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Promotion of follicular antrum formation by pig oocytes in vitro

Published online by Cambridge University Press:  15 January 2010

Xiangju Shen
Affiliation:
The Graduate School of Science and Technology and the Faculty of Agriculture, Kobe University, Kobe, Japan
Takashi Miyano*
Affiliation:
The Graduate School of Science and Technology and the Faculty of Agriculture, Kobe University, Kobe, Japan
Seishiro Kato
Affiliation:
The Graduate School of Science and Technology and the Faculty of Agriculture, Kobe University, Kobe, Japan
*
T. Miyano, Laboratory of Animal Breeding and Reproduction, Faculty of Agriculture, Kobe University, Nada-ku, Kobe 657, Japan. Tel: +81 78 803 0621. Fax: +81 78 803 0622. e-mail: miyano@kobe-u.ac.jp.

Summary

Pig oocyte–cumulus–granulosa cell complexes (OCG complexes) from pig early antral follicles reorganise an antrum under the stimulation of FSH. The purpose of this study was to examine the role of the oocytes in antrum formation. In the first experiment, oocyte–cumulus complexes were removed from pig OCG complexes, and the antrum formation of parietal granulosa cells themselves (PGs) was examined. Antrum formation by sham-operated OCG complexes (OC/G complexes), in which the connections between the oocyte–cumulus complexes and the parietal granulosa cells had been disrupted, was also examined. The complexes were cultured for 8 days in collagen gels in the presence of 10ng/ml FSH. Antra were formed in about 60% of the intact OCG complexes and the sham-operated OCG complexes, while only 20% of the PGs formed antra. In the second experiment, oocyte–cumulus complexes in the OCG complexes were replaced by denuded oocytes (O/G complexes) or Sephadex G-25 beads (B/G complexes) similar in diameter to the oocytes, and the two types of complexes were cultured under the same conditions. The O/G complexes formed antra to a similar extent as the OC/G complexes, whereas the B/G complexes scarcely formed any antra. The histological sections showed that the granulosa cells in the OC/G and O/G complexes were in intimate contact with each other and retained a shape similar to those in the ovarian follicles, while the granulosa cells in the PGs and B/G complexes became quite irregular in shape. These results suggest that pig oocytes promote contact between the granulosa cells to induce antrum formation in a physiological manner.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1998

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References

Buccione, R., Vanderhyden, B.C., Caron, P.J. & Eppig, J.J. (1990). FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte. Dev. Biol. 138, 1625.CrossRefGoogle ScholarPubMed
Dong, J., Albertini, D.F., Nishimori, K., Kumar, T.R., Lu, N. & Matzuk, M.M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531–5.CrossRefGoogle ScholarPubMed
Edwards, R.G. (1974). Follicular fluid, J. Reprod. Fertil. 37, 189219.CrossRefGoogle ScholarPubMed
Eppig, J.J. (1994). Oocyte-somatic cell communication in the ovarian follicles of mammals. Dev. Biol. 5, 51–9.CrossRefGoogle Scholar
Eppig, J.J., Wigglesworth, K. & Chesnel, F. (1993). Secretion of cumulus expansion enabling factor by mouse oocytes: relationship to oocyte growth and competence to resume meiosis. Dev. Biol. 158, 400–9.CrossRefGoogle ScholarPubMed
Gore-Langton, R.E. & Daniel, S.A.J. (1990). Follicle-stimulating hormone and estradiol regulate antrum-like reorganization of granulosa cells in rat preantral follicle cultures. Biol. Reprod. 43, 6572.CrossRefGoogle ScholarPubMed
Greenwald, G.S. & Terranova, P.F. (1988). Follicular selection and its control. In The Physiology of Reproduction, ed. Knobil, E. & Neill, J.D., pp. 387445. New York: Raven Press.Google Scholar
Hirao, Y., Nagai, T., Kubo, M., Miyano, T., Miyake, M. & Kato, S. (1994). In vitro growth and maturation of pig oocytes. J. Reprod. Fertil. 100, 333–9.CrossRefGoogle ScholarPubMed
Lawrence, T.S., Ginzberg, R.D., Gilula, N.B. & Beers, W.H. (1979). Hormonally induced cell shape changes in cultured rat ovarian granulosa cells, J. Cell Biol. 80, 2136.CrossRefGoogle ScholarPubMed
McNatty, K.P. (1978). Follicular fluid. In The Vertebrate Ovary, ed. Jones, R.E., pp. 215–59. New York: Plenum Press.Google Scholar
Nayudu, P.L. & Osborn, S.M. (1992). Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro. J. Reprod. Fertil. 95, 349–62.CrossRefGoogle ScholarPubMed
Qvist, R., Blackwell, L.F., Bourne, H. & Brown, J.B. (1990). Development of mouse ovarian follicles from primary to preovulatory stages in vitro. J. Reprod. Fertil. 89, 169–80.CrossRefGoogle ScholarPubMed
Roy, S.K. & Greenwald, G.S. (1989). Hormonal requirements for the growth and differentiation of hamster preantral follicles in long-term culture, J. Reprod. Fertil. 87, 103–14.CrossRefGoogle ScholarPubMed
Salustri, A., Yanagishita, M. & Hascall, V.C. (1990). Mouse oocytes regulate hyaluronic acid synthesis and mucification by FSH-stimulated cumulus cells. Dev. Biol. 138, 2632.CrossRefGoogle ScholarPubMed
Schweitzer, M., Jackson, J.C. & Ryan, R.J. (1981). The porcine ovarian follicle. VII. FSH stimulation of in vitro [3H]-glucosamine incorporation into mucopolysaccharides. Biol. Reprod. 24, 332–40.CrossRefGoogle ScholarPubMed
Shen, X., Hirata, M., Miyano, T. & Kato, S. (1997). In vitro antrum formation of oocyte-cumulus-granulosa cell complexes from pig early antral follicles, J. Mamm. Ova Res. 14, 183–90.CrossRefGoogle Scholar
Snell, W.J. & White, J.M. (1996). The molecules of mammalian fertilization. Cell 85, 629–37.CrossRefGoogle ScholarPubMed
Vanderhyden, B.C. (1996). Oocyte-secreted factors regulate granulosa cell steroidogenesis. Zygote 4, 317–21.CrossRefGoogle ScholarPubMed
Vanderhyden, B.C. & Tonary, A.M. (1995). Differential regulation of progesterone and estradiol production by mouse cumulus and mural granulosa cells by a factor(s) secreted by the oocyte. Biol. Reprod. 53, 1243–50.CrossRefGoogle ScholarPubMed
Vanderhyden, B.C., Caron, P.J., Buccione, R. & Eppig, J.J. (1990). Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev. Biol. 140, 307–17.CrossRefGoogle ScholarPubMed
Vanderhyden, B.C., Telfer, E.E. & Eppig, J.J. (1992). Mouse oocytes promote proliferation of granulosa cells from preantral and antral follicles in vitro. Biol. Reprod. 42, 1196–204.CrossRefGoogle Scholar
Vanderhyden, B.C., Cohen, J.N. & Morley, P. (1993). Mouse oocytes regulate granulosa cell steroidogenesis. Endocrinology 133, 423–6.CrossRefGoogle ScholarPubMed