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J. Biol. Chem., Vol. 282, Issue 49, 35887-35898, December 7, 2007

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Decorin-transforming Growth Factor-β Interaction Regulates Matrix Organization and Mechanical Characteristics of Three-dimensional Collagen Matrices^*

Zannatul Ferdous, Victoria Mariko Wei, Renato Iozzo, Magnus Höök^¶, and Kathryn Jane Grande-Allen¹

From the Department of Bioengineering, Rice University, Houston, Texas 77005, the Department of Pathology, Anatomy and Cell Biology, and the Kimmel Cancer Center, Thomas Jefferson University, Philadelphia, Pennsylvania 19107, and the ^¶Center for Extracellular Matrix Biology, Texas A&M University System Health Science Center, Institute of Bioscience and Technology, Houston, Texas 77030

The small leucine-rich proteoglycan decorin has been demonstrated to be a key regulator of collagen fibrillogenesis; decorin deficiencies lead to irregularly shaped collagen fibrils and weakened material behavior in postnatal murine connective tissues. In an in vitro investigation of the contributions of decorin to tissue organization and material behavior, model tissues were engineered by seeding embryonic fibroblasts, harvested from 12.5–13.5 days gestational aged decorin null (Dcn^-/-) or wild-type mice, within type I collagen gels. The resulting three-dimensional collagen matrices were cultured for 4 weeks under static tension. The collagen matrices seeded with Dcn^-/- cells exhibited greater contraction, cell density, ultimate tensile strength, and elastic modulus than those seeded with wild-type cells. Ultrastructurally, the matrices seeded with Dcn^-/- cells contained a greater density of collagen. The decorin-null tissues contained more biglycan than control tissues, suggesting that this related proteoglycan compensated for the absence of decorin. The effect of transforming growth factor-β (TGF-β), which is normally sequestered by decorin, was also investigated in this study. The addition of TGF-β1 to the matrices seeded with wild-type cells improved their contraction and mechanical strength, whereas blocking TGF-β1 in the Dcn^-/- cell-seeded matrices significantly reduced the collagen gel contraction. These results indicate that the inhibitory interaction between decorin and TGF-β1 significantly influenced the matrix organization and material behavior of these in vitro model tissues.

Received for publication, June 25, 2007 , and in revised form, September 13, 2007.

^* This work was supported by National Institutes of Health Grant R03EB005444. 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.

¹ To whom correspondence should be addressed: MS 142, Rice University, P. O. Box 1892, Houston, TX 77251-1892. Tel.: 713-348-3704; Fax: 713-348-5877; E-mail: grande{at}rice.edu.

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