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BOR - Papers in Press, published online ahead of print October 23, 2002.
Biol Reprod 2002, 10.1095/biolreprod.102.008698
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Submitted June 25, 2002
Returned for revision July 24, 2002
Accepted September 5, 2002

Ovary


Oocyte-Mediated Suppression of Follicle-Stimulating Hormone- and Insulin-Like Growth Factor-Induced Secretion of Steroids and Inhibin-Related Proteins by Bovine Granulosa Cells In Vitro: Possible Role of Transforming Growth Factor {alpha}

Claire Glister 1, Nigel P. Groome 2, Philip G. Knight 1*
1 University of Reading
2 Oxford Brookes Unviersity

* To whom correspondence should be addressed. E-mail: p.g.knight{at}reading.ac.uk.

Abstract

The objective was to investigate the potential role of the oocyte in modulating proliferation and basal, FSH- and IGF-induced secretion of inhibin A (inh A), activin A (act A), follistatin (FS), estradiol (E2) and progesterone (P4) by mural bovine granulosa cells. Cells from 4- to 6-mm follicles were cultured in serum-free medium containing insulin and androstenedione, and the effects of ovine FSH and IGF analogue (LR3-IGF-1) were tested alone and in the presence of denuded bovine oocytes (2, 8 or 20 per well). Medium was changed every 48h and cultures terminated after 144h when viable cell number was determined. Results are based on combined data from 4 independent cultures and are presented for the last time period only when responses were maximal. Both FSH and IGF increased (P<0.001) secretion of inh A, act A, FS, E2 and P4 and raised cell number. In the absence of FSH or IGF, co-culture with oocytes had no effect on any of the measured hormones although cell number was increased up to 1.8-fold (P<0.0001). Addition of ocytes to FSH-stimulated cells dose-dependently suppressed (P<0.0001) inh A (6-fold), act A (5.5-fold), FS (3.6-fold), E2 (4.6-fold) and P4 (2.4-fold) with fold-suppression increasing with FSH dose (maximum suppression in parentheses above). Likewise, oocytes suppressed (P<0.001) IGF-induced secretion of inh A, act A, FS and E2 (P<0.05) but enhanced IGF-induced P4 secretion (1.7-fold; P<0.05). Given the similarity of these oocyte-mediated actions to those we observed previously following EGF treatment, we used immunocytochemistry to determine whether bovine oocytes express EGF or TGF{alpha}. Intense staining with TGF{alpha} antibody (but not with EGF antibody) was detected in oocytes both before and after co-culture. Experiments involving addition of TGF{alpha} to granulosa cells confirmed that the peptide mimicked the effects of oocytes on cell proliferation and on FSH- and IGF-induced hormone secretion. These experiments indicate that: (i) bovine oocytes secrete a factor(s) capable of modulating granulosa cell proliferation and responsiveness to FSH and IGF in terms of steroidogenesis and production of inhibin-related peptides; (ii) bovine oocytes express TGF{alpha} but not EGF; (iii) TGF{alpha} is a prime candidate for mediating the actions of oocytes on bovine granulosa cells.



Key words: Activin • Follicle • Follistatin • Granulosa cells • Inhibin


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