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Volume 270, Number 31, Issue of August 04, pp. 18558-18562, 1995
©1995 by The American Society for Biochemistry and Molecular Biology, Inc.
Heparin Binding by Fibronectin Module III-13 Involves Six Discontinuous Basic Residues Brought Together to Form a Cationic Cradle

(Received for publication, May 15, 1995)

Thomas F. Busby ,  W. Scott Argraves ,  Shelesa A. Brew ,  Igor Pechik ,  Gary L. Gilliland ,  Kenneth C. Ingham

The thirteenth type III domain of fibronectin binds heparin almost as well as fibronectin itself and contains a so-called heparin-binding consensus sequence, Arg^6-Arg^7-Ala^8-Arg^9 (residues 1697-1700 in plasma fibronectin). Barkalow and Schwarzbauer (Barkalow, F. J., and Schwarzbauer, J. E. (1991) J. Biol. Chem. 266, 7812-7818) showed that mutation of Arg^6-Arg^7 in domain III-13 of recombinant truncated fibronectins abolished their ability to bind heparin-Sepharose. However, synthetic peptides containing this sequence have negligible affinity for heparin (Ingham, K. C., Brew, S. A., Migliorini, M. M., and Busby, T. F.(1993) Biochemistry 32, 12548-12553). We generated a three-dimensional model of fibronectin type III-13 based on the structure of a homologous domain from tenascin. The model places Arg, Lys, and Arg parallel to and in close proximity to the Arg^6-Arg^7-Ala^8-Arg^9 motif, suggesting that these residues may also contribute to the heparin-binding site. Domain III-13 and six single-site mutants containing Ser in place of each of the above-mentioned basic residues were expressed in Escherichia coli. All of the purified mutant domains melted reversibly with a Tm near that of the wild type indicating that they were correctly folded. When fluorescein-labeled heparin was titrated at physiological ionic strength, the wild type domain increased the anisotropy in a hyperbolic fashion with a K of 5-7 µM, close to that of the natural domain obtained by proteolysis of fibronectin. The R54S mutant bound 3-fold weaker and the remaining mutants bound at least 10-fold weaker than wild type. The results point out that the Arg^6-Arg^7-Ala^8-Arg^9 consensus sequence by itself has little affinity for heparin under physiological conditions, even when presented in the context of a folded domain. Thus, the heparin-binding site in fibronectin is more complex than previously realized. It is formed by a cluster of 6 positively charged residues that are remote in the sequence but brought together on one side of domain III-13 to form a ``cationic cradle'' into which the anionic heparin molecule could fit.



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