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J. Biol. Chem., Vol. 282, Issue 11, 8011-8018, March 16, 2007

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Identification of a Novel Chondroitin-sulfated Collagen in the Membrane Separating Theca and Granulosa Cells in Chicken Ovarian Follicles

THE GRANULOSA-THECA CELL INTERFACE IS NOT A BONA FIDE BASEMENT MEMBRANE^*

Susanna Hummel¹, Sabine Christian¹, Andreas Osanger, Hans Heid, Johannes Nimpf, and Wolfgang J. Schneider²

From the Department of Medical Biochemistry, Max F. Perutz Laboratories, Medical University of Vienna, Dr. Bohr Gasse 9/2, A-1030 Vienna, Austria and the Deutsches Krebsforschungszentrum Heidelberg, D-69120 Heidelberg, Germany

The membranous structure separating the granulosa from theca cells in the developing ovarian follicles of birds is generally perceived as a genuine basement membrane (BM). Previously, we suggested that this membrane is unusual in that it lacks several typical BM components, e.g. collagen IV, laminin B, perlecan, and fibronectin (Hummel, S., Osanger, A., Bajari, T. M., Balasubramani, M., Halfter, W., Nimpf, J., and Schneider, W. J. (2004) J. Biol. Chem. 279, 23486–23494). We have now identified a novel chondroitin sulfate-modified collagen, tentatively termed ggBM1 (Gallus gallus basement membrane protein1) as a major component of the border between the vascularized theca and the epitheloid granulosa cells. In biosynthetic experiments using [³H]proline and [³⁵S]sulfate, ggBM1 was shown to be synthesized by and secreted from the granulosa cells that support the developing oocyte. The acidic heterogeneous 135-kDa proteoglycan was converted to a protein with an apparent M_r of 95,000 by treatment with chondroitinase ABC and was completely degraded by collagenase. Sequencing of tryptic fragments revealed peptides typical of collagens. The follicular BM accumulated apolipoprotein B and apo-VLDLII, the major resident proteins of the yolk precursor very low density lipoprotein. Interestingly, and likely indicating an analogous situation to the follicle, ggBM1 is also a component of Bruch's membrane of the eye, which separates the vascularized choroid from retinal pigmented epithelial cells. Based on our data we propose that in addition to thecal perlecan, ggBM1 is involved in the transfer of yolk precursors from the thecal capillary bed to oocyte surface lipoprotein receptors mediating their uptake into oocytes.

Received for publication, June 23, 2006 , and in revised form, November 13, 2006.

^* This work was supported by research grants from the Austrian Science Foundation (FWF F-0608) and the Herzfelder Family Endowment. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement"in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ These authors contributed equally to this work.

² To whom correspondence should be addressed: Dept. of Medical Biochemistry, Dr. Bohr Gasse 9/2, A-1030 Vienna, Austria. Tel.: 43-1-4277-61803; Fax: 43-1-4277-61804; E-mail: wolfgang.schneider{at}meduniwien.ac.at.

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