Volume 271, Number 36, Issue of September 6, 1996 pp. 22090-22099
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.

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Characterization and Hormonal Modulation of Anticoagulant Heparan Sulfate Proteoglycans Synthesized by Rat Ovarian Granulosa Cells

(Received for publication, February 22, 1996, and in revised form, May 20, 1996)

Ghamartaj Hosseini , Jian Liu ^§ and Ariane I. de Agostini

From the  Sterility and Gynaecologic Endocrinology Clinic, Department of Gynaecology and Obstetrics, Geneva University Hospital, CH 1211 Geneva 14, Switzerland and the ^§ Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

Anticoagulant heparan sulfate proteoglycans endow the vascular endothelium with antithrombotic properties, but their role outside the vascular bed is unknown. Granulosa cells form an avascular compartment in the ovarian follicle, in which a heparin-like activity has been described. At ovulation extravascular coagulation occurs around ovulatory follicles, and after expulsion of the oocyte, a fibrin clot forms in the antral cavity. Granulosa cells synthesize two major heparan sulfate proteoglycans, whose anticoagulant nature has not been investigated. The purpose of this study was to characterize anticoagulant heparan sulfate proteoglycans synthesized by rat ovarian granulosa cells. Affinity purified ³⁵S-labeled anticoagulant heparan sulfate glycosaminoglycans represent 6.5% of the total heparan sulfate synthesized, and they contain 13% 3-O-sulfated disaccharides that are markers of the antithrombin-binding site of heparin. The biological activity of granulosa cell heparan sulfate proteoglycans was demonstrated by their ability to bind antithrombin and to accelerate the formation of thrombin-antithrombin complexes. The impact of hormonal stimulation on granulosa cell anticoagulant heparan sulfate proteoglycans was studied using ¹²⁵I-antithrombin binding assays. Folliclestimulating hormone induced a redistribution of anticoagulant heparan sulfate proteoglycans from the granulosa cell layer to the culture medium, indicating that their distribution could be modulated according to the stage of follicular development. These results suggest that anticoagulant heparan sulfate might be critically located in the follicle to maintain fluidity around the oocyte until its expulsion at ovulation.

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