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Molecular Evidence That Growth of Dominant Follicles Involves a Reduction in Follicle-Stimulating Hormone Dependence and an Increase in Luteinizing Hormone Dependence in Cattle¹

Division of Cell Sciences,³ Faculty of Veterinary Medicine, University of Glasgow, Glasgow G61 1QH, United Kingdom Department of Animal Science and Center for Animal Functional Genomics,⁴ Michigan State University, East Lansing, Michigan 48824 School of Agriculture,⁵ Food and Veterinary Science and the Conway Institute, University College Dublin, Dublin 4, Ireland

ABSTRACT

The bovine dominant follicle (DF) model was used to identify molecular mechanisms potentially involved in initial growth of DF during the low FSH milieu of ovarian follicular waves. Follicular fluid and RNA from granulosa and theca cells were harvested from 10 individual DF obtained between 2 and 5.5 days after emergence of the first follicular wave of the estrous cycle. Follicular fluid was subjected to RIA to determine estradiol (E) and progesterone (P) concentrations and RNA to cDNA microarray analysis and (or) quantitative real-time PCR. Results showed that DF growth was associated with a decrease in intrafollicular E:P ratio and in mRNA for the FSH receptor, estrogen receptor 2 (ER beta), inhibin alpha, activin A receptor type I, and a proliferation (cyclin D2) and two proapoptotic factors (apoptosis regulatory protein Siva, Fas [TNFRSF6]-associated via death domain) in granulosa cells. In contrast, mRNAs for the LH receptor in granulosa cells and for two antiapoptotic factors (TGFB1-induced antiapoptotic factor 1, LAG1 longevity assurance homolog 4 [Saccharomyces cerevisiae]) and one proapoptotic factor (tumor necrosis factor [ligand] superfamily, member 8) were increased in theca cells. We conclude that the bovine DF provides a unique model to identify novel genes potentially involved in survival and apoptosis of follicular cells and, importantly, to determine the FSH-, estradiol-, and LH-target genes regulating its growth and function. Results provide new molecular evidence for the hypothesis that DF experience a reduction in FSH dependence but acquire increased LH dependence as they grow during the low FSH milieu of follicular waves.

apoptosis, estradiol receptor, follicle-stimulating hormone receptor, follicular development, gene regulation

¹ Supported by a fellowship from the Faculty of Veterinary Medicine, University of Glasgow, BBSRC 17/S17355 and BBSRC 36727/1 to M.M. and by National Research Initiative Competitive grants 2000-02255 and 2004-01697 from the USDA Cooperative State Research, Education and Extension Service and the Agricultural Experiment Station at Michigan State University to J.J.I.

² Correspondence: M. Mihm, Division of Cell Sciences, Faculty of Veterinary Medicine, University of Glasgow, Bearsden Road, Glasgow G61 1QH, U.K. FAX: 44 141 330 5797;

¹⁰¹ m.mihm{at}vet.gla.ac.uk

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