Differential effects of insulin-Like Growth factor-I and follicle-stimulating hormone on proliferation and differentiation of bovine cumulus cells and granulosa cells

David T. Armstrong, Ping Xia, Gillian De Gannes, Francis R. Tekpetey, Firouz Khamsi

Research output: Contribution to journalArticle

Abstract

Effects of gonadotropins and peptide growth factors on 3H-thymidine incorporation, as an indicator of proliferation of granulosa cells and cumulus cells from bovine ovarian follicles during in vitro culture, were determined. Incorporation of 3H-thymidine in cumulus cells during 24-h culture in protein-free medium was about 100-fold greater than in granulosa cells from small follicles. Small but significant (p<0.05) increases in incorporation of 3H-thymidine in cumulus cells (2.5-fold), but not in granulosa cells, resulted from addition of FSH, LH, or epidermal growth factor to culture media. Much larger, highly significant (p<0.01) increases in 3H-thymidine incorporation resulted from exposure of both cumulus cells (18-fold) and granulosa cells (6-fold) to insulin-like growth factor-I (IGF-I). Addition of IGF-I together with FSH resulted in additive increases in 3H-thymidine incorporation in granulosa cells over a wide range of each agonist. In contrast, addition of FSH markedly decreased the stimulatory effect of a maximally effective concentration of IGF-I on incorporation in cumulus cells. Addition of estradiol, either alone or with IGF-I, had no consistent effect on 3H-thymidine incorporation in either cumulus cells or granulosa cells. Differentiated functions of cumulus and granulosa cells, including cumulus expansion (an indicator of hyaluronic acid secretion) and progesterone secretion, were investigated under the same culture conditions. FSH was highly effective in stimulation of cumulus cell expansion, with maximal expansion occurring at the lowest concentration tested (0.04 μg/ml). LH was effective only at considerably higher concentrations consistent with degree of contamination with FSH. IGF-I was ineffective in inducing cumulus expansion, either alone or together with FSH. FSH and IGF-I by themselves each stimulated progesterone secretion by both cumulus and granulosa cells, with further additive stimulatory effects by the two agents in combination. On a per cell basis, cumulus cells produced considerably more progesterone than granulosa cells under both basal and hormone-stimulated conditions. The results suggest that IGF-I has a dual role m follicle regulation - that it acts additiveiy with FSH as an autocrine regulator of granulosa cell growth and, in the absence of FSH, as a paracrine regulator of cumulus cell proliferation in small antral follicles. The effect of FSH, by inducing cumulus expansion, may terminate further cumulus cell proliferation before ovulation.

Original languageEnglish (US)
Pages (from-to)331-338
Number of pages8
JournalBiology of Reproduction
Volume54
Issue number2
DOIs
StatePublished - Jan 1 1996
Externally publishedYes

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Cumulus Cells
Granulosa Cells
Follicle Stimulating Hormone
Insulin-Like Growth Factor I
Thymidine
Progesterone
Cell Proliferation
Ovarian Follicle
Serum-Free Culture Media
Hyaluronic Acid
Ovulation
Gonadotropins
Epidermal Growth Factor
Culture Media
Estradiol
Intercellular Signaling Peptides and Proteins

ASJC Scopus subject areas

  • Cell Biology

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Differential effects of insulin-Like Growth factor-I and follicle-stimulating hormone on proliferation and differentiation of bovine cumulus cells and granulosa cells. / Armstrong, David T.; Xia, Ping; De Gannes, Gillian; Tekpetey, Francis R.; Khamsi, Firouz.

In: Biology of Reproduction, Vol. 54, No. 2, 01.01.1996, p. 331-338.

Research output: Contribution to journalArticle

Armstrong, David T. ; Xia, Ping ; De Gannes, Gillian ; Tekpetey, Francis R. ; Khamsi, Firouz. / Differential effects of insulin-Like Growth factor-I and follicle-stimulating hormone on proliferation and differentiation of bovine cumulus cells and granulosa cells. In: Biology of Reproduction. 1996 ; Vol. 54, No. 2. pp. 331-338.
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