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J. Biol. Chem., Vol. 279, Issue 51, 53331-53337, December 17, 2004

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Type V Collagen Controls the Initiation of Collagen Fibril Assembly^*

Richard J. Wenstrup, Jane B. Florer, Eric W. Brunskill¶, Sheila M. Bell, Inna Chervoneva||, and David E. Birk**

From the Cincinnati Children's Hospital Research Foundation, Cincinnati, Ohio 45229, ^¶Department of Internal Medicine, University of Cincinnati, Cincinnati, Ohio 45267-0555, and Departments of^||Medicine and Pathology and ^**Anatomy and Cell Biology, Thomas Jefferson University, Philadelphia, Pennsylvania 19107

Vertebrate collagen fibrils are heterotypically composed of a quantitatively major and minor fibril collagen. In non-cartilaginous tissues, type I collagen accounts for the majority of the collagen mass, and collagen type V, the functions of which are poorly understood, is a minor component. Type V collagen has been implicated in the regulation of fibril diameter, and we reported recently preliminary evidence that type V collagen is required for collagen fibril nucleation (Wenstrup, R. J., Florer, J. B., Cole, W. G., Willing, M. C., and Birk, D. E. (2004) J. Cell. Biochem. 92, 113–124). The purpose of this study was to define the roles of type V collagen in the regulation of collagen fibrillogenesis and matrix assembly. Mouse embryos completely deficient in pro-1(V) chains were created by homologous recombination. The col5a1–/– animals die in early embryogenesis, at approximately embryonic day 10. The type V collagen-deficient mice demonstrate a virtual lack of collagen fibril formation. In contrast, the col5a1+/– animals are viable. The reduced type V collagen content is associated with a 50% reduction in fibril number and dermal collagen content. In addition, relatively normal, cylindrical fibrils are assembled with a second population of large, structurally abnormal collagen fibrils. The structural properties of the abnormal matrix are decreased relative to the wild type control animals. These data indicate a central role for the evolutionary, ancient type V collagen in the regulation of fibrillogenesis. The complete dependence of fibril formation on type V collagen is indicative of the critical role of the latter in early fibril initiation. In addition, this fibril collagen is important in the determination of fibril structure and matrix organization.

Received for publication, August 20, 2004 , and in revised form, September 16, 2004.

^* This work was supported by National Institutes of Health Grants AR47054 (to R. J. W.) and EY05129 (to D. E. B.). 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: Div. of Human Genetics, Children's Hospital Research Foundation, 3333 Burnet Ave., ML 4006, Cincinnati, OH 45229-3039. Tel.: 513-636-2438; Fax: 513-636-2261. E-mail: richard.wenstrup{at}cchmc.org.

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