Abstract
Fibronectin (FN) fibrillogenesis depends on the binding of FN to cellular receptors and subsequent unfolding of bound FN. Integrins αIIbβ3, αvβ3, and α5β1 are known to assemble FN fibrils on platelets. In our study, we examined the contribution of these integrins to FN binding, unfolding, and assembly on platelets in suspension and adherent platelets in the presence or absence of agonists. Phorbol 12-myristate 13-acetate (PMA), but not adenosine diphosphate (ADP), induced binding of FN to platelets in suspension. In contrast, adherent platelets were able to deposit FN on their surfaces in the absence of agonists. β3 integrins had a major impact on the interaction of FN on platelets. αvβ3 showed a similar contribution to the binding of FN as αIIbβ3 on PMA-stimulated platelets in suspension but had a lesser contribution to unfolding and deposition of FN on adherent platelets. α5β1 also participated in the interaction of FN with platelets by mediating the unfolding and assembly of FN, but to a lesser extent than β3 integrins. None of the distinct antibodies directed against one of the three integrins caused a complete inhibition of binding, unfolding, and assembly of FN by platelets. Thus, it is likely that αIIbβ3, αvβ3, and α5β1 or another still unknown receptor can be substituted.
We thank Drs. Kristopher E. Kubow and Maria Mitsi for sharing their experience in FN purification and labeling. We thank Dr. Barry S. Coller for providing 10E5 antibody. We gratefully acknowledge the support (and training) from the International NRW Research School BioStruct, granted by the Ministry of Innovation, Science and Research of the State North Rhine-Westphalia, the Heinrich-Heine-University of Düsseldorf, and the Entrepreneur Foundation at the Heinrich-Heine-University of Düsseldorf. This work was also supported by the Deutsche Forschungsgemeinschaft (SFB612, TPB2).
References
Ali, I.U. and Hynes, R.O. (1977). Effects of cytochalasin B and colchicine on attachment of a major surface protein of fibroblasts. Biochim. Biophys. Acta 471, 16–24.10.1016/0005-2736(77)90388-1Search in Google Scholar
Beaulieu, J.F. (1999). Integrins and human intestinal cell functions. Front. Biosci. 4, D310–D321.Search in Google Scholar
Bourguignon, L.Y., Walker, G., and Bourguignon, G.J. (1985). Phorbol ester-induced phosphorylation of a transmembrane glycoprotein (GP 180) in human blood platelets. J. Biol. Chem. 260, 11775–11780.10.1016/S0021-9258(17)39097-XSearch in Google Scholar
Cho, J. and Mosher, D.F. (2006). Role of fibronectin assembly in platelet thrombus formation. J Thromb. Haemost. 4, 1461–1469.10.1111/j.1538-7836.2006.01943.xSearch in Google Scholar
Engvall, E. and Ruoslahti, E. (1977). Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int. J. Cancer 20, 1–5.10.1002/ijc.2910200102Search in Google Scholar
Fogerty, F.J., Akiyama, S.K., Yamada, K.M., and Mosher, D.F. (1990). Inhibition of binding of fibronectin to matrix assembly sites by anti-integrin (α5β1) antibodies. J. Cell. Biol. 111, 699–708.10.1083/jcb.111.2.699Search in Google Scholar
Ginsberg, M., Pierschbacher, M.D., Ruoslahti, E., Marguerie, G., and Plow, E. (1985). Inhibition of fibronectin binding to platelets by proteolytic fragments and synthetic peptides which support fibroblast adhesion. J. Biol. Chem. 260, 3931–3936.10.1016/S0021-9258(18)89211-0Search in Google Scholar
Hollopeter, G., Jantzen, H.M., Vincent, D., Li, G., England, L., Ramakrishnan, V., Yang, R.B., Nurden, P., Nurden, A., Julius, D., et al. (2001). Identification of the platelet ADP receptor targeted by antithrombotic drugs. Nature 409, 202–207.10.1038/35051599Search in Google Scholar
Hynes, R.O. (1990). Fibronectins (New York: Springer-Verlag).10.1007/978-1-4612-3264-3Search in Google Scholar
Hynes, R.O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673–687.10.1016/S0092-8674(02)00971-6Search in Google Scholar
Kasirer-Friede, A., Kahn, M.L., and Shattil, S.J. (2007). Platelet integrins and immunoreceptors. Immunol. Rev. 218, 247–264.10.1111/j.1600-065X.2007.00532.xSearch in Google Scholar PubMed
Kieffer, N., Fitzgerald, L.A., Wolf, D., Cheresh, D.A., and Phillips, D.R. (1991). Adhesive properties of the β 3 integrins: comparison of GP IIb-IIIa and the vitronectin receptor individually expressed in human melanoma cells. J. Cell. Biol. 113, 451–461.10.1083/jcb.113.2.451Search in Google Scholar
Li, S., Van Den Diepstraten, C., D’Souza, S.J., Chan, B.M., and Pickering, J.G. (2003). Vascular smooth muscle cells orchestrate the assembly of type I collagen via α2β1 integrin, RhoA, and fibronectin polymerization. Am. J. Pathol. 163, 1045–1056.10.1016/S0002-9440(10)63464-5Search in Google Scholar
Mao, Y. and Schwarzbauer, J.E. (2005). Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. Matrix Biol. 24, 389–399.10.1016/j.matbio.2005.06.008Search in Google Scholar
McCarty, O.J., Zhao, Y., Andrew, N., Machesky, L.M., Staunton, D., Frampton, J., and Watson, S.P. (2004). Evaluation of the role of platelet integrins in fibronectin-dependent spreading and adhesion. J. Thromb. Haemost. 2, 1823–1833.10.1111/j.1538-7836.2004.00925.xSearch in Google Scholar
McKeown-Longo, P.J. and Mosher, D.F. (1983). Binding of plasma fibronectin to cell layers of human skin fibroblasts. J. Cell. Biol. 97, 466–472.10.1083/jcb.97.2.466Search in Google Scholar
Morgan, M.R., Humphries, M.J., and Bass, M.D. (2007). Synergistic control of cell adhesion by integrins and syndecans. Nat. Rev. Mol. Cell. Biol. 8, 957–969.10.1038/nrm2289Search in Google Scholar
Mosher, D.F. (1989). Fibronectin (San Diego: Academic Press).Search in Google Scholar
Olorundare, O.E., Peyruchaud, O., Albrecht, R.M., and Mosher, D.F. (2001). Assembly of a fibronectin matrix by adherent platelets stimulated by lysophosphatidic acid and other agonists. Blood 98, 117–124.10.1182/blood.V98.1.117Search in Google Scholar
Petersen, T.E., Thogersen, H.C., Skorstengaard, K., Vibe-Pedersen, K., Sahl, P., Sottrup-Jensen, L., and Magnusson, S. (1983). Partial primary structure of bovine plasma fibronectin: three types of internal homology. Proc. Natl. Acad. Sci. USA 80, 137–141.10.1073/pnas.80.1.137Search in Google Scholar
Plow, E.F. and Ginsberg, M.H. (1981). Specific and saturable binding of plasma fibronectin to thrombin-stimulated human platelets. J. Biol. Chem. 256, 9477–9482.10.1016/S0021-9258(19)68787-9Search in Google Scholar
Plow, E.F., McEver, R.P., Coller, B.S., Woods, V.L., Jr., Marguerie, G.A., and Ginsberg, M.H. (1985). Related binding mechanisms for fibrinogen, fibronectin, von Willebrand factor, and thrombospondin on thrombin-stimulated human platelets. Blood 66, 724–727.10.1182/blood.V66.3.724.724Search in Google Scholar
Quackenbush, J. (2002). Microarray data normalization and transformation. Nat. Genet. 32, 496–501.10.1038/ng1032Search in Google Scholar
Ruggeri, Z.M. and Mendolicchio, G.L. (2007). Adhesion mechanisms in platelet function. Circ. Res. 100, 1673–1685.10.1161/01.RES.0000267878.97021.abSearch in Google Scholar
Schwarzbauer, J.E. and DeSimone, D.W. (2011). Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harb. Perspect. Biol. 3.10.1101/cshperspect.a005041Search in Google Scholar
Sechler, J.L., Cumiskey, A.M., Gazzola, D.M., and Schwarzbauer, J.E. (2000). A novel RGD-independent fibronectin assembly pathway initiated by α4β1 integrin binding to the alternatively spliced V region. J. Cell. Sci. 113, 1491–1498.10.1242/jcs.113.8.1491Search in Google Scholar
Singh, P., Carraher, C., and Schwarzbauer, J.E. (2010). Assembly of fibronectin extracellular matrix. Annu. Rev. Cell. Dev. Biol. 26, 397–419.10.1146/annurev-cellbio-100109-104020Search in Google Scholar
Smith, M.L., Gourdon, D., Little, W.C., Kubow, K.E., Eguiluz, R.A., Luna-Morris, S., and Vogel, V. (2007). Force-induced unfolding of fibronectin in the extracellular matrix of living cells. PLoS Biol. 5, e268.10.1371/journal.pbio.0050268Search in Google Scholar
Switala-Jelen, K., Dabrowska, K., Opolski, A., Lipinska, L., Nowaczyk, M., and Gorski, A. (2004). The biological functions of β3 integrins. Folia Biol. (Praha) 50, 143–152.Search in Google Scholar
von der Mark, K. and Sorokin, L. (2003). Adhesive glycoproteins. In: Connective Tissue and Its Heritable Disorders (Hoboken, NJ, USA: John Wiley & Sons, Inc.), pp. 293–328.Search in Google Scholar
Wennerberg, K., Lohikangas, L., Gullberg, D., Pfaff, M., Johansson, S., and Fassler, R. (1996). Beta 1 integrin-dependent and independent polymerization of fibronectin. J. Cell. Biol. 132, 227–238.10.1083/jcb.132.1.227Search in Google Scholar
Wu, C., Keivens, V.M., O’Toole, T.E., McDonald, J.A., and Ginsberg, M.H. (1995). Integrin activation and cytoskeletal interaction are essential for the assembly of a fibronectin matrix. Cell 83, 715–724.10.1016/0092-8674(95)90184-1Search in Google Scholar
Wu, C., Hughes, P.E., Ginsberg, M.H., and McDonald, J.A. (1996). Identification of a new biological function for the integrin α5β3: initiation of fibronectin matrix assembly. Cell. Adhes. Commun. 4, 149–158.10.3109/15419069609014219Search in Google Scholar PubMed
Zardi, L., Cecconi, C., Barbieri, O., Carnemolla, B., Picca, M., and Santi, L. (1979). Concentration of fibronectin in plasma of tumor-bearing mice and synthesis by Ehrlich ascites tumor cells. Cancer Res. 39, 3774–3779.Search in Google Scholar
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