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J. Biol. Chem., Vol. 281, Issue 37, 27621-27632, September 15, 2006

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Matricellular Hevin Regulates Decorin Production and Collagen Assembly^*

Millicent M. Sullivan¹, Thomas H. Barker, Sarah E. Funk, Ari Karchin^¶, Neung S. Seo^||, Magnus Höök^||, Joan Sanders^¶, Barry Starcher^**, Thomas N. Wight, Pauli Puolakkainen, and E. Helene Sage²

From the Hope Heart Program, Benaroya Research Institute at Virginia Mason, Seattle, Washington 98101, the Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, Georgia 30332, the ^¶Department of Bioengineering, University of Washington, Seattle, Washington 98195, the ^||Center for Extracellular Matrix Biology, Texas A&M University System Health Science Center, Institute of Bioscience and Technology, Houston, Texas 77030, the ^**Department of Biochemistry, University of Texas Health Center, Tyler, Texas 75708, and the Department of Surgery, Helsinki Central University Hospital, P. O. Box 340, 00290 Helsinki, Finland

Matricellular proteins such as SPARC, thrombospondin 1 and 2, and tenascin C and X subserve important functions in extracellular matrix synthesis and cellular adhesion to extracellular matrix. By virtue of its reported interaction with collagen I and deadhesive activity on cells, we hypothesized that hevin, a member of the SPARC gene family, regulates dermal extracellular matrix and collagen fibril formation. We present evidence for an altered collagen matrix and levels of the proteoglycan decorin in the normal dermis and dermal wound bed of hevin-null mice. The dermal elastic modulus was also enhanced in hevin-null animals. The levels of decorin protein secreted by hevin-null dermal fibroblasts were increased by exogenous hevin in vitro, data indicating that hevin might regulate both decorin and collagen fibrillogenesis. We also report a decorin-independent function for hevin in collagen fibrillogenesis. In vitro fibrillogenesis assays indicated that hevin enhanced fibril formation kinetics. Furthermore, cell adhesion assays indicated that cells adhered differently to collagen fibrils formed in the presence of hevin. Our observations support the capacity of hevin to modulate the structure of dermal extracellular matrix, specifically by its regulation of decorin levels and collagen fibril assembly.

Received for publication, September 26, 2005 , and in revised form, June 14, 2006.

^* This work was supported in part by the National Institutes of Health (NIH) Grants GM40711 and CA109559 (to E. H. S.), as well as by grants from the Helsinki University Central Hospital Research Funds (to P. P.). 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Fig. S1.

¹ Supported by NIH postdoctoral fellowship 5F32 GM073363. Present address: Colburn Laboratory, University of Delaware, Newark, DE.

² To whom correspondence should be addressed: Hope Heart Program, Benaroya Research Institute at Virginia Mason, 1201 Ninth Ave., Seattle, WA 98101. Tel.: 206-341-1314; Fax: 206-341-1375; E-mail: hsage{at}benaroyaresearch.org.

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