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J Biol Chem, Vol. 275, Issue 2, 1463-1470, January 14, 2000

Cell Density-dependent Regulation of Proteoglycan Synthesis by Transforming Growth Factor-beta 1 in Cultured Bovine Aortic Endothelial Cells*

Toshiyuki KajiDagger , Akihiro Yamada, Sawako Miyajima, Chika Yamamoto, Yasuyuki Fujiwara, Thomas N. Wight§, and Michael G. Kinsella§

From the Department of Environmental Health, Faculty of Pharmaceutical Sciences, Hokuriku University, Ho-3 Kanagawa-machi, Kanazawa 920-1181, Japan and the § Department of Pathology, School of Medicine, University of Washington, Seattle, Washington 98195-7470

The regulation of vascular endothelial cell behavior during angiogenesis and in disease by transforming growth factor-beta 1 (TGF-beta 1) is complex, but it clearly involves growth factor-induced changes in extracellular matrix synthesis. Proteoglycans (PGs) synthesized by endothelial cells contribute to the formation of the vascular extracellular matrix and also influence cellular proliferation and migration. Since the effects of TGF-beta 1 on vascular smooth muscle cell growth are dependent on cell density, it is possible that TGF-beta 1 also directs different patterns of PG synthesis in endothelial cells at different cell densities. In the present study, dense and sparse cultures of bovine aortic endothelial cells were metabolically labeled with [3H]glucosamine, [35S]sulfate, or 35S-labeled amino acids in the presence of TGF-beta 1. The labeled PGs were characterized by DEAE-Sephacel ion exchange chromatography and Sepharose CL-4B molecular sieve chromatography. The glycosaminoglycan Mr and composition were analyzed by Sepharose CL-6B chromatography, and the core protein Mr was analyzed by SDS-polyacrylamide gel electrophoresis, before and after digestion with papain, heparitinase, or chondroitin ABC lyase. These experiments indicate that the effect of TGF-beta 1 on vascular endothelial cell PG synthesis is dependent on cell density. Specifically, TGF-beta 1 induced an accumulation of small chondroitin/dermatan sulfate PGs (CS/DSPGs) with core proteins of ~50 kDa in the medium of both dense and sparse cultures, but a cell layer-associated heparan sulfate PG with a core protein size of ~400 kDa accumulated only in dense cultures. Moreover, only in the dense cell cultures did TGF-beta 1 cause CS/DSPG hydrodynamic size to increase, which was due to the synthesis of CS/DSPGs with longer glycosaminoglycan chains. The heparan sulfate PG and CS/DSPG core proteins were identified as perlecan and biglycan, respectively, by Western blot analysis. The present data suggest that TGF-beta 1 promotes the synthesis of both perlecan and biglycan when endothelial cell density is high, whereas only biglycan synthesis is stimulated when the cell density is low. Furthermore, glycosaminoglycan chains are elongated only in biglycan synthesized by the cells at a high cell density.

* This work was supported in part by Grants-in-aid for Scientific Research 07672395, 08672540, and 09672260 (to T. K.) from the Ministry of Education, Science, Sports and Culture of Japan.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger To whom correspondence should be addressed: Dept. of Environmental Health, Faculty of Pharmaceutical Sciences, Hokuriku University, Ho-3 Kanagawa-machi, Kanazawa 920-1181, Japan. Tel./Fax: 81-76-229-6208; E-mail: t-kaji@hokuriku-u.ac.jp.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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