Advertisement

The Testis pp 43-54 | Cite as

Regulation of the Differentiation of the Undifferentiated Spermatogonia

  • Dirk G. de Rooij
  • Bianca H. G. J. Schrans-Stassen
  • Ans M. M. van Pelt
  • Gladis A. Shuttlesworth
  • Marvin L. Meistrich
  • Masaru Okabe
  • Yoshitake Nishimune
Part of the Serono Symposia USA book series (SERONOSYMP)

Abstract

In the seminiferous epithelium of adult nonprimate mammals, so-called A-single (As) spermatogonia are the stem cells of spermatogenesis (1–3). Upon division of the As spermatogonia, the daughter cells either migrate away from each other and become two new stem cells, or the cells stay together becoming A-paired (Apr) spermatogonia connected by an intercellular bridge. About half of the stem-cell population normally divides to form Apr spermatogonia, whereas the other half goes through self-renewing divisions, thereby maintaining stem-cell numbers (Fig. 5.1).

Keywords

Sertoli Cell Stem Cell Factor Seminiferous Epithelium Spermatogonial Stem Cell Intercellular Bridge 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Huckins C. The spermatogonial stem cell population in adult rats. I. Their mor¬phology, proliferation and maturation. Anat Rec 1971; 169: 533 – 57.PubMedCrossRefGoogle Scholar
  2. 2.
    Oakberg EF . Spermatogonial stem-cell renewal in the mouse. Anat Rec 1971; 169:515–31.PubMedCrossRefGoogle Scholar
  3. 3.
    de Rooij DG . Proliferation and differentiation of undifferentiated spermatogonia in the mammalian testis. In: Potten CS, ed. Stem cells. Their identification and characterization. Edinburgh: Churchill Livingstone, 1983.89–117.Google Scholar
  4. 4.
    Russell LD, Ettlin RA, Hikim APS, Clegg ED. Histological and histopathological evaluation of the testis. Clearwater, FL: Cache River Press, 1990.Google Scholar
  5. 5.
    Lok D, de Rooij DG. Spermatogonial multiplication in the Chinese hamster. III. Labelling indices of undifferentiated spermatogonia throughout the cycle of the seminiferous epithelium. Cell Tissue Kinet 1983;16:31–40.PubMedGoogle Scholar
  6. 6.
    Lok D, Weenk D, de Rooij DG. Morphology, proliferation, and differentiation of undifferentiated spermatogonia in the Chinese hamster and the ram. Anat Rec 1982;203:83–99.PubMedCrossRefGoogle Scholar
  7. 7.
    Tegelenbosch RA, de Rooij DG. A quantitative study of spermatogonial multipli¬cation and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res 1993;290:193–200.PubMedGoogle Scholar
  8. 8.
    de Rooij DG . Stem cells in the testis. Int J Exp Pathol 1998;79:67–80.PubMedCrossRefGoogle Scholar
  9. 9.
    van Beek ME, Meistrich ML, de Rooij DG. Probability of self-renewing divisions of spermatogonial stem cells in colonies, formed after fission neutron irradiation. Cell Tissue Kinet 1990;23:1–16.PubMedGoogle Scholar
  10. 10.
    van Beek ME, Davids JA, van de Kant HJ, de Rooij DG. Response to fission neutron irradiation of spermatogonial stem cells in different stages of the cycle of the seminiferous epithelium. Radiat Res 1984;97:556–69.PubMedCrossRefGoogle Scholar
  11. 11.
    van Pelt AM, de Rooij DG. The origin of the synchronization of the seminiferous epithelium in vitamin A-deficient rats after vitamin A replacement. Biol Reprod 1990;42:677–82.PubMedCrossRefGoogle Scholar
  12. 12.
    van Pelt AM, van Dissel-Emiliani FM, Gaemers IC, van der Burg MJ, Tanke HJ, de Rooij DG. Characteristics of A spermatogonia and preleptotene spermatocytes in the vitamin A-deficient rat testis. Biol Reprod 1995;53:570–78.PubMedCrossRefGoogle Scholar
  13. 13.
    de Rooij DG, van Pelt AMM, van de Kant HJG, van der Saag PT, Peters AHFM, Heyting C, et al. Role of retinoids in spermatogonial proliferation and differentiation and the meiotic prophase. In: Bartke A, ed. Function of somatic cells in the testis. New York: Springer Verlag, 1994:345–61.Google Scholar
  14. 14.
    Nishimune Y, Haneji T. Testicular DNA synthesis in vivo: comparison between unilaterally cryptorchid testis and contralateral intact testis in mouse. Arch Androl 1981;6:61–65.PubMedCrossRefGoogle Scholar
  15. 15.
    Nishimune Y, Haneji T, Aizawa S. Testicular DNA synthesis in vivo: changes in DNA synthetic activity following artificial cryptorchidism and its surgical reversal. Fertil Steril 1981;35:359–62.PubMedGoogle Scholar
  16. 16.
    Mizunuma M, Dohmae K, Tajima Y, Koshimizu U, Watanabe D, Nishimune Y. Loss of sperm in juvenile spermatogonial depletion (jsd) mutant mice is ascribed to a defect of intratubular environment to support germ cell differentiation. J Cell Physiol 1992;150:188–93.PubMedCrossRefGoogle Scholar
  17. 17.
    Kojima Y, Kominami K, Dohmae K, Nonomura N, Miki T, Okuyama A, et al. Cessation of spermatogenesis in juvenile spermatogonial depletion (jsd/jsd) mice. Int J Urol 1997;4:500–7.PubMedCrossRefGoogle Scholar
  18. 18.
    Beamer WG, Cunliffe-Beamer TL, Shultz KL, Langley SH, Roderick TH. Juvenile spermatogonial depletion (jsd): a genetic defect of germ cell proliferation of male mice. Biol Reprod 1988;38:899–908.PubMedCrossRefGoogle Scholar
  19. 19.
    Brannan CI, Bedell MA, Resnick JL, Eppig JJ, Handel MA, Williams DE, et al. Developmental abnormalities in Steel 17H mice result from a splicing defect in the steel factor cytoplasmic tail. Genes Dev 1992;6:1832–42.PubMedCrossRefGoogle Scholar
  20. 20.
    Boekelheide K . Rat testis during 2,5-hexanedione intoxication and recovery. II. Dynamics of pyrrole reactivity, tubulin content, and microtubule assembly. Toxicol Appl Pharmacol 1988;92:28–33.PubMedCrossRefGoogle Scholar
  21. 21.
    Allard EK, Hall SJ, Boekelheide K. Stem cell kinetics in rat testis after irreversible injury induced by 2,5-hexanedione. Biol Reprod 1995;53:186–92.PubMedCrossRefGoogle Scholar
  22. 22.
    Allard EK, Boekelheide K. Fate of germ cells in 2,5-hexanedione-induced testicu¬lar injury. II. Atrophy persists due to a reduced stem cell mass and ongoing apoptosis. Toxicol Appl Pharmacol 1996;137:149–56.CrossRefGoogle Scholar
  23. 23.
    Kangasniemi M, Huhtaniemi I, Meistrich ML. Failure of spermatogenesis to recover despite the presence of a spermatogonia in the irradiated LBNF1 rat. Biol Reprod 1996;54:1200–8.PubMedCrossRefGoogle Scholar
  24. 24.
    de Rooij DG, Okabe M, Nishimune M. Arrest of spermatogonial differentiation in jsd/jsd, Sl17H/Sl17H and cryptorchid mice. Biol Reprod 1999;61:842–47.PubMedCrossRefGoogle Scholar
  25. 25.
    Shuttlesworth GA, de Rooij DG, Huhtaniemi I, Reissmann T, Russell LD, Shetty G, et al. Enhancement of A spermatogonial proliferation and differentiation in irradiated rats by GnRH antagonist administration. Endocrinology 2000; 141: 37–49.PubMedCrossRefGoogle Scholar
  26. 26.
    Huckins C . The morphology and kinetics of spermatogonial degeneration in normal adult rats: an analysis using a simplified classification of the germinal epithelium. Anat Rec 1978;190:905–26.PubMedCrossRefGoogle Scholar
  27. 27.
    de Rooij DG . Spermatogonial stem cell renewal in the mouse. I. Normal situation. Cell Tissue Kinet 1973;6:281–87.PubMedGoogle Scholar
  28. 28.
    Erickson BH . Survival and renewal of murine stem spermatogonia following 60Co gamma radiation. Radiat Res 1981;86:34–51.PubMedCrossRefGoogle Scholar
  29. 29.
    Erickson BH, Hall GG. Comparison of stem-spermatogonial renewal and mitotic activity in the gamma-irradiated mouse and rat. Mutat Res 1983;108:317–35.PubMedGoogle Scholar
  30. 30.
    Huang HFS, Li MT, Anesetti R, Giglio W, Ottenweller JE, Pogach LM . Effects of spinal cord injury on spermatogenesis and the expression of messenger ribonucleic acid for Sertoli cell proteins in rat Sertoli cell-enriched testes. Biol Reprod 1999;60:635–41.PubMedCrossRefGoogle Scholar
  31. 31.
    van Pelt AM, van den Brink CE, de Rooij DG, van der Saag PT. Changes in retinoic acid receptor messenger ribonucleic acid levels in the vitamin A-deficient rat testis after administration of retinoids. Endocrinology 1992;131:344–40.PubMedCrossRefGoogle Scholar
  32. 32.
    Gaemers IC, van Pelt AM, van der Saag PT, Hoogerbrugge JW, Themmen AP, de Rooij DG. Effect of retinoid status on the messenger ribonucleic acid expression of nuclear retinoid receptors alpha, beta, and gamma, and retinoid X receptors alpha, beta, and gamma in the mouse testis. Endocrinology 1997;138:1544–51.PubMedCrossRefGoogle Scholar
  33. 33.
    Gaemers IC, van Pelt AM, van der Saag PT, Hoogerbrugge JW, Themmen AP, de Rooij DG. Differential expression pattern of retinoid X receptors in adult murine testicular cells implies varying roles for these receptors in spermatogenesis. Biol Reprod 1998;58:1351–56.PubMedCrossRefGoogle Scholar
  34. 34.
    Meistrich ML, Wilson G, Zhang Y, Kurdoglu B, Terry NH. Protection from procarbazine-induced testicular damage by hormonal pretreatment does not involve arrest of spermatogonial proliferation. Cancer Res 1997;57:1091–97.PubMedGoogle Scholar
  35. 35.
    Meistrich ML, Kangasniemi M. Hormone treatment after irradiation stimulates recovery of rat spermatogenesis from surviving spermatogonia. J Androl 1997; 18:80–87.PubMedGoogle Scholar
  36. 36.
    Meistrich ML . Hormonal stimulation of the recovery of spermatogenesis following chemo- or radiotherapy. Review article. Apmis 1998;106:37–45.PubMedCrossRefGoogle Scholar
  37. 37.
    Blanchard KT, Lee J, Boekelheide K. Leuprolide, a gonadotropin-releasing hormone agonist, reestablishes spermatogenesis after 2,5-hexanedione-induced irreversible testicular injury in the rat, resulting in normalized stem cell factor expression. Endocrinology 1998;139:236–44.PubMedCrossRefGoogle Scholar
  38. 38.
    Meistrich ML, Wilson G, Huhtaniemi I. Hormonal treatment after cytotoxic theraphy stimulates recovery of spermatogenesis. Cancer Res 1999;59:3557–60.PubMedGoogle Scholar
  39. 39.
    Nishimune Y, Okabe M . Mammalian male gametogenesis: growth, differentiation and maturation of germ cells. Develop Growth Differ 1993;35:479–86.CrossRefGoogle Scholar
  40. 40.
    Mintz B . Embryological development of primordial germ cells in the mouse: influence of a new mutation, WJ. J. Embryol Exp Morphol 1957;5:396–403.Google Scholar
  41. 41.
    Mintz B, Russell ES. Gene-induced embryological modifications of primordial germ cells in the mouse. J Exp Zool 1957;134:207–37.PubMedCrossRefGoogle Scholar
  42. 42.
    McCoshen JA, McCallion DJ. A study of the primordial germ cells during their migratory phase in Steel mutant mice. Experientia 1975;31:589–90.PubMedCrossRefGoogle Scholar
  43. 43.
    Guenet JL, Marchal G, Milon G, Tambourin P, Wendling F. Fertile dominant spotting in the house mouse. A new allele at the W locus. J Hered 1979;70:9–12.PubMedGoogle Scholar
  44. 44.
    Koshimizu U, Sawada K, Tajima Y, Watanabe D, Nishimune Y. White-spotting mutations affect the regenerative differentiation of testicular germ cells: demonstration by experimental cryptorchidism and its surgical reversal. Biol Reprod 1991;45:642–48.PubMedCrossRefGoogle Scholar
  45. 45.
    Tajima Y, Sakamaki K, Watanabe D, Koshimizu U, Matsuzawa T, Nishimune Y. Steel-Dickie (Sld) mutation affects both maintenance and differentiation of testicular germ cells in mice. J Reprod Fertil 1991;91:441–49.PubMedCrossRefGoogle Scholar
  46. 46.
    Allard EK, Blanchard KT, Boekelheide K. Exogenous stem cell factor (SCF) com-pensates for altered endogenous SCF expression in 2,5-hexanedione-induced testicular atrophy in rats. Biol Reprod 1996;55:185–93.PubMedCrossRefGoogle Scholar
  47. 47.
    Manova K, Nocka K, Besmer P, Bachvarova RF. Gonadal expression of c-kit encoded at the W locus of the mouse. Development 1990;110:1057–69.PubMedGoogle Scholar
  48. 48.
    Rossi P, Albanesi C, Grimaldi P, Geremia R. Expression of the mRNA for the ligand of c-kit in mouse Sertoli cells. Biochem Biophys Res Commun 1991 ;176: 910–14.PubMedCrossRefGoogle Scholar
  49. 49.
    Mauduit C, Chatelain G, Magre S, Bran G, Benahmed M, Michel D. Regulation by pH of the alternative splicing of the stem cell factor pre–mRNA in the testis. J Biol Chem 1999;274:770–75.PubMedCrossRefGoogle Scholar
  50. 50.
    Morena AR, Boitani C, Pesce M, De Felici M, Stefanini M. Isolation of highly purified type A spermatogonia from prepubertal rat testis. J Androl 1996; 17: 708–17.PubMedGoogle Scholar
  51. 51.
    Yoshinaga K, Nishikawa S, Ogawa M, Hayashi S, Kunisada T, Fujimoto T. Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development 1991;113:689–99.PubMedGoogle Scholar
  52. 52.
    Schrans-Stassen BHGJ, van de Kant HJG, de Rooij DG, van Pelt AMM. Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 1999;140:5894–900.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York, Inc. 2000

Authors and Affiliations

  • Dirk G. de Rooij
  • Bianca H. G. J. Schrans-Stassen
  • Ans M. M. van Pelt
  • Gladis A. Shuttlesworth
  • Marvin L. Meistrich
  • Masaru Okabe
  • Yoshitake Nishimune

There are no affiliations available

Personalised recommendations