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Originally published In Press as doi:10.1074/jbc.M207554200 on October 23, 2002

J. Biol. Chem., Vol. 278, Issue 1, 327-334, January 3, 2003
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Collagen I Initiates Endothelial Cell Morphogenesis by Inducing Actin Polymerization through Suppression of Cyclic AMP and Protein Kinase A*

Mary C. Whelan and Donald R. SengerDagger

From the Division of Cancer Biology and Angiogenesis, Department of Pathology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts 02215

Collagen I provokes endothelial cells to assume a spindle-shaped morphology and to align into solid cord-like assemblies. These cords closely imitate the solid pre-capillary cords of embryonic angiogenesis, raising interesting questions about underlying mechanisms. Studies described here identify a critical mechanism beginning with collagen I ligation of integrins alpha 1beta 1 and alpha 2beta 1, followed by suppression of cyclic AMP and cyclic AMP (cAMP)-dependent protein kinase A, and marked induction of actin polymerization to form prominent stress fibers. In contrast to collagen I, laminin-1 neither suppressed cAMP nor protein kinase A activity nor induced actin polymerization or changes in cell shape. Moreover, fibroblasts did not respond to collagen I with changes in cAMP, actin polymerization, or cell shape, thus indicating that collagen signaling, as observed in endothelial cells, does not extend to all cell types. Pharmacological elevation of cAMP blocked collagen-induced actin polymerization and formation of cords by endothelial cells; conversely, pharmacological suppression of either cAMP or protein kinase A induced actin polymerization. Collectively, these studies identify a previously unrecognized and critical mechanism, involving suppression of cAMP-dependent protein kinase A and induction of actin polymerization, through which collagen I drives endothelial cell organization into multicellular pre-capillary cords.

* This work was supported by United States Public Health Services Grant CA77357 (to D. R. S.) from NCI, National Institutes of Health, and by the V. Kann Rasmussen Foundation.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 Pathology, Research North, Beth Israel Deaconess Medical Center, 99 Brookline Ave., Boston, MA 02215. Tel.: 617-667-5766; Fax: 617-667-3591; E-mail: dsenger@caregroup.harvard.edu.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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