Skip to main content
  • La Fecondation par Micro-Injection des Spermatides: Problemes Resolus, Questions Posees
  • Published:

La spermatide, cette méconnue

The spermatid, an unrecognized germ cell

Resume

L'usage de la micro-insémination ovocytaire de spermatides rondes ou allongées, dans certains cas d'infertilité masculine, nécessite de reconsidérer la séquence des modifications morphologiques et fonctionnelles qui surviennent durant la spermiogenèse. Cet article a pour objet de passer en revue les acquisitions essentielles sur la morphogenèse des spermatides, l'expression du génome au cours de la différenciation des spermatozoïdes et les interactions cellulaires entre les spermatides elles-mêmes et entre les spermatides et les cellules de Sertoli. Il apparaît que les spermatides rondes et les spermatides allongées représentent deux classes de cellules structuralement et fonctionnellement différentes. Une interrogation demeure: sur quels critères peut-on affirmer qu'une spermatide ronde est fonctionnellement normale quand il y a arrêt ou altération de la spermiogenèse?

Abstract

The use of microinsemination of round or elongated spermatids into ovocytes, in certain cases of male infertility, requires re-examination of the sequence of morphological and functional changes that occur throughout spermiogenesis. This paper reviews essential findings on morphogenesis of spermatids, genome expression during sperm differentiation and cellular interactions between spermatids themselves and between spermatids and Sertoli cells. Round and elongated spermatids appear to represent two classes of structuraly and functionnaly different cells. One question remains: on what criteria can one claim that a round spermatid functions normally when spermiogenesis is blocked or impaired?

References

  1. Ariel M., Cedar H., Mc. Carrey J.: Developmental changes in methylation of spermatogenesis. specific genes include reprogramming in the epididymis. Nature Gen. 1994, 7, 59–63.

    Article  CAS  Google Scholar 

  2. Auger J., Dadoune J.P.: Nuclear status of human sperm cells by transmission electron microscopy and image cytometry: Changes in nuclear shape and chromatin texture during spermiogenesis and epididymal transit. Biol. Reprod., 1993, 49, 166–175.

    Article  PubMed  CAS  Google Scholar 

  3. Balhorn R.: Mammalian protamines: Structure and molecular interaction. In: Molecular Biology of Chromosome Function Adolph K.W., ed., Springer, New York, 1989, 366–395.

    Google Scholar 

  4. Baskaran R., Rao M.R.S.: Interaction of spermatid specific protein TP2 with nucleic acids in vitro. A comparative study with TP1. J. Biol. Chem., 1990, 265, 21039–21047.

    PubMed  CAS  Google Scholar 

  5. Bellvé A.R., O'Brien D.A.: The mammalian spermotozoon: Structure and temporal assembly. In: Mechanism and control of animal fertilization, Hartman J.F., ed. Academic Press, New York, 1983, p.p. 55–137.

    Google Scholar 

  6. Blendy J.A., Kaestner K.H., Weinbauer G.F., Nieschlag E., Schutz G.: Severe impairment of spermatogenesis in mice lacking the CREM gene. Nature, 1996, 380, 162–165.

    Article  PubMed  CAS  Google Scholar 

  7. Boutinard Rouelle Rossier V., Biggiogera M., Fakan S.: Ultrastructure detection of calcium and magnesium in the chromatoid body of mouse spermatids by electron spectroscopic imaging and electron energy loss spectroscopy. J. Histochem. Cytochem. 1993, 41, 1155–1162.

    Google Scholar 

  8. Branca A.: Les canalicules testiculaires et spermatogenèse de l'homme. Arch. Zool. Exp. Gen. 1924, 62, 53–252.

    Google Scholar 

  9. Braun R.E., Keesook L., Schumacher J.M., Farjardo M.A.: Molecular genetic analysis of mammalian spermatid differentiation. Recent Progress in Hormone Research, 1995, 50, 275–286.

    PubMed  CAS  Google Scholar 

  10. Caldwell K.A., Handel M.A.: Protamine transcript sharing among post-meiotic spermatids. Proc. Natl. Acad. Sci. U.S.A., 1991, 88, 2407–2411.

    Article  PubMed  CAS  Google Scholar 

  11. Clermont Y.: The cycle of the seminiferous epithelium in man. Amer. J. Anat., 1963, 112, 35–51.

    Article  PubMed  CAS  Google Scholar 

  12. Concha I.I., Urzua U., Yanez A., Schroeder R., Pessot C., Burzio L.O.: U1 and U2 snRNA are localized in the sperm nucleus. Exp. Cell. Res., 1993, 204, 378–381.

    Article  PubMed  CAS  Google Scholar 

  13. Courtens J.L., Biggiogera M., Rothfield N.F., Burnier M., Fakan S.: Migration of centromere proteins in rabbit spermatids. Molec., Reprod. Dev., 1992, 32, 369–377.

    Article  CAS  Google Scholar 

  14. Dadoune J.P.: The nuclear status of human sperm cells. Micron, 1995, 26, 323–345.

    Article  PubMed  CAS  Google Scholar 

  15. Dadoune J.P., Alfonsi M.F.: Ultrastructural and cytochemical changes of the head components of human spermatids and spermatozoa. Gamete Res., 1986, 14, 33–46.

    Article  Google Scholar 

  16. Dadoune J.P., Alfonsi M.F., Fain-Maurel M.A.: Cytochemical variations in the nucleolus during spermiogenesis in man and monkey. Cell. Tissue Res., 1991, 264, 167–173.

    Article  PubMed  CAS  Google Scholar 

  17. Dadoune J.P., Siffroi J.P., Alfonsi M.F.: Ultrastructure localization of rDNA and rRNA by in situ hybridization in the nucleolus of human spermatids. Cell Tissue Res., 1994, 278, 611–616.

    Article  PubMed  CAS  Google Scholar 

  18. Domenjoud L., Nussbaum G., Adham I.M., Greeske G., Engel W.: Genomic sequences of human protamines whose genes, PRM1 and PRM2, are clustered. Genomics, 1990, 8, 127–133.

    Article  PubMed  CAS  Google Scholar 

  19. Domenjoud L., Kremling H., Burfeind P., Maeir W.M., Engel W.: On the expression of protamine genes in the testis of man and other mammals. Andrologia, 1991, 23, 333–337.

    PubMed  CAS  Google Scholar 

  20. Delmas V., Van Der Hoorn F., Mellström B., Jegou B., Sassone-Corsi P.: Induction of CREM activator proteins in spermatid: Downstream targets and implications for haploïd germ cell differentialon. Molec. Endocrinol., 1993, 7, 2502–2513.

    Article  Google Scholar 

  21. Engel W., Keime S., Kremling H., Hameister H., Schlüter G.: The Genes for protamines 1 and 2 (PRM1 and PRM2) and transition protein 2 (TNP2) are closely linked in the mammalian genome. Cytogenet. Cell. Genet., 1992, 61, 158–159.

    Article  PubMed  CAS  Google Scholar 

  22. Fishel S.: Pregnancy after intracytoplasmic injection of spermatid. Lancet, 1995, 245, 1641–1642.

    Article  Google Scholar 

  23. Hannay T.: New Japanese IVF method finally made available in Japan. Nature Med., 1995, 1, 289–290.

    Article  CAS  Google Scholar 

  24. Hecht N.B.: Molecular biology of structural proteins of the mammalian testis. In: Molecular Biology of Chromosome Function. Adolph K.W., ed., Springer, New York, 1989, p.p. 396–420.

    Google Scholar 

  25. Hecht N.B.: Gene expression during spermiogenesis. In: Cellular and Molecular Events in Spermiogenesis, Hamilton, D.W. and Waites, G.M.H. eds, Cambridge University Press, 1990, p.p. 265–283.

  26. Heller C.G., Clermont Y.: Spermatogenesis in man: an estimate of its duration. Science, 1963, 140, 184–186.

    Article  PubMed  CAS  Google Scholar 

  27. Heller C.G., Clermont Y.: Kinetics of the germinal eptithelium in man: Rec., Prog., Horm. Res, 1964, 20, 545–575.

    CAS  Google Scholar 

  28. Holstein A.F., Roosen-Runge E.C.: Atlas of Human Spermatogenesis. Grosse-Verlag, Berlin, 1981.

    Google Scholar 

  29. Jegou B., Syed V., Sourdaine P., Byers St, Gerard N., Vellez De La Calle J., Pineau Ch., Garnier D.H., Bauchi F.: The dialogue between late spermatids and Sertoli cells in vertebrates: A century research. In: Nieschlag E., Habenicht U.F. eds, Spermatogenesis, Fertilization, Contraception, Springer-Verlag, Berlin, Heidelberg, 1992, p.p. 57–95.

    Google Scholar 

  30. Le Lannic G., Arkhis A., Vendrely E., Chevaillier P., Dadoune J.P.: Production, characterization, and immunocytochemical applications of monoclonal antibodies to human sperm protamines. Molec. Reprod. Dev., 1993, 36, 106–112.

    Article  PubMed  Google Scholar 

  31. Luerssen H., Hoyer-Fender S., Engel W.: The nucleotide sequence of human transition protein 1 cDNA. Nucleic Acids. Res., 1988, 16, 7723.

    Article  PubMed  CAS  Google Scholar 

  32. Luerssen H., Mattei M.G., Schröter M., Grzeschik K.H., Adham I.M., Engel W.: Nucleotide sequence of the gene for human transition protein1 and its chromosomal localization on chromosome 2. Genomics, 1990, 8, 324–330.

    Article  PubMed  CAS  Google Scholar 

  33. McPherson S.M., Longo F.J.: Localization of DNAse I-Hypersensitive regions during rat spermatogenesis: Stage-dependent patterns and unique sensitivity of elongating spermatids. Molec. Reprod. Dev., 1992, 31, 268–279.

    Article  PubMed  CAS  Google Scholar 

  34. Moss S.B., Burnham B.L., Bellvé A.R.: The differential expression of lamin epitopes during mouse spermatogenesis. Molec. Reprod. Dev., 1993, 34, 164–174.

    Article  PubMed  CAS  Google Scholar 

  35. Nantel F., Monaco L., Foulkes N.S., Masquilier D., Le Meur M., Henriksen K., Dierich A., Parvinem M., Sassone-Corsi P.: Spermiogenesis deficiency and germ-cell apoptosis in CREM. mutant mice. Nature, 1996, 380, 159–162.

    Article  PubMed  CAS  Google Scholar 

  36. Navara Ch. S., Simerly C., Zoran S., Schatten G.: The sperm centrosome during fertilization in mammals: Implications for fertility and reproduction. Reprod. Fertil., Dev., 1995, 7, 747–754.

    Article  CAS  Google Scholar 

  37. Oliva R.F., Dixon G.H.: Vertebrate protamine genes and the histone-to-protamine replacement reaction. Prog. Nucleic Acids Res. Mol. Biol., 1991, 40, 25–94.

    Article  CAS  Google Scholar 

  38. Parrington J., Swann K., Shevchenko V.I., Sesay A.K., Lai F.A.: Calcium oscillations in mammalian eggs triggered by a soluble, sperm protein. Nature, 1996, 379, 364–368.

    Article  PubMed  CAS  Google Scholar 

  39. Parvinen M., Mali P.: The chromatoid body in early spermatids: Its dependence on haploid gene expression and cytoplasmic microtubules. In: Cellular and Molecular Events in Spermiogenesis, Hamilton, D.W. Waites, G.M.H. eds, Cambridge University Press, Cambridge, 1990, p.p. 257–264.

    Google Scholar 

  40. Peterson K., Sapienza C.: Imprinting the genome: Imprinted genes, imprinting genes and a hypothesis for their interaction. Annu. Rev. Genet., 1993, 27, 7–31.

    Article  PubMed  CAS  Google Scholar 

  41. Piquet-Pellorce C., Gomez E., Cudicini C., Stephan J.P., Dejucq N., Jegou B.: Cytokines and spermatogenesis. In: Fertility and Sterility. A current overview. Proceedings of the 15 th World Congress on Fertility and Sterility, Montpellier France. HEDON B., BRINGER J., MARES P., eds, The Parthenon Publishing Group, New-York, London, 1995, p.p. 249–255.

    Google Scholar 

  42. Prigent Y., Muller S., Dadoune J.P.: Immunoelectron distribution of histones H2B and H3 and protamines during human spermiogenesis. Molec. Human Reprod. (sous presse).

  43. Roux Ch., Mathieson J., Dadoune J.P.: Localisation immunocytologique des protamines du groupe HP1 dans le testicule humain et le spermatozoïde éjaculé. Bull. Assoc. Anat., 1987, 71, 65–69.

    CAS  Google Scholar 

  44. An antiserum against protamines for immunohistochemical studies of histone to protamine transition during human spermiogenesis. J. Reprod. Fert., 1988, 82, 35–42.

  45. Schlüter G., Kremling H., Engel W.: The gene for human transition protein 2: Nucleotide sequence, assignment to the protamine gene cluster, and evidence for its low expression. Genomics, 1992, 14, 377–383.

    Article  PubMed  Google Scholar 

  46. Schumacher J.M., Lee K., Edelhoff S., Braun R.E.: Spnr, a murine RNA binding protein that is localized to cytoplasmic microtubules. J. Cell. Biol., 1995, 129, 1023–1032.

    Article  PubMed  CAS  Google Scholar 

  47. Schoysman R., Lejeune B., Van Roosendaal E., Segal L., Vanderzwalmen P., Nijs M., Vandamme B., Bertin G.: La procréation médicalement assistée avec spermatozoïdes immatures: Impératifs cliniques et techniques chirurgicales. Andrologie, 1996, 6, no 4, 432–439

    Article  Google Scholar 

  48. Siffroi J.P., Straub B., Alfonsi M.F., Dadoune J.P.: Ultrastructural localization of the mRNAS of protamines 1 and 2 in human spermatids. Molec. Reprod. Dev. (soumis pour publication).

  49. Szabo P.E., Mann J.R.: Biallelic expression of imprinted genes in the mouse germ line: Implications for erasure, establishement, and mechanisms of genomic imprinting genes, 1995, 9, 1857–1868.

    CAS  Google Scholar 

  50. Tesarik J., Mendoza C, Testart J.: Viable embryos from injection of round spermatids into ovocytes. N. Eng. J. Med., 1995, 333, 525.

    Article  CAS  Google Scholar 

  51. Tesarik J., Rolet F., Brami C., Sedbon E., Thorel J., Tibi C., Thebault A.: Spermatid injection into human ovocytes. II. Clinical application in the treatment of infertility due to non-obstructive azoospermia. Human Reprod., 1996, 11, 780–783.

    CAS  Google Scholar 

  52. Tres J.L., Kierszenbaum A.L.: Sak 57, an acidic keratin initially present in the spermatid manchette before becoming a component of paraxonemal structures of the developing tail. Molec. Reprod. Dev. 1996, 44, 395–407.

    Article  PubMed  CAS  Google Scholar 

  53. Unni E., Meistrich M.L.: Purification and characterization of the rat spermatid basic nuclear protein TP4. J. Biol. Chem., 1992, 267, 25359–25363.

    PubMed  CAS  Google Scholar 

  54. Unni E., Zhang Y., Kangasniemi M., Saperstein W., Moss S.B., Meistrich M.L.: Stage-specific distribution of the spermatid-specific histone 2B in the rat testis. Biol. Reprod, 1995, 53, 820–826.

    Article  PubMed  CAS  Google Scholar 

  55. Vanderzwalmem P., Lejeune B., Nijs M., Segal-Bertin G., Vandamme B., Schoysman R.: Fertilization of an ovocyte microinseminated with a spermatid in an in vitro fertilization programme. Human Reprod., 1995, 10, 502–503.

    Google Scholar 

  56. Viguié F., Domenjoud L., Rousseau-Merck F., Dadoune J.P., Chevaillier P.: Chromosomal localization of the human protamine genes, PRM1 et PRM2, to 16p13.3, by in situ hybridization. Hum. Genet., 1990, 85, 171–174.

    Article  PubMed  Google Scholar 

  57. Villar A.J., Eddy E.M., Pedersen R.A.: Developmental regulation of genomic impriving during garmetogenesis. Develop. Biol. 1995, 172, 264–271.

    Article  PubMed  CAS  Google Scholar 

  58. Von La Valette, St George A.J.H.: Spermatologische Beitrage. Arch. Mikrosk. Anat., 1885, 25, 581–593.

    Article  Google Scholar 

  59. Ward W.S., Coffey D.S.: DNA packaging and organization in mammalian spermatozoa: Comparison with somatic cells. Biol. Reprod., 1991, 44, 569–574.

    Article  PubMed  CAS  Google Scholar 

  60. Willison K., Ashworth A.: Mammalian spermatogenic gene expression. Trends Genet. 1987, 3, 351–355.

    Article  Google Scholar 

  61. Winer M.A., Wolgemuth D.J.: Patterns of expression and potential functions of proto-oncogenes during mammalian spermatogenesis. In: Molecular Biology of the Male Reproductive System, De Kretser D. ed, Academic Press, New York, 1993, p.p. 96–113.

    Google Scholar 

  62. Wykes S.M., Nelson J.E., Visscher D.W., Djakiew D., Krawetz S.A.: Coordinate expression of the PRM1, PRM2, and TNP2 multigene locus in human testis. DNA Cell. Biol., 1995, 14, 155–161.

    Article  PubMed  CAS  Google Scholar 

  63. Zalensky A.O., Breneman J.W., Zalenskaya I.A., Brinkley B.R., Bradbury E.M.: Organization of centromeres in the decondensed nuclei of mature human sperm chromosoma, 1993, 102, 509–518.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dadoune, J.P. La spermatide, cette méconnue. Androl. 7, 22–33 (1997). https://doi.org/10.1007/BF03034517

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03034517

Mots clés

Key words