Skip to main content
Log in

The Role of the Extracellular Matrix in Ovarian Follicle Development

  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

Regulation of ovarian follicle development depends on endocrine- and paracrine-acting hormones, the 3-dimensional architecture of the follicle, and the physical rigidity of the surrounding tissue. These 3 forces are integrated throughout the life cycle of the follicle to ensure appropriate hormone secretion, differentiation of the somatic cells, and maturation of the oocyte. The process of in-follicle maturation provides a new tool for understanding ovarian follicle development under the influence of these factors.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Zhao Y., Luck MR Gene expression and protein distribution of collagen, fibronectin and laminin in bovine follicles and corpora lutea. J Reprod Fertil. 1995;104:115–123.

    Article  CAS  PubMed  Google Scholar 

  2. Rodgers HF, Irvine CM, van Wezel IL, et al. Distribution of the α1 to α6 chains of type IV collagen in bovine follicles. Biol Reprod. 1998;59:1334–1341.

    Article  CAS  PubMed  Google Scholar 

  3. McArthur ME, Irving-Rodgers HF, Byers S., Rodgers RJ Identification and immunolocalization of decorin, versican, perlecan, nidogen, and chondroitin sulfate proteoglycans in bovine small-antral ovarian follicles. Biol Reprod. 2000;63: 913–924.

    Article  CAS  PubMed  Google Scholar 

  4. Rodgers RJ, Irving-Rodgers HF, van Wezel IL, Krupa M., Lavranos TC Dynamics of the membrana granulosa during expansion of the ovarian follicular antrum. Mol Cell Endocrinol. 2001; 171:41–48.

    Article  CAS  PubMed  Google Scholar 

  5. Yamada S., Fujiwara H., Honda T, et al. Human granulosa cells express integrin α2 and collagen type IV: possible involvement of collagen type IV in granulosa cell luteinization. Mol Hum Reprod. 1999;5:607–617.

    Article  CAS  PubMed  Google Scholar 

  6. Iwahashi M., Muragaki Y, Ooshima A, Nakano R. Type VI collagen expression during growth of human ovarian follicles. Fertil Steril. 2000; 74:343–347.

    Article  CAS  PubMed  Google Scholar 

  7. Rajah R., Sundaram GS Protein distribution and gene expression of collagen type IV in the neonatal rat ovary during follicle formation. Cell Mol Biol (Noisy-le-grand). 1994; 40:769–780.

    CAS  Google Scholar 

  8. Frojdman K., Pelliniemi LJ, Virtanen I. Differential distribution of type IV collagen chains in the developing rat testis and ovary. Differentiation. 1998; 63:125–130.

    Article  CAS  PubMed  Google Scholar 

  9. Huet C., Pisselet C., Mandon-Pepin B., Monget P., Monniaux D. Extracellular matrix regulates ovine granulosa cell survival, proliferation and steroidogenesis: relationships between cell shape and function. J Endocrinol. 2001;169:347–360.

    Article  CAS  PubMed  Google Scholar 

  10. Le Bellego F., Pisselet C., Huet C., Monget P., Monniaux D. Laminin-α6β1 integrin interaction enhances survival and proliferation and modulates steroidogenesis of ovine granulosa cells. J Endocrinol. 2002; 172:45–59.

    Article  PubMed  Google Scholar 

  11. Gentry PA, Zareie M., Liptrap RM Fibronectin concentrations correlate with ovarian follicular size and estradiol values in equine follicular fluid. Anim Reprod Sci. 1996;45:91–102.

    Article  CAS  PubMed  Google Scholar 

  12. Berkholtz et al. In press.

  13. Ben-Ze’ev A., Amsterdam A. Regulation of cytoskeletal proteins involved in cell contact formation during differentiation of granulosa cells on extracellular matrix. Proc Natl Acad Sci U S A. 1986;83:2894–2898.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Ben-Rafael Z., Benadiva CA, Mastroianni L. Jr., et al. Collagen matrix influences the morphologic features and steroid secretion of human granulosa cells. Am J Obstet Gynecol. 1988; 159: 1570–1574.

    Article  CAS  PubMed  Google Scholar 

  15. Furman A., Rotmensch S., Dor J, et al. Culture of human granulosa cells from an in vitro fertilization program: effects of extracellular matrix on morphology and cyclic adenosine 30,50 monophosphate production. Fertil Steril. 1986;46:514–517.

    Article  CAS  PubMed  Google Scholar 

  16. Asem EK, Feng S., Stingley-Salazar SR, et al. Basal lamina of avian ovarian follicle: influence on morphology of granulosa cells in-vitro. Comp Biochem Physiol Part C. 2000;125:189–201.

    CAS  Google Scholar 

  17. Bussenot I., Ferre G., Azoulay-Barjonet C, et al. Culture of human preovulatory granulosa cells: effect of extracellular matrix on steroidogenesis. Biol Cell. 1993;77:181–186.

    Article  CAS  PubMed  Google Scholar 

  18. Carnegie JA, Byard R., Dardick I., Tsang BK Culture of granulosa cells in collagen gels: the influence of cell shape on steroidogenesis. Biol Reprod. 1988;38:881–890.

    Article  CAS  PubMed  Google Scholar 

  19. Gomes JE, Correia SC, Gouveia-Oliveira A., Cidadao AJ, Plancha CE Three-dimensional environments preserve extracellular matrix compartments of ovarian follicles and increase FSH-dependent growth. Mol Reprod Dev. 1999; 54:163–172.

    Article  CAS  PubMed  Google Scholar 

  20. Hwang DH, Kee SH, Kim K, et al. Role of reconstituted basement membrane in human granulosa cell culture. Endocr J. 2000;47:177–183.

    Article  CAS  Google Scholar 

  21. Maresh GA, Timmons TM, Dunbar BS Effects of extracellular matrix on the expression of specific ovarian proteins. Biol Reprod. 1990;43:965–976.

    Article  CAS  PubMed  Google Scholar 

  22. Amsterdam A., Rotmensch S., Furman A., Venter EA, Vlodavsky I. Synergistic effect of human chorionic gonadotropin and extracellular matrix on in vitro differentiation of human granulosa cells: progesterone production and gap junction formation. Endocrinology. 1989;124:1956–1964.

    Article  CAS  PubMed  Google Scholar 

  23. Rowley JA, Madlambayan G., Mooney DJ Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials. 1999;20:45–53.

    Article  CAS  PubMed  Google Scholar 

  24. Kidder GM, Mhawi AA Gap junctions and ovarian folliculogenesis. Reproduction. 2002;123:613–620.

    Article  CAS  PubMed  Google Scholar 

  25. Richardson MC, Slack C., Stewart IJ Rearrangement of extracellular matrix during cluster formation by human luteinising granulosa cells in culture. J Anat. 2000;196(pt 2): 243–248.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Aharoni D., Meiri I., Atzmon R., Vlodavsky I., Amsterdam A. Differential effect of components of the extracellular matrix on differentiation and apoptosis. Curr Biol. 1997;7:43–51.

    Article  CAS  PubMed  Google Scholar 

  27. Ruoslahti E., Reed JC Anchorage dependence, integrins, and apoptosis. Cell. 1994;77:477–478.

    Article  CAS  PubMed  Google Scholar 

  28. Adams JC, Watt FM Regulation of development and differentiation by the extracellular matrix. Development. 1993;117: 1183–1198.

    CAS  PubMed  Google Scholar 

  29. Bortolussi M., Zanchetta R., Doliana R, et al. Changes in the organization of the extracellular matrix in ovarian follicles during the preovulatory phase and atresia: an immunofluorescence study. BasicAppl Histochem. 1989;33:31–38.

    CAS  Google Scholar 

  30. Irving-Rodgers HF, Mussard ML, Kinder JE, Rodgers RJ Composition and morphology of the follicular basal lamina during atresia of bovine antral follicles. Reproduction. 2002;123:97–106.

    Article  CAS  PubMed  Google Scholar 

  31. Yasuda K., Hagiwara E., Takeuchi A, et al. Changes in the distribution of tenascin and fibronectin in the mouse ovary during folliculogenesis, atresia, corpus luteum formation and luteolysis. ZoologSci. 2005;22:237–245.

    CAS  Google Scholar 

  32. Hovatta O., Silye R., Abir R., Krausz T., Winston RM Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture. Hum Reprod. 1997;12:1032–1036.

    Article  CAS  PubMed  Google Scholar 

  33. Gospodarowicz D., Delgado D., Vlodavsky I. Permissive effect of the extracellular matrix on cell proliferation in vitro. Proc Natl Acad Sci U S A. 1980;77:4094–4098.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kreeger PK, Deck JW, Woodruff TK, Shea LD The in vitro regulation of ovarian follicle development using alginate-extracellular matrix gels. Biomaterials. 2006;27:714–723.

    Article  CAS  PubMed  Google Scholar 

  35. Oktay K., Karlikaya G., Akman O., Ojakian GK, Oktay M. Interaction of extracellular matrix and activin-A in the initiation of follicle growth in the mouse ovary. Biol Reprod. 2000; 63:457–461.

    Article  CAS  PubMed  Google Scholar 

  36. Kreeger PK, Woodruff TK, Shea LD Murine granulosa cell morphology and function are regulated by a synthetic Arg-Gly-Asp matrix. Mol Cell Endocrinol. 2003; 205:1–10.

    Article  CAS  Google Scholar 

  37. Furman A., Rotmensch S., Kohen F., Mashiach S., Amsterdam A. Regulation of rat granulosa cell differentiation by extracellular matrix produced by bovine corneal endothelial cells. Endocrinology. 1986;118:1878–1885.

    Article  CAS  PubMed  Google Scholar 

  38. Aten RF, Kolodecik TR, Behrman HR A cell adhesion receptor antiserum abolishes, whereas laminin and fibronectin glycoprotein components of extracellular matrix promote luteinization of cultured rat granulosa cells. Endocrinology. 1995;136:1753–1758.

    Article  CAS  PubMed  Google Scholar 

  39. Asem EK, Stingley-Salazar SR, Robinson JP, Turek JJ Effect of basal lamina on progesterone production by chicken granulosa cells in vitro—influence of follicular development. Comp Biochem Physiol Part C. 2000; 125:233–244.

    CAS  Google Scholar 

  40. Sites CK, Kessel B., LaBarbera AR Adhesion proteins increase cellular attachment, follicle-stimulating hormone receptors, and progesterone production in cultured porcine granulosa cells. Proc Soc Exp Biol Med. 1996;212:78–83.

    Article  CAS  PubMed  Google Scholar 

  41. Wang X., Otsu K., Saito H., Hiroi M., Ishikawa K. Sandwich configuration of type I collagen suppresses progesterone production in primary cultured porcine granulosa cells by reducing gene expression of cytochrome P450 cholesterol side-chain cleavage enzyme. Arch Biochem Biophys. 2000;376:117–123.

    Article  CAS  PubMed  Google Scholar 

  42. Emmen JM, Couse JF, Elmore SA, et al. In vitro growth and ovulation of follicles from ovaries of estrogen receptor (ER)α and ERβ null mice indicate a role for ERβ in follicular maturation. Endocrinology. 2005;146:2817–2826.

    Article  CAS  PubMed  Google Scholar 

  43. Rodgers RJ, Vella CA, Rodgers HF, Scott K., Lavranos TC Production of extracellular matrix, fibronectin and steroidogenic enzymes, and growth of bovine granulosa cells in anchorage independent culture. Reprod Fertil Dev. 1996;8:249–257.

    Article  CAS  PubMed  Google Scholar 

  44. O’Shea JD Heterogeneous cell types in the corpus luteum of sheep, goats and cattle. J Reprod Fertil Suppl. 1987;34:71–85.

    PubMed  Google Scholar 

  45. Kreeger PK, Fernandes NN, Woodruff TK, Shea LD. Regulation of mouse follicle development by follicle stimulating hormone in a three-dimensional in vitro culture system is dependent on follicle stage and dose. Biol Reprod. 2005; 73:942–950.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Pangas SA A novel in vitro culture system for the analysis of follicle development. Tissue Eng. 2003;9:1013–1021.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Teresa K. Woodruff PhD.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Woodruff, T.K., Shea, L.D. The Role of the Extracellular Matrix in Ovarian Follicle Development. Reprod. Sci. 14 (Suppl 8), 6–10 (2007). https://doi.org/10.1177/1933719107309818

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1177/1933719107309818

Keywords

Navigation