Recent discoveries in physiology of insulin-like growth factor-1 and its interaction with gonadotropins in folliculogenesis

Abstract

Ovarian follicular development is under the influence of gonadotrophins. The manner by which gonadotrophins achieve their role in cell replication and hormone production is through other specialized molecules. Insulin-like growth factor-1 (IGF-1) is considered to be one of the most important of these molecules. IGF-1 is present in relatively large amounts in the ovary and the IGF-1 gene is expressed in the graafian follicle. IGF-1 binding proteins modulate the action of IGF-1 and are influenced by gonadotrophins. Null mutations of genes encoding IGF-1 and type-1 IGF receptor have demonstrated the obligatory role of IGF-1 in folliculogenesis. It was proposed that IGF-1 may be an obligatory mediator of gonadotrophin-induced folliculogenesis and that the interaction is synergistic.

From this point, one group embarked on a series of physiological studies to further elucidate the interaction of these molecules. We discovered that, according to circumstances, follicle stimulating hormone (FSH) may act with IGF-1 synergistically (as was postulated before), additively, independently, or even antagonistically. We discovered that granulosa cells must first be exposed to FSH and then they respond well to IGF-1. All previous studies of granulosa cells were done on mural granulosa cells. We subsequently showed that cumulus type of granulosa cells (adjacent to the oocyte) behave differently in their responses to gonadotrophins and IGF-1.

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References

  1. 1.

    Dorrington, J. H. and Armstrong, D. T. (1979). Recent Prog. Horm. Res. 35, 301–342.

    PubMed  CAS  Google Scholar 

  2. 2.

    Richards, J. S. (1980). Physiol. Rev. 60, 51–89.

    PubMed  CAS  Google Scholar 

  3. 3.

    Savion, N., Lui, G.-M., Laherty, R., and Gospodarowicz, D. (1981). Endocrinology 109, 409–417.

    PubMed  CAS  Google Scholar 

  4. 4.

    May, J. V., Frost, J. P., and Schomberg, D. W. (1988). Endocrinology 123, 168–179.

    PubMed  CAS  Google Scholar 

  5. 5.

    Greenwald, G. S. and Terranova, P. F. (1988). In: The physiology of reproduction, vol. 1. Knobil, E. and Neill, J. (eds.). Raven: New York.

    Google Scholar 

  6. 6.

    Adashi, E. Y., Resnick, C. E., D’ercole, A. J., et al. (1985). Endocr. Rev. 6(3), 400–420.

    PubMed  CAS  Google Scholar 

  7. 7.

    Singh, B. and Armstrong, D. T. (1994). Theriogenology 41, 295–301.

    Article  Google Scholar 

  8. 8.

    Erickson, G. F. and Shimasaki, S. (1996). Department of Reproductive Medicine (0674), University of California.

  9. 9.

    Murphy, L. J., Bell, G. I., and Friesen, H. G. (1987). Endocrinology 120, 1279–1282.

    PubMed  CAS  Google Scholar 

  10. 10.

    Oliver, J. E., Aitman, T. J., Powell, J. F., Wilson, C. A., and Ciayton, R. N. (1989). Endocrinology 124, 2670–2679.

    Google Scholar 

  11. 11.

    Zhou, J., Chin, E., and Bondy, C. (1991). Endocrinology 129, 3281–3288.

    PubMed  CAS  Google Scholar 

  12. 12.

    Hernandez, E. R., Roberts, C. H., LeRoith, D., and Adashi, E. Y. (1989). Endocrinology 125, 572–574.

    PubMed  CAS  Google Scholar 

  13. 13.

    Hansson, H.-A., Nilsson, A., Isgaard, J., Billig, H., Isaksson, O., Skottner, A., Andersson, I. K., and Rozell, B. (1988). Histochemistry 89, 403–410.

    PubMed  Article  CAS  Google Scholar 

  14. 14.

    Goldenberg, R. L., Vaitukaitis, J. L., and Ross, G. T. (1972). Endocrinology 90, 1492–1498.

    PubMed  CAS  Google Scholar 

  15. 15.

    Lonergan, P., Monaghan, P., Rizos, D., Boland, M. P., and Gordon, I. (1994). Mol. Reprod. Dev. 37, 48–53.

    PubMed  Article  CAS  Google Scholar 

  16. 16.

    Hsu, C.-J. and Hammond, J. M. (1986). Endocrinology 120, 198–207.

    Google Scholar 

  17. 17.

    Hammond, J. M., Hsu, C.-J., Klindt, J., Tsang, B. K., and Downey, B. R. (1988). Biol. Reprod. 38, 304–308.

    PubMed  Article  CAS  Google Scholar 

  18. 18.

    Magoffin, D. A. and Erickson, G. F. (1988). Cell. Dev. Biol. 24, 862–870.

    Article  CAS  Google Scholar 

  19. 19.

    Magoffin, D. A., Kurtz, K. M., and Erickson, G. F. (1990). Mol. Endocrinol. 4, 489–496.

    PubMed  CAS  Google Scholar 

  20. 20.

    Hernandez, E. R., Resnick, C. E., Svoboda, M. E., Van Wyk, J. J., Payne, D. W., and Adashi, E. Y. (1988). Endocrinology 122, 1603–1612.

    PubMed  CAS  Google Scholar 

  21. 21.

    Caubo, B., De Vinna, R. S., and Tonetta, S. A. (1989). Endocrinology 125, 321–326.

    PubMed  CAS  Google Scholar 

  22. 22.

    Cara, J. F. and Rosenfield, R. L. (1988). Endocrinology 123, 733–739.

    PubMed  CAS  Google Scholar 

  23. 23.

    Cara, J. F., Fan, J., Azzarello, J., and Rosenfield, R. L. (1990). J. Clin. Invest. 86, 560–565.

    PubMed  CAS  Google Scholar 

  24. 24.

    Magoffin, D. A. and Weitsman, S. R. (1994). Biol. Reprod. 1994; 51, 766–775.

    PubMed  Article  CAS  Google Scholar 

  25. 25.

    Magoffin, D. A. and Weitsman, S. R. (1993). Biol. Reprod. 48, 1166–1173.

    PubMed  Article  CAS  Google Scholar 

  26. 26.

    Magoffin, D. A. and Weitsman, S. R. (1993). Mol. Cell. Endocrinol. 96, 45–51.

    PubMed  Article  CAS  Google Scholar 

  27. 27.

    Magoffin, D. A. and Weitsman, S. R. (1993). Endocrinology 132, 1945–1951.

    PubMed  Article  CAS  Google Scholar 

  28. 28.

    Nakatani, A., Shimasaki, S., Erickson, G. F., and Ling, N. (1991). Endocrinology 129, 1521–1529.

    PubMed  CAS  Google Scholar 

  29. 29.

    Erickson, G. F., Nakatani, A., Ling, N., and Shimasaki, S. (1992). Endocrinology 130, 625–636.

    PubMed  Article  CAS  Google Scholar 

  30. 30.

    Erickson, G., Nakatani, A., Ling, N., and Shimasaki, S. (1992). Endocrinology 130, 1867–1878.

    PubMed  Article  CAS  Google Scholar 

  31. 31.

    Adashi, E. Y., Resnick, C. E., Svoboda, M. E., and Van Wyk, J. J. (1986). Biol. Reprod. 34, 81–88.

    PubMed  Article  CAS  Google Scholar 

  32. 32.

    Ricciarelli, E., Hernandez, E. R., Hurwitz, A., Kokia, E., Rosenfeld, R. G., Schwander, J., and Adashi, E. Y. (1991). Endocrinology 129, 2266–2268.

    PubMed  CAS  Google Scholar 

  33. 33.

    Ricciarelli, E., Hernandez, E. R., Kokia, E., Rohan, R. M., Tedeschi, C., Botero, L., Rosenfeld, R. G., Albiston, A. L., Herington, A. C., and Adashi, E. Y. (1992). Endocrinology 130, 3092–3094.

    PubMed  Article  CAS  Google Scholar 

  34. 34.

    Rohan, R. M., Ricciarelli, E., Kiefer, M. C., Resnick, C. E., and Adashi, E. Y. (1993). Endocrinology 132, 2507–2512.

    PubMed  Article  CAS  Google Scholar 

  35. 35.

    Ui, M., Shimonaka, M., Shimasaki, S., and Ling, N. (1989). Endocrinology 25, 912–916.

    Article  Google Scholar 

  36. 36.

    Shimasaki, S., Shimonaka, M., Ui, M., Inouye, S., Shibata, F., and Ling, N. (1990). J. Biol. Chem. 265, 2198–2202.

    PubMed  CAS  Google Scholar 

  37. 37.

    Bicsak, T. S., Shimonaka, M., Malkowski, M., and Ling, N. (1990). Endocrinology 126, 2184–2189.

    PubMed  CAS  Google Scholar 

  38. 38.

    Bicsak, T. S., Long, N., and DePaolo, L. V. (1991). Biol. Reprod. 44, 599–603.

    PubMed  Article  CAS  Google Scholar 

  39. 39.

    Shimasaki, S., Murakami, K., Morita, Y., and Erickson, G. F. (1995). Frontiers in endocrinology. Serono Symposium, Elsevier, New York.

    Google Scholar 

  40. 40.

    Erickson, G. F., Nakatani, A., Liu, X.-J., Shimasaki, S., and Ling, N. (1994). In: Molecular biology of the female reproductive system. Findlay, J. K. (ed.). Academic: New York.

    Google Scholar 

  41. 41.

    Liu, X.-J., Malkowski, M., Guo, T.-L., Erickson, G. F., Shimasaki, S., and Ling, N. (1993). Endocrinology 132, 1176–1183.

    PubMed  Article  CAS  Google Scholar 

  42. 42.

    Erickson, G. F., Li, D., Sadkhanloo, R., Liu, X.-J., Shimasaki, S., and Ling, N. (1994). Endocrinology 134, 1365–1372.

    PubMed  Article  CAS  Google Scholar 

  43. 43.

    Erickson, G. F., Li, D., Weitsman, S. R., Shimasaki, S., Ling, N., and Magoffin, D. A. (1995). Endocrine 3, 525–531.

    CAS  Google Scholar 

  44. 44.

    Yoshimura, Y., Aoki, N., Sueoka, K., Miyazarki, T., Kuji, N., Tanaka, M., and Kobayashi, T. J. (1996). Clin. Invest. 98(2), 308–316.

    CAS  Article  Google Scholar 

  45. 45.

    Efstratiadis, A. (1994). In: Developmental endocrinology, frontiers in endocrinology, vol. 6. Sizonenko, P. C., Aubert, M. L., and Vassali, J. D. (eds.). Ares-Serono Symposia Publications.

  46. 46.

    Xia, P., Tekpetey, F. R., and Armstrong, D. T. (1994). Mol. Reprod. Dev. 38, 373–379.

    PubMed  Article  CAS  Google Scholar 

  47. 47.

    Brower, P. T. and Schultz, R. M. (1982). Dev. Biol. 90, 144–153.

    PubMed  Article  CAS  Google Scholar 

  48. 48.

    Moore, R. M. (1983). In: Current problems in germ cell differentiation. McLaren, A. and Wylie, C. C. (eds.). University Press: Cambridge, UK.

    Google Scholar 

  49. 49.

    Adashi, E. Y., Resnick, C. E., Dercole, A. J., Svoboda, M. C., and Van Wyk, J. J. (1985). Endocr. Rev. 6(3), 400–420.

    PubMed  CAS  Google Scholar 

  50. 50.

    Armstrong, D. T., Xia, P., de Gannes, G., Tekpetey, F. R., and Khamsi, F. (1996). Biol. Reprod. 54, 331–338.

    PubMed  Article  CAS  Google Scholar 

  51. 51.

    Khamsi, F. and Armstrong, D. T. (1997). Biol. Reprod. 57, 684–688.

    PubMed  Article  CAS  Google Scholar 

  52. 52.

    Khamsi, F. and Roberge, S. (2001). Fertil. Steril. 75, 997–1002.

    PubMed  Article  CAS  Google Scholar 

  53. 53.

    Khamsi, F. and Roberge, S. (2001). J. Endocrinol. 170, 565–573.

    PubMed  Article  CAS  Google Scholar 

  54. 54.

    Francis, A. L., Ross, M., Ballard, F. J., Milner, S. J., Senn, E., McNeil, K. M., Wallace, J. C., King, R., and Wells, J. R. E. (1992). J. Mol. Endocrinol. 8, 213–230.

    PubMed  CAS  Article  Google Scholar 

  55. 55.

    Ballafd, F. J., Francis, A. L., Walton, P. E., Knowles, S. E., Owens, P. C., Read, L. C., and Tomas, F. M. (1993). Aust. J. Agric. Sci. 44, 567–577.

    Article  Google Scholar 

  56. 56.

    Khamsi, F. and Roberge, S. (2000). Endocrine 12(1), 41–45.

    PubMed  Article  CAS  Google Scholar 

  57. 57.

    Khamsi, F., Roberge, S., and Wong, J. (2001). Endocrine 14(3), 175–180.

    PubMed  Article  CAS  Google Scholar 

  58. 58.

    Khainsi, F., Roberge, S., Lacanna, I., Wong, J., and Yavas, Y. (1999). Endocrine 10, 161–166.

    Article  Google Scholar 

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Correspondence to Dr. F. Khamsi.

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Khamsi, F., Roberge, S., Yavas, Y. et al. Recent discoveries in physiology of insulin-like growth factor-1 and its interaction with gonadotropins in folliculogenesis. Endocr 16, 151–165 (2001). https://doi.org/10.1385/ENDO:16:3:151

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Key Words

  • Insulin-like growth factor-1
  • follicle-stimulating hormone
  • luteinizing hormone
  • granulosa cells
  • cumulus cells
  • DNA synthesis