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Endocrine

, Volume 26, Issue 3, pp 301–316 | Cite as

Oogenesis in adult mammals, including humans

A review
  • Antonin Bukovsky
  • Michael R. Caudle
  • Marta Svetlikova
  • Jay Wimalasena
  • Maria E. Ayala
  • Roberto Dominguez
Article

Abstract

The origin of oocytes and primary follicles in ovaries of adult mammalian females has been a matter of dispute for over 100 yr. The prevailing belief that all oocytes in adult mammalian females must persist from the fetal period of life seems to be a uniquely retrogressive reproductive mechanism requiring humans to preserve their gametes from the fetal period for several decades. The utilization of modern techniques during last 10 yr clearly demonstrates that mammalian primordial germ cells originate from somatic cell precursors. This indicates that if somatic cells are precursors of germ cells, then somatic mutations can be passed on to progeny. Mitotically active germline stem cells have been described earlier in ovaries of adult prosimian primates and recently have been reported to also be present in the ovaries of adult mice. We have earlier shown that in adult human females, mesenchymal cells in the ovarian tunica albuginea undergo a mesenchymal-epithelial transition into ovarian surface epithelium cells, which differentiate sequentially into primitive granulosa and germ cells. Recently, we have reported that these structures assemble in the deeper ovarian cortex and form new follicles to replace earlier primary follicles undergoing atresia (follicular renewal). Our current observations also indicate that follicular renewal exists in rat ovaries, and human oocytes can differentiate from ovarian surface epithelium in fetal ovaries in vivo and from adult ovaries in vitro. These reports challenge the established dogma regarding the fetal origin of eggs and primary follicles in adult mammalian ovaries. Our data indicate that the pool of primary follicles in adult human ovaries does not represent a static but a dynamic population of differentiating and regressing structures. Yet, the follicular renewal may cease at a certain age, and this may predetermine the onset of the natural menopause or premature ovarian failure. A lack of follicular renewal in aging ovaries may cause an accumulation of spontaneously arising or environmentally induced genetic alterations of oocytes, and that may be why aging females have a much higher chance of having oocytes with more mutations in persisting primary follicles.

Key Words

Oogenesis ovary adult mammals human 

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References

  1. 1.
    Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., and Walter, P. (2002). Molecular biology of the cell. Garland Science: New York.Google Scholar
  2. 2.
    Allen, E. (1923). Am. J. Anat. 31, 439–481.CrossRefGoogle Scholar
  3. 3.
    Auersperg, N., Pan, J., Grove, B. D., et al. (1999). Proc. Natl. Acad. Sci. USA 96, 6249–6254.PubMedCrossRefGoogle Scholar
  4. 4.
    Auersperg, N., Wong, A. S., Choi, K. C., Kang, S. K., and Leung, P. C. (2001). Endocr. Rev. 22, 255–288.PubMedCrossRefGoogle Scholar
  5. 5.
    Baker, T. G. (1972). In: Reproductive biology. Balin, H. and Glasser S. (eds.). Excerpta Medica: Amsterdam, pp. 398–437.Google Scholar
  6. 6.
    Barclay, A. N., Letarte-Muirhead, M., Williams, A. F., and Faulkes, R. A. (1976). Nature 267, 563–567.CrossRefGoogle Scholar
  7. 7.
    Block, E. (1952). Acta Anat. (Basel) 14, 108–123.Google Scholar
  8. 8.
    Bousfield, G. R., Butnev, V. Y., Gotschall, R. R., Baker, V. L., and Moore, W. T. (1996). Mol. Cell Endocrinol. 125, 3–19.PubMedCrossRefGoogle Scholar
  9. 9.
    Brambell, F. W. R. (1927). Proc. Roy. Soc. 101, 391–409.CrossRefGoogle Scholar
  10. 10.
    Bukovsky, A., Caudle, M. R., and Keenan, J. A. (1997). In: Microscopy of reproduction and development: a dynamic approach. Motta, P. M. (ed.) Antonio Delfino Editore: Roma, pp. 79–89.Google Scholar
  11. 11.
    Bukovsky, A., Caudle, M. R., Keenan, J. A., et al. (2001). BMC Dev. Biol. 1, 11.PubMedCrossRefGoogle Scholar
  12. 12.
    Bukovsky, A., Caudle, M. R., Keenan, J. A., Wimalasena, J., Foster, J. S., and Van Meter, S. E. (1995). Biol. Reprod. 52, 776–792.PubMedCrossRefGoogle Scholar
  13. 13.
    Bukovsky, A., Caudle, M. R., Keenan, J. A., Wimalasena, J., Upadhyaya, N. B., and Van Meter, S. E. (1995). Biol. Reprod. 53, 1373–1384.PubMedCrossRefGoogle Scholar
  14. 14.
    Bukovsky, A., Caudle, M. R., Keenan, J. A., Wimalasena, J., Upadhyaya, N. B., and Van Meter, S. E. (1996). Am. J. Reprod. Immunol. 36, 327–341.PubMedGoogle Scholar
  15. 15.
    Bukovsky, A., Caudle, M. R., Svetlikova, M., and Upadhyaya, N. B. (2004). Reprod. Biol. Endocrinol. 2, 20.PubMedCrossRefGoogle Scholar
  16. 16.
    Bukovsky, A., Indrapichate, K., Fujiwara, H., et al. (2003). Reprod. Biol. Endocrinol. 1, 46.PubMedCrossRefGoogle Scholar
  17. 17.
    Bukovsky, A., Keenan, J. A., Caudle, M. R., Wimalasena, J., Upadhyaya, N. B., and Van Meter, S. E. (1995). Am. J. Reprod. Immunol. 33, 323–340.PubMedGoogle Scholar
  18. 18.
    Bukovsky, A., Svetlikova, M., and Caudle, M. R. (2005). Reprod. Biol. Endocrinol. 3, 17.PubMedCrossRefGoogle Scholar
  19. 19.
    Butler, H. and Juma, M. B. (1970). Nature 226, 552–553.PubMedCrossRefGoogle Scholar
  20. 20.
    Byskov, A. G., Skakkebaek, N. E., Stafanger, G., and Peters, H. (1997). J. Anat. 123, 77–86.Google Scholar
  21. 21.
    Carlson, J. L., Bakst, M. R., and Ottinger, M. A. (1996). Poult. Sci. 75, 1569–1578.PubMedGoogle Scholar
  22. 22.
    Choi, K. C., Auersperg, N., and Leung, P. C. (2003). Reprod. Biol. Endocrinol. 1, 71.PubMedCrossRefGoogle Scholar
  23. 23.
    Cohen, F. E., Novotny, J., Sternberg, M. J. E., Campbell, D. G., and Williams, A. F. (1981). Biochem. J. 195, 31–40.PubMedGoogle Scholar
  24. 24.
    Cox, R. T. and Spradling, A. C. (2003). Development 130, 1579–1590.PubMedCrossRefGoogle Scholar
  25. 25.
    Czernobilsky, B., Moll, R., Levy, R., and Franke, W. W. (1985). Eur. J. Cell Biol. 37, 175–190.PubMedGoogle Scholar
  26. 26.
    David, G. F., Anand Kumar, T. C., and Baker, T. G. (1974). J. Reprod. Fertil. 41, 447–451.PubMedCrossRefGoogle Scholar
  27. 27.
    de Winiwarter, H. (1901). Arch. Biol. Paris 17, 33–199.Google Scholar
  28. 28.
    Dunbar, B. S., Timmons, T. M., Skinner, S. M., and Prasad, S. V. (2001). Biol. Reprod. 65, 951–960.PubMedCrossRefGoogle Scholar
  29. 29.
    Dyck, H. G., Hamilton, T. C., Godwin, A. K., Lynch, H. T., Maines-Bandiera, S., and Auersperg, N. (1996). Int. J. Cancer 69, 429–436.PubMedCrossRefGoogle Scholar
  30. 30.
    Edelman, G. M. (1988). Biochemistry 27, 3533–3543.PubMedCrossRefGoogle Scholar
  31. 31.
    Erickson, B. H. (1966). J. Anim. Sci. 25, 800–805.PubMedGoogle Scholar
  32. 32.
    Erickson, G. F. and Shimasaki, S. (2003). Reprod. Biol. Endocrinol. 1, 9.PubMedCrossRefGoogle Scholar
  33. 33.
    Evans, H. M. and Swezy, O. (1931). Mem. Univ. Calif. 9, 119–224.Google Scholar
  34. 34.
    Everett, N. B. (1943). J. Exp. Zool. 92, 49–91.CrossRefGoogle Scholar
  35. 35.
    Franchi, L. L., Mandl, A. M., and Zuckerman, S. (1962). In: The ovary. Zuckerman, S. (ed.). Academic Press: London, pp. 1–88.Google Scholar
  36. 36.
    Geijsen, N., Horoschak, M., Kim, K., Gribnau, J., Eggan, K., and Daley, G. Q. (2004). Nature 427, 148–154.PubMedCrossRefGoogle Scholar
  37. 37.
    Ginsburg, M., Snow, M. H., and McLaren, A. (1990). Development 110, 521–528.PubMedGoogle Scholar
  38. 38.
    Gosden, R. G. (2004). Hum. Reprod. Update 10, 193–195.PubMedCrossRefGoogle Scholar
  39. 39.
    Gougeon, A., Echochard, R., and Thalabard, J. C. (1994). Biol. Reprod. 50, 653–663.PubMedCrossRefGoogle Scholar
  40. 40.
    Hershkovitz, R., Erez, O., Sheiner, E., Landau, D., Mankuta, D., and Mazor, M. (2003). Acta Obstet. Gynecol. Scand. 82, 22–27.PubMedCrossRefGoogle Scholar
  41. 41.
    Hubner, K., Fuhrmann, G., Christenson, L. K., et al. (2003). Science 300, 1251–1256.PubMedCrossRefGoogle Scholar
  42. 42.
    Ingram, D. L. (1962). In: The ovary. Zuckerman, S. (ed.). Academic Press: London, pp. 247–273.Google Scholar
  43. 43.
    Ioannou, J. M. (1968). J. Embryol. Exp. Morphol. 17, 139–145.Google Scholar
  44. 44.
    Johnson, J., Canning, J., Kaneko, T., Pru, J. K., and Tilly, J. L. (2004). Nature 428, 145–150.PubMedCrossRefGoogle Scholar
  45. 45.
    Kelly, S. J. (1977). J. Exp. Zool. 200, 365–376.PubMedCrossRefGoogle Scholar
  46. 46.
    Kingery, H. M. (1917). J. Morphol. 30, 261–315.CrossRefGoogle Scholar
  47. 47.
    Lawson, K. A., Dunn, N. R., Roelen, B. A., et al. (1999). Genes Dev. 13, 424–436.PubMedGoogle Scholar
  48. 48.
    Lawson, K. A. and Hage, W. J. (1994). Ciba Found. Symp. 182, 68–84.PubMedGoogle Scholar
  49. 49.
    Makabe, S., Iwaki, A., Hafez, E. S. E., and Motta, P. M. (1980). In: Biology of the ovary. Motta, P. M. and Hafez, E. S. E. (eds.). Martinus Nijhoff Publishers: The Hague, pp. 279–290.Google Scholar
  50. 50.
    Mathe, G. (1997). Biomed. Pharmacother. 51, 49–57.PubMedCrossRefGoogle Scholar
  51. 51.
    McLaren, A. (1999). Genes Dev. 13, 373–376.PubMedGoogle Scholar
  52. 52.
    Mossman, H. W. and Duke, K. L. (1973). In: Handbook of physiology, Sect. 7: endocrinology. Greep, R. O. (ed.). American Physiological Society: Washington, DC, pp. 389–402.Google Scholar
  53. 53.
    Motta, P. M. and Makabe, S. (1986). J. Submicrosc. Cytol. 18, 271–290.PubMedGoogle Scholar
  54. 54.
    Motta, P. M., Makabe, S., Naguro, T., and Correr, S. (1994). Arch. Histol. Cytol. 57, 369–394.PubMedGoogle Scholar
  55. 55.
    Motta, P. M., Nottola, S. A., Makabe, S., and Heyn, R. (2000). Hum. Reprod. 15(Suppl. 2), 129–147.PubMedGoogle Scholar
  56. 56.
    Motta, P. M., Van Blerkom, J., and Makabe, S. (1980). J. Submicrosc. Cytol. 12, 407–425.Google Scholar
  57. 57.
    Page-Roberts, B. A. (1972). Invest. Urol. 9, 385–389.PubMedGoogle Scholar
  58. 58.
    Pan, J. and Auersperg, N. (1998). Biochem. Cell Biol. 76, 27–35.PubMedCrossRefGoogle Scholar
  59. 59.
    Penny, R., Olambiwonnu, O., and Frasier, S. D. (1976). Pediatrics 58, 110–114.PubMedGoogle Scholar
  60. 60.
    Pepling, M. E. and Spradling, A. C. (1998). Development 125, 3323–3328.PubMedGoogle Scholar
  61. 61.
    Pepling, M. E. and Spradling, A. C. (2001). Dev. Biol. 234, 339–351.PubMedCrossRefGoogle Scholar
  62. 62.
    Peters, H. and McNatty, K. P. (1980). The ovary. a correlation of structure and function in mammals. University of California Press: Berkeley and Los Angeles, CA.Google Scholar
  63. 63.
    Picher, M., Burch, L. H., Hirsh, A. J., Spychala, J., and Boucher, R. C. (2003). J. Biol. Chem. 278, 13468–13479.PubMedCrossRefGoogle Scholar
  64. 64.
    Prindull, G. and Zipori, D. (2004). Blood 103, 2892–2899.PubMedCrossRefGoogle Scholar
  65. 65.
    Quinones, J. A. and van Bogaert, L. J. (1979). Acta Histochem. 64, 106–112.PubMedGoogle Scholar
  66. 66.
    Richardson, R. T., Yamasaki, N., and O’Rand, M. G. (1994). Dev. Biol. 165, 688–701.PubMedCrossRefGoogle Scholar
  67. 67.
    Santini, D., Ceccarelli, C., Mazzoleni, G., Pasquinelli, G., Jasonni, V. M., and Martinelli, G. N. (1993). Histochemistry 99, 311–319.PubMedCrossRefGoogle Scholar
  68. 68.
    Simkins, C. S. (1932). J. Anat. 51, 465–505.CrossRefGoogle Scholar
  69. 69.
    Skinner, S. M. and Dunbar, B. S. (1992). J. Histochem. Cytochem. 40, 1031–1036.PubMedGoogle Scholar
  70. 70.
    Skinner, S. M., Kieback, D. G., Chunn, J., et al. (1997). Anticancer Res. 17, 907–911.PubMedGoogle Scholar
  71. 71.
    Skinner, S. M., Lee, V. H., Kieback, D. G., Jones, L. A., Kaplan, A. L., and Dunbar, B. S. (1997). Anticancer Res. 17, 901–906.PubMedGoogle Scholar
  72. 72.
    Tam, P. P. and Zhou, S. X. (1996). Dev. Biol. 178, 124–132.PubMedCrossRefGoogle Scholar
  73. 73.
    Treisman, R. (1996). Curr. Opin. Cell Biol. 8, 205–215.PubMedCrossRefGoogle Scholar
  74. 74.
    Van Blerkom, J. and Motta, P. M. (1979). The cellular basis of mammalian reproduction. Urban & Schwarzenberg: Baltimore-Munich.Google Scholar
  75. 75.
    Waldeyer, W. (1996). In: Hanbuch der vergleichenden und experimentellen Entwicklung der Wirbeltiere. Hertwig, O. (ed.). Fisher: Jena, pp. 86–476.Google Scholar
  76. 76.
    Waldeyer, W. (1870). Eierstock und Ei. Engelmann, Leipig.Google Scholar
  77. 77.
    Wartenberg, H. (1983). Bibl. Anat. 24, 67–76.Google Scholar
  78. 78.
    Weissmann, A. (1885). Die Continuitat des Keimplasmas als Grundlage einer Theorie der Vererbung. Fischer-Verlag: Jena.Google Scholar
  79. 79.
    Williams, A. F. and Barclay, A. N. (1988). Annu. Rev. Immunol. 6, 381–405.PubMedGoogle Scholar
  80. 80.
    Yamashita, J., Itoh, H., Hirashima, M., et al. (2000). Nature 408, 92–96.PubMedCrossRefGoogle Scholar
  81. 81.
    Zamboni, L. (1970). Biol. Reprod. Suppl. 2, 44–63.PubMedCrossRefGoogle Scholar
  82. 82.
    Ziomek, C. A., Lepire, M. L., and Torres, I. (1990). J. Histochem. Cytochem. 38, 437–442.PubMedGoogle Scholar

Copyright information

© Humana Press Inc. 2005

Authors and Affiliations

  • Antonin Bukovsky
    • 1
    • 2
  • Michael R. Caudle
    • 1
    • 2
  • Marta Svetlikova
    • 1
  • Jay Wimalasena
    • 2
  • Maria E. Ayala
    • 3
  • Roberto Dominguez
    • 3
  1. 1.Laboratory of Development, Differentiation and CancerThe University of Tennessee Graduate School of MedicineKnoxvilleUSA
  2. 2.Department of Obstetrics and GynecologyThe University of Tennessee Graduate School of MedicineKnoxvilleUSA
  3. 3.Laboratory of Biology of ReproductionFacultad de Estudios Profesionales, UNAMMexico D.F.Mexico

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