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J. Biol. Chem., Vol. 278, Issue 43, 42200-42207, October 24, 2003

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-Helical Coiled-coil Oligomerization Domains Are Almost Ubiquitous in the Collagen Superfamily^*

Audrey McAlinden, Thomasin A. Smith, Linda J. Sandell, Damien Ficheux¶, David A. D. Parry, and David J. S. Hulmes¶||

From the Department of Orthopedic Surgery, Washington University School of Medicine, Barnes-Jewish Hospital, St. Louis, Missouri 63110, Institute of Fundamental Sciences, Massey University, Palmerston North, New Zealand, and ^¶Institut de Biologie et Chimie des Protéines, CNRS UMR 5086, Université Claude Bernard Lyon 1, 69367 Lyon Cedex 7, France

-Helical coiled coils are widely occurring protein oligomerization motifs. Here we show that most members of the collagen superfamily contain short, repeating heptad sequences typical of coiled coils. Such sequences are found at the N-terminal ends of the C-propeptide domains in all fibrillar procollagens. When fused C-terminal to a reporter molecule containing a collagen-like sequence that does not spontaneously trimerize, the C-propeptide heptad repeats induced trimerization. C-terminal heptad repeats were also found in the oligomerization domains of the multiplexins (collagens XV and XVIII). N-terminal heptad repeats are known to drive trimerization in transmembrane collagens, whereas fibril-associated collagens with interrupted triple helices, as well as collagens VII, XIII, XXIII, and XXV, were found to contain heptad repeats between collagen domains. Finally, heptad repeats were found in the von Willebrand factor A domains known to be involved in trimerization of collagen VI, as well as in collagen VII. These observations suggest that coiled-coil oligomerization domains are widely used in the assembly of collagens and collagen-like proteins.

Received for publication, March 10, 2003 , and in revised form, July 22, 2003.

^* This work was supported by the CNRS Programme "Protéomique et Ingeniérie des Protéines" and National Institutes of Health Grants AR48250-01 (to A. M.) and AR-36994 (to L. J. S.). 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.

^|| To whom correspondence should be addressed: IBCP, 7 Passage du Vercors, 69367 Lyon Cedex 07, France. Tel.: 33 472722667; Fax: 33 472722604; E-mail: d.hulmes{at}ibcp.fr.

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