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Originally published In Press as doi:10.1074/jbc.M202086200 on June 24, 2002

J. Biol. Chem., Vol. 277, Issue 37, 33545-33558, September 13, 2002
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Functions of Transforming Growth Factor-beta Family Type I Receptors and Smad Proteins in the Hypertrophic Maturation and Osteoblastic Differentiation of Chondrocytes*

Ulrich ValcourtDagger §, Jérôme GouttenoireDagger , Aristidis Moustakas, Daniel HerbageDagger , and Frédéric Mallein-GerinDagger ||

From the Dagger  Institut de Biologie et Chimie des Protéines, UMR 5086 CNRS/Université Claude Bernard Lyon 1, 7 passage du Vercors, 69367 Lyon Cedex 07, France and the  Ludwig Institute for Cancer Research, Box 595, SE-751 24 Uppsala, Sweden

We investigated the effects of bone morphogenetic protein (BMP)-2, a member of the transforming growth factor-beta superfamily, on the regulation of the chondrocyte phenotype, and we identified signaling molecules involved in this regulation. BMP-2 triggers three concomitant responses in mouse primary chondrocytes and chondrocytic MC615 cells. First, BMP-2 stimulates expression or synthesis of type II collagen. Second, BMP-2 induces expression of molecular markers characteristic of pre- and hypertrophic chondrocytes, such as Indian hedgehog, parathyroid hormone/parathyroid hormone-related peptide receptor, type X collagen, and alkaline phosphatase. Third, BMP-2 induces osteocalcin expression, a specific trait of osteoblasts. Constitutively active forms of transforming growth factor-beta family type I receptors and Smad proteins were overexpressed to address their role in this process. Activin receptor-like kinase (ALK)-1, ALK-2, ALK-3, and ALK-6 were able to reproduce the hypertrophic maturation of chondrocytes induced by BMP-2. In addition, ALK-2 mimicked further the osteoblastic differentiation of chondrocytes induced by BMP-2. In the presence of BMP-2, Smad1, Smad5, and Smad8 potentiated the hypertrophic maturation of chondrocytes, but failed to induce osteocalcin expression. Smad6 and Smad7 impaired chondrocytic expression and osteoblastic differentiation induced by BMP-2. Thus, our results indicate that Smad-mediated pathways are essential for the regulation of the different steps of chondrocyte and osteoblast differentiation and suggest that additional Smad-independent pathways might be activated by ALK-2.

* This work was supported in part by "Program Thématique Prioritaire" Grant 085113 from the Rhône-Alpes region and by "Ingénierie Tissulaire" Grant 2000-03 from CNRS-INSERM.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.

§ Supported by doctoral fellowships from the French government and from the "Fondation pour la Recherche Médicale" (Grant FDT20010920081/1). Present address: Ludwig Inst. for Cancer Research, SE-751 24 Uppsala, Sweden.

|| To whom correspondence and reprint requests should be addressed: Institut de Biologie et Chimie des Protéines, UMR 5086 CNRS/Université Claude Bernard Lyon 1, 7 passage du Vercors, 69367 Lyon Cedex 07, France. Tel.: 33-4-72-72-26-19; Fax: 33-4-72-72-26-04; E-mail: f.mallein-gerin@ibcp.fr.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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