Laminin and fibronectin concentrations of the follicular fluid correlate with granulosa cell luteinization and oocyte quality

Abstract

Background and Aims:  Progesterone production of human cultured luteinizing granulosa cells was reported to be modified by extracellular matrix, suggesting that extracellular matrix regulates luteinization of granulosa cells after ovulation. In the present study, the relationship among laminin, fibronectin, progesterone and estradiol in follicular fluid along with oocyte quality was analyzed to estimate the physiological role of extracellular matrix in follicular luteinization and oocyte quality during ovulation.

Methods and Results:  Follicular fluid was collected at oocyte pick-up from the patients undergoing in vitro fertilization treatment and intracytoplasmic sperm injection. The concentrations of laminin, fibronectin, progesterone and estradiol in the follicular fluid were measured by enzyme immunoassay and radioimmunoassay. The morphology of oocytes were also assessed during the procedure of intracytoplasmic sperm injection and was classified into normal and abnormal groups. The fibronectin concentration was higher in the normal ooplasm group than in the abnormal group, but it did not correlate with estradiol or progesterone concentration. However, laminin concentration significantly correlated with that of progesterone, but not with cytoplasm morphology of oocytes. There was no difference in estradiol or progesterone concentration between the normal and abnormal groups.

Conclusion:  These findings suggest that extracellular matrix plays some roles in regulating human granulosa cell luteinization and oocyte quality during ovulation. (Reprod Med Biol 2004; 3: 43–49)

REFERENCES 1 Hill GA, Freeman M, Bastias MC et al. The influence of oocyte maturity and embryo quality on pregnancy rate in a program for in vitro fertilization-embryo transfer. Fertil Steril 1989; 52: 801–806. 2 Veeck LL. Abnormal morphology of the human oocyte and conceptus. In: Atlas of the Human Oocyte and Early Conceptus, Vol. 2. Baltimore: Williams & Wilkins, 1991; 151–255. 3 Adashi EY. The ovarian life cycle. In: Yen SCC, Jaffe RB (eds). Reproductive Endocrinology, 3rd edn. Philadelphia: WB Saunders, 1991; 181–237. 4 Fujiwara H, Maeda M, Ueda M et al. A differentiation-related molecule on the cell surface of human granulosa cells. J Clin Endocrinol Metab 1993; 76: 956–961. 5 Honda T, Fujiwara H, Ueda M, Maeda M, Mori T. Integrin α6 is a differentiation antigen of human granulosa cells. J Clin Endocrinol Metab 1995; 80: 2899–2905. 6 Fujiwara H, Honda T, Ueda M et al. Laminin suppresses progesterone production by human luteinizing granulosa cells via interaction with integrin α6β1. J Clin Endocrinol Metab 1997; 82: 2122–2128. 7 Nakamura K, Fujiwara H, Higuchi H et al. Integrin α6 is involved in follicular growth in mice. Biochem Biophys Res Commun 1997; 235: 524–528. 8 Honda T, Fujiwara H, Yamada S et al. Integrin α5 is expressed on human luteinizing granulosa cells during corpus luteum formation, and its expression is enhanced by hCG in vitro. Mol Hum Reprod 1997; 3: 979–984. 9 Fujiwara H, Maeda M, Honda T et al. Granulosa cells express integrin α6: Possible involvement of integrin α6 on folliculogenesis. Horm Res 1996; 46: 24–30. 10 Fujiwara H, Kataoka N, Honda T et al. Physiological roles of integrin α6β1 in ovarian functions. Horm Res 1998; 50: 25–29. 11 Fusi FM, Vignali M, Gailit J, Bronson RA. Mammalian oocytes exhibit specific recognition of the RGD (Arg-Gly-Asp) tripeptide and express oolemmal integrins. Mol Reprod Dev 1993; 36: 212–219. 12 Fujiwara H, Fukuoka M, Yasuda K et al. Cytokines stimulate dipeptidyl peptidase-IV expression on human luteinizing granulosa cells. J Clin Endocrinol Metab 1994; 79: 1007–1011. 13 Veeck LL. Oocyte assessment and biological performance. Ann NY Acad Sci 1988; 541: 259–274. 14 Dorrington JH, Skinner MK. Cytodifferentiation of granulosa cells induced by gonadotropin-releasing hormone promotes fibronectin secretion. Endocrinology 1986; 118: 2065–2071. 15 Carnegie JA. Secretion of fibronectin by rat granulosa cells occurs primarily during early follicular development. J Reprod Fertil 1990; 89: 579–589. 16 Asem EK, Carnegie JA, Tsang BK. Fibronectin production by chicken granulosa cells in vitro: effect of follicular development. Acta Endocrinol 1992; 127: 466–470. 17 Lobb DK, Dorrington JH. Human granulosa and thecal cells secrete distinct protein profiles. Fertil Steril 1987; 48: 243–248. 18 Familiari G, Verlengia C, Nottola SA et al. Heterogeneous distribution of fibronectin, tenascin-C, and laminin immunoreactive material in the cumulus-corona-cells surrounding mature human oocytes from IVF-ET protocols – evidence that they are composed of different subpopulations: an immunohistochemical study using scanning confocal laser and fluorescence microscopy. Mol Reprod Dev 1996; 43: 392–402. 19 Tsuiki A, Preyer J, Hung TT. Fibronectin and glycosaminoglycans in human preovulatory follicular fluid and their correlation to follicular maturation. Hum Reprod 1988; 3: 425–429. 20 Mori T, Suzuki A, Nishimura T, Kambegawa A. Inhibition of ovulation in immature rats by anti-progesterone antiserum. J Endocr 1977; 73: 185–186. 21 Iwamasa J, Shibata S, Tanaka N, Matsuura K, Okamura H. The relation between ovarian progesterone and proteolytic enzyme activity during ovulation in the gonadotropin-treated immature rat. Biol Reprod 1992; 46: 309–313. 22 Wassarman PM. Oogenesis. In: Adashi EY, Rock JA, Rosenwaks Z (eds). Reproductive Endocrinology, Surgery, and Technology. Philadelphia: Lippincott-Raven Publishers, 1996; 341–357. 23 Salustri A, Yanagishita M, Underhill CB, Laurent TC, Hascall VC. Localization and synthesis of hyaluronic acid in the cumulus cells and mural granulosa cells of the preovulatory follicle. Dev Biol 1992; 151: 541–551. 24 Camaioni A, Salustri A, Yanagishita M, Hascall VC. Proteoglycans and proteins in the extracellular matrix of mouse cumulus cell-oocyte complexes. Arch Biochem Biophys 1996; 325: 190–198.