atlas of Sperm Structure and Function for Assisted Reproductive Technology. Singapore, Serono, 1996

    Google Scholar 

  40. Hancock AD, de Kretser DM: The axonemal ultrastructure of spermatozoa from men with asthenospermia. Fertil Steril 1992;57:661–664

    Google Scholar 

  41. Asch R, Simerly C, Ord T, Ord VA, Schatten G: The stages at which human fertilization arrests: Microtubule and chromosome configurations in inseminated oocytes which failed complete fertilization and development in humans. Hum Reprod 1995;10: 1879–1906

    Google Scholar 

  42. Navara C, First N, Schatten G: Individual bulls affect sperm aster size and quality: Relationship between the sperm centrosome and development. Mol Biol Cell 1993;4:828a

    Google Scholar 

  43. Zamboni L, Stefanini M: The fine structure of the neck of mammalian spermatozoa. Anat Rec 1970;169:155–172

    Google Scholar 

  44. Sathananthan AH, Chen C: Sperm-oocyte membrane fusion in the human during monospermic fertilisation. Gamete Res 1986;15:177–186

    Google Scholar 

  45. Sathananthan AH, Ng SC, Edirisinge R, Ratnam SS, Wong PC: Sperm-oocyte interaction in the human during polyspermic fertilisation in vitro. Gamete Res 1986;15:317–326

    Google Scholar 

  46. Nagy ZP, Lui J, Joris H, Verheyen G, Tournaye H Camus M, Derde MP, Devroey P, Van Steirteghem AC: The result of intracytoplasmic sperm injection is not related to any of the three basic sperm parameters. Hum Reprod 1995;10:1123–1129

    Google Scholar 

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Authors and Affiliations

  1. La Trobe and Monash Universities, Melbourne, Australia

    A. Henry Sathananthan

  2. National University Hospital, Singapore

    A. Henry Sathananthan

  3. Institute of Reproduction & Development, Monash Medical Centre, 276 Clayton Road, Clayton, Victoria 3168, Australia

    A. Henry Sathananthan

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  1. A. Henry Sathananthan
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Sathananthan, A.H. Paternal Centrosomal Dynamics in Early Human Development and Infertility. J Assist Reprod Genet 15, 129–139 (1998). https://doi.org/10.1023/A:1023056804548

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