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© The Rockefeller University Press, 0021-9525/1997//279 $5.00
The Journal of Cell Biology, Volume 139, Number 1, , 1997 279-293

Regulation of Tenascin-C, a Vascular Smooth Muscle Cell Survival Factor that Interacts with the _vβ₃ Integrin to Promote Epidermal Growth Factor Receptor Phosphorylation and Growth

Division of Cardiovascular Research, Research Institute, The Hospital for Sick Children and Departments of Pediatrics, Pathology, and Medicine, University of Toronto, Toronto, Ontario, Canada M5G 1X8

Tenascin-C (TN-C) is induced in pulmonary vascular disease, where it colocalizes with proliferating smooth muscle cells (SMCs) and epidermal growth factor (EGF). Furthermore, cultured SMCs require TN-C for EGF-dependent growth on type I collagen. In this study, we explore the regulation and function of TN-C in SMCs. We show that a matix metalloproteinase (MMP) inhibitor (GM6001) suppresses SMC TN-C expression on native collagen, whereas denatured collagen promotes TN-C expression in a β3 integrin– dependent manner, independent of MMPs. Floating type I collagen gel also suppresses SMC MMP activity and TN-C protein synthesis and induces apoptosis, in the presence of EGF. Addition of exogenous TN-C to SMCs on floating collagen, or to SMCs treated with GM6001, restores the EGF growth response and "rescues" cells from apoptosis. The mechanism by which TN-C facilitates EGF-dependent survival and growth was then investigated. We show that TN-C interactions with _vβ₃ integrins modify SMC shape, and EGF- dependent growth. These features are associated with redistribution of filamentous actin to focal adhesion complexes, which colocalize with clusters of EGF-Rs, tyrosine-phosphorylated proteins, and increased activation of EGF-Rs after addition of EGF. Cross-linking SMC β₃ integrins replicates the effect of TN-C on EGF-R clustering and tyrosine phosphorylation. Together, these studies represent a functional paradigm for ECM-dependent cell survival whereby MMPs upregulate TN-C by generating β₃ integrin ligands in type I collagen. In turn, _vβ₃ interactions with TN-C alter SMC shape and increase EGF-R clustering and EGF-dependent growth. Conversely, suppression of MMPs downregulates TN-C and induces apoptosis.

Abbreviations used in this paper: ECM, extracellular matrix; EGF-R, epidermal growth factor receptor; MMP, matrix metalloproteinase; SFM, serum-free medium; SMC, smooth muscle cell; TN-C, tenascin-C.

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