Skip to main content
Book cover

Ovulation pp 67–75Cite as

The Role of the Oocyte in Ovulation

  • Chapter

Part of the book series: Proceedings in the Serono Symposia USA Series ((SERONOSYMP))

Abstract

Ovulation requires tight control of extracellular matrix modifications, within both the follicle wall and the inner mass of granulosa cells surrounding the oocyte, namely the cumulus cells. In most mammals, prior to ovulation, mural granulosa cells promote selective degradation of perifollicular matrix, resulting in the formation of a thinner area at the follicular apex. At the same time, the cumulus cells synthesize and deposit a large and viscoelastic extracellular matrix around the oocyte, a process known as cumulus expansion or mucification. As ovulation approaches, the apical follicle wall breaks, and a hole is formed that is sufficiently large to allow a portion of the cumulus mass to pass through it. Deformation of the cumulus matrix allows the passage of the first cumulus cells through the rupture site, after which the oocyte, surrounded by the remaining cumulus cells, is rapidly extruded from the follicle. Cumulus cells and the oocyte remain firmly bound within the matrix so that they are not dispersed during the extrusion.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Chen L, Russell PT, Larsen WJ. Functional significance of cumulus expansion in the mouse: roles for the preovulatory synthesis of hyaluronic acid within the cumulus mass. Mol Reprod Dev 1993;34:87–93.

    Article  PubMed  CAS  Google Scholar 

  2. Mahi-Brown CA, Yanagimachi R. Parameters influencing ovum pickup by oviductal fimbria in the golden hamster. Gamete Res 1983;8:1–10.

    Article  CAS  Google Scholar 

  3. Rankin T, Familiari M, Lee E, Ginsberg A, Dwyer N, Blanchette-Mackie J, et al. Mouse homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are fertile. Development 1996; 122:2903–10.

    PubMed  CAS  Google Scholar 

  4. Liu C, Litscher ES, Mortillo S, Sakai Y, Kinloch RA, Stewart CL, et al. Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice. Proc Natl Acad Sci 1996;93:5431–36.

    Article  PubMed  CAS  Google Scholar 

  5. Fraser JR, Laurent TC, Laurent UB. Hyaluronan: its nature, distribution, functions and turnover. J Intern Med 1997;242:27–33.

    Article  PubMed  CAS  Google Scholar 

  6. Cherr GN, Yudin AI, Katz DE Organization of the hamster cumulus extracellular matrix: a hyaluronate-glycoprotein gel which modulates sperm access to the oocyte. Dev Growth Differ 1990;32:353–65.

    Article  CAS  Google Scholar 

  7. Talbot P. Sperm penetration through oocyte investments in mammals. Am J Anat 1985; 174:331–46.

    Article  PubMed  CAS  Google Scholar 

  8. Camaioni A, Hascall VC, Yanagishita M, Salustri A. Effect of exogenous hyaluronic acid and serum on matrix organization and stability in the mouse cumulus cell-oocyte complex. J Biol Chem 1993;268:20473–81.

    PubMed  CAS  Google Scholar 

  9. Fulop C, Kamath RV, Li Y, Otto JM, Salustri A, Olsen BR, et al. Coding sequence, exon-intron structure and chromosomal localization of murine TNF-stimulated gene 6 that is specifically expressed by expanding cumulus cell-oocyte complexes. Gene 1997;202:95–102.

    Article  PubMed  CAS  Google Scholar 

  10. Lesley J, Hyman R, Kincade PW. CD44 and its interaction with extracellular matrix. Adv Immunol 1993;54:271–335.

    Article  PubMed  CAS  Google Scholar 

  11. Wisniewski HG, Burgess WH, Oppenheim JD, Vilcek J. TSG-6, an arthritis-associ-ated hyaluronan binding protein, form a stable complex with the serum protein inter-alpha-trypsin inhibitor. Biochemistry 1994; 33:7423–29.

    Article  PubMed  CAS  Google Scholar 

  12. Chen LC, Mao SJT, Larsen WL. Identification of a factor in fetal bovine serum that stabilizes the cumulus extracellular matrix. J Biol Chem 1992;267:12380–86.

    PubMed  CAS  Google Scholar 

  13. Chen L, Mao SJ, McLean LR, Powers RW, Larsen WJ. Proteins of the inter-alpha-trypsin inhibitor family stabilize the cumulus extracellular matrix through thier direct binding with hyaluronic acid. J Biol Chem 1994;269:28282–87.

    PubMed  CAS  Google Scholar 

  14. Wisniewski HG, Hua JC, Poppers DM, Naime D, Vilcek J, Cronstein BN. TNF/IL-1 inducible protein TSG-6 potentiates plasmin inhibition by inter-alpha-inhibitor and exerts a strong anti-inflammatory effect in vivo. J Immunol 1996; 156:1609–15.

    PubMed  CAS  Google Scholar 

  15. Canipari R, Epifano O, Siracusa G, Salustri A. Mouse oocytes inhibit plasminogen activator production by ovarian cumulus and granulosa cells. Dev Biol 1995; 167: 371–78.

    Article  PubMed  CAS  Google Scholar 

  16. Hagglund AC, Ny A, Liu K, Ny T. Coordinated and cell-specific induction of both physiological plasminogen activators creates functionally redundant mechanisms for plasmin formation during ovulation. Endocrinology 1996; 137:5671–77.

    Article  PubMed  CAS  Google Scholar 

  17. Thibault CG. Final stages of mammalian oocyte maturation. In: Biggers JD, Schuetz AW, eds. Ooogenesis. Baltimore: University Park Press; 1972:397–411.

    Google Scholar 

  18. Ball GD, Bellin ME, Ax RL, First NL. Glycosaminoglycans in bovine cumulus-oocyte complexes: morphology and chemistry. Mol Cell Endocrinol 1982;28:113–22.

    Article  PubMed  CAS  Google Scholar 

  19. Singh B, Barbe GJ, Armstrong DT. Factors influencing resumption of meiotic maturation and cumulus expansion of porcine oocy te-cumulus cell complexes in vitro. Mol Reprod Dev 1993;36:113–19.

    Article  PubMed  CAS  Google Scholar 

  20. Armstrong DT, Xia P, de Gannes G, Tekpetey FR, Khamsi F. Differential effects of insulin-like growth factor-1 and follicle-stimulating hormone on proliferation and differentiation of bovine cumulus cells and granulosa cells. Biol Reprod 1996;54: 331–38.

    Article  PubMed  CAS  Google Scholar 

  21. Eppig JJ. FSH stimulates hyaluronic acid synthesis by oocyte-cumulus cell complexes from mouse preovulatory follicles. Nature 1979;281:483–84.

    Article  PubMed  CAS  Google Scholar 

  22. Amsterdam A, Koch Y, Lieberman ME, Lindner HR. Distributions of binding sites for human chorionic gonadotropin in the preovulatory follicle of the rat. J Cell Biol 1975;67:894–900.

    Article  PubMed  CAS  Google Scholar 

  23. Lawrence TS, Dekel N, Beers WH. Binding of human chorionic gonadotropin by rat cumuli oophori and granulosa cells: a comparative study. Endocrinology 1980; 106:1114–18.

    Article  PubMed  CAS  Google Scholar 

  24. Channing CP, Bae IH, Stone SL, Anderson LD, Edelson S, Fowler SC. Porcine granulosa and cumulus cell properties. LH/hCG receptors, ability to secrete progesterone and ability to respond to LH. Mol Cell Endocrinol 1981;22:359–70.

    CAS  Google Scholar 

  25. Oxberry BA, Greenwald GS. An autoradiographic study of the binding of 125I-labeled follicle stimulating hormone, human chorionic gonadotropin, and prolactin to the hamster ovary throughout the estrous cycle. Biol Reprod 1982;27:505–16.

    Article  PubMed  CAS  Google Scholar 

  26. Salustri A, Yanagishita M, Hascall VC. Synthesis and accumulation of hyaluronic acid and proteoglycans in the mouse cumulus cell-oocyte complex during follicle stimulating hormone-induced mucification. J Biol Chem 1989;264:13840–47.

    PubMed  CAS  Google Scholar 

  27. Tirone E, D’Alessandris C, Hascall VC, Siracusa G, Salustri A. Hyaluronan synthesis by mouse cumulus cells is regulated by interactions between follicle-stimulating hormone (or epidermal growth factor) and a soluble oocyte factor (or transforming growth factor beta 1). J Biol Chem 1997;272:4787–94.

    Article  PubMed  CAS  Google Scholar 

  28. Schultz RM, Montgomery RR, Belanoff JR. Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorilation in commitment to resume meiosis. Dev Biol 1983;97:264–73.

    Article  PubMed  CAS  Google Scholar 

  29. Eppig JJ, Downs SM. Gonadotropin-induced murine oocyte maturation in vivo is not associated with decreased cyclic adenosine monophosphate in the oocyte-cumulus cell complex. Gamete Res 1988;20:125–31.

    Article  PubMed  CAS  Google Scholar 

  30. Salustri A, Yanagishita M, Underhill C, Laurent TC, Hascall VC. Localization and synthesis of hyaluronic acid in the cumulus cells and mural granulosa cells of the preovulatory follicles. Dev Biol 1992;151:541–51.

    Article  PubMed  CAS  Google Scholar 

  31. Eppig JJ. Regulation of cumulus oophorus expansion by gonadotropins in vivo and in vitro. Biol Reprod 1980;23:545–52.

    Article  PubMed  CAS  Google Scholar 

  32. Eppig JJ. Prostaglandin E2 stimulates cumulus expansion and hyaluronic acid synthesis by cumuli oophori isolated from mice. Biol Reprod 1981;25:191–95.

    Article  PubMed  CAS  Google Scholar 

  33. Downs SM, Longo FJ. Effects of indomethacin on preovulatory follicles in immature, superovulated mice. Am J Anat 1982; 164:265–74.

    Article  PubMed  CAS  Google Scholar 

  34. Salustri A, Petrungaro S, Siracusa G. Granulosa cells stimulate in vitro the expansion of isolated mouse cumuli oophori: involvement of prostaglandin E2. Biol Reprod 1985;33:229–34.

    Article  PubMed  CAS  Google Scholar 

  35. Fulop C, Salustri A, Hascall VC. Coding sequence of a hyaluronan synthase homologue expressed during expansion of the mouse cumulus-oocyte complex. Arch Biochem Biophys 1997;337:261–66.

    Article  PubMed  CAS  Google Scholar 

  36. Salustri A, Yanagishita M, Hascall VC. Mouse oocytes regulate hyaluronic acid synthesis and mucification by FSH-stimulated cumulus cells. Dev Biol 1990; 138:26–32.

    Article  PubMed  CAS  Google Scholar 

  37. Buccione R, Vanderhyden BC, Caron PJ, Eppig JJ. FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte. Dev Biol 1990; 138:16–25.

    Article  PubMed  CAS  Google Scholar 

  38. Eppig JJ, Peters AHFM, Telfer E, Wigglesworth K. Production of cumulus expansion enabling factor by mouse oocytes grown in vitro: preliminary characterization of the factor. Mol Reprod Dev 1993;34:450–56.

    Article  PubMed  CAS  Google Scholar 

  39. Vanderhyden BC, Caron PJ, Buccione R, Eppig JJ. 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 1990; 140:307–17.

    Article  PubMed  CAS  Google Scholar 

  40. Eppig JJ, Wigglesworth K, Chesnel F. Secretion of cumulus expansion enabling factor by mouse oocytes: relationship to oocyte growth and competence to resume meiosis. Dev Biol 1993;158:400–9.

    Article  PubMed  CAS  Google Scholar 

  41. Salustri A, Ulisse S, Yanagishita M, Hascall VC. Hyaluronic acid synthesis by mural granulosa cells and cumulus cells in vitro is selectively stimulated by a factor produced by oocytes and by transforming growth factor-beta. J Biol Chem 1990;265:19517–23.

    PubMed  CAS  Google Scholar 

  42. Prochazka E, Nagyova E, Rimkeviova T, Nagai T, Kikuchi K, Motlik J. Lack of effect of oocytectomy on expansion of the porcine cumulus. J Reprod Fertil 1991;93:569–76.

    Article  PubMed  CAS  Google Scholar 

  43. Vanderhyden BC. Species differences in the regulation of cumulus expansion by an oocyte-secreted factor(s). J Reprod Fertil 1993;98:219–27.

    Article  PubMed  CAS  Google Scholar 

  44. Singh B, Zhang X, Armstrong DT. Porcine oocytes release cumulus expansion-enabling activity even though porcine cumulus expansion in vitro is independent of the oocyte. Endocrinology 1993; 132:1860–62.

    Article  PubMed  CAS  Google Scholar 

  45. Ralph JH, Telfer EE, Wilmut I. Bovine cumulus cell expansion does not depend on the presence of an oocyte secreted factor. Mol Reprod Dev 1995;42:248–53.

    Article  PubMed  CAS  Google Scholar 

  46. Prochazka R, Nagyova E, Brem G, Schellander K, Motlik J. Secretion of cumulus expansion-enabling factor (CEEF) in porcine follicles. Mol Reprod Dev 1998;49:141–49.

    Article  PubMed  CAS  Google Scholar 

  47. Nakayama T, Inoue M, Sato E. Effect of oocytectomy on glycosaminoglycan composition during cumulus expansion of porcine cumulus-oocyte complexes cultured in vitro. Biol Reprod 1996;55:1299–304.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer Science+Business Media New York

About this chapter

Cite this chapter

Salustri, A., Fulop, C., Hascall, V.C., Camaioni, A., Di Giacomo, M. (2000). The Role of the Oocyte in Ovulation. In: Adashi, E.Y. (eds) Ovulation. Proceedings in the Serono Symposia USA Series. Springer, New York, NY. https://doi.org/10.1007/978-0-387-21508-2_6

Download citation

  • DOI: https://doi.org/10.1007/978-0-387-21508-2_6

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4899-0521-5

  • Online ISBN: 978-0-387-21508-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics