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J. Biol. Chem., Vol. 283, Issue 3, 1234-1242, January 18, 2008

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A Secreted Collagen- and Fibronectin-binding Streptococcal Protein Modulates Cell-mediated Collagen Gel Contraction and Interstitial Fluid Pressure^*

Åsa Lidén¹, Tijs van Wieringen¹, Jonas Lannergård^¶, Anja Kassner^||, Dick Heinegård^||, Rolf K. Reed, Bengt Guss^¶, and Kristofer Rubin²

From the Department of Medical Biochemistry and Microbiology, Uppsala University, BMC, Box 582, SE-751 23 Uppsala, Sweden, the Department of Biomedicine, University of Bergen, Jonas Lies vei 91, N-5009 Bergen, Norway, the ^¶Department of Microbiology, Swedish University of Agricultural Sciences, Box 7025, SE-750 07 Uppsala, Sweden, and the ^||Department of Experimental Medical Sciences, BMC, B-12, University of Lund, SE-221 84 Lund, Sweden

Fibroblast-mediated collagen gel contraction depends on collagen-binding β1 integrins. Perturbation of these integrins reveals an alternative contraction process that is integrin Vβ3-dependent and platelet-derived growth factor (PDGF) BB-stimulated. Connective tissue cells actively control interstitial fluid pressure (IFP), and inflammation-induced lowering of IFP provides a driving force for edema formation. PDGF-BB normalizes a lowered IFP by an Vβ3-dependent process. A potential modulation of IFP by extracellular matrix-binding bacterial proteins has previously not been addressed. The fibronectin (FN)-binding protein FNE is specifically secreted by the highly virulent Streptococcus equi subspecies equi. FNE bound FN and native collagen type I with K_d values of 20 and 50 nM determined by solid-phase binding assays. Rotary shadowing revealed a single FNE binding site located at on average 122 nm from the C terminus of procollagen type I. FNE induced Vβ3-mediated contraction by C2C12 cells in a concentration-dependent manner having a maximal effect at 100 nM. This activity of FNE required cellular FN, and FNE acted synergistically to added plasma FN or PDGF-BB. FNE enhanced binding of soluble FN to immobilized collagen, and conversely the binding of collagen to immobilized FN. Marked bell-shaped concentration dependences for these interactions suggest that FNE forms a bridge between FN and collagen. Finally, FNE normalized dermal IFP lowered by anaphylaxis. Our data suggest that secreted FNE normalized lowering of IFP by stimulating connective tissue cell contraction.

Received for publication, June 12, 2007 , and in revised form, October 5, 2007.

^* This study was supported in part by grants from the Swedish Cancer Foundation (to K. R.), the Swedish Research Council (to K. R. and D. H.), the Gustaf V:s 80-årsfond (to K. R. and D. H.), the Research Council of Norway (to R. K. R.), the AgriFunGen program at the Swedish University of Agricultural Sciences (to B. G.), the Swedish Horse Board (SSH:0447057) (to B. G.), and the Anna-Greta Crafoord Foundation (to A. K.). 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 Both authors contributed equally to the work.

² To whom correspondence should be addressed: Dept. of Medical Biochemistry and Microbiology, BMC, Box 582, SE-751 23 Uppsala, Sweden. Tel.: 46-18-471-41-16; Fax: 46-18-471-46-73; E-mail: Kristofer.Rubin{at}imbim.uu.se.

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