The tyrosine kinase c-Src specifically binds to the active integrin αIIbβ3 to initiate outside-in signaling in platelets

Journal of Biological Chemistry

Volumn 290, Issue 25, 2015, Pages 15825-15834

  Wu, Yibing ^a   Span, Lisa M ^b   Nygren, Patrik ^b   Zhu, Hua ^b   Moore, David T ^b   Cheng, Hong ^c   Roder, Heinrich ^b,c   DeGrado, William F ^a   Bennett, Joel S ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING SITES; CHEMICAL ACTIVATION; CHEMICAL SHIFT; ENZYMES; INDIUM PLATING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLATELETS;

CHEMICAL SHIFT PERTURBATIONS; CYTOPLASMIC TAIL; IMMUNOPRECIPITATIONS; NEGATIVE CONTROL; PLATELET ACTIVATION; POLY PROLINES; TIME DEPENDENT; TYROSINE KINASE;

PEPTIDES;

ALPHAIIBBETA3 INTEGRIN; INTEGRIN; PEPTIDE; PROTEIN SH3; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; CSK TYROSINE-PROTEIN KINASE; FIBRINOGEN RECEPTOR; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; GENE MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOCYTE ACTIVATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; ENZYME ACTIVATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; SRC HOMOLOGY DOMAIN;

BLOOD PLATELETS; ENZYME ACTIVATION; HUMANS; PEPTIDES; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN BINDING; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; SRC-FAMILY KINASES;

EID: 84940023653     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.648428     Document Type: Article

References (34)

1. Shattil, S. J., Kashiwagi, H., and Pampori, N. (1998) Integrin signaling: the platelet paradigm. Blood 91, 2645-2657
2. Haling, J. R., Monkley, S. J., Critchley, D. R., and Petrich, B. G. (2011) Talin-dependent integrin activation is required for fibrin clot retraction by platelets. Blood 117, 1719-1722
3. Arias-Salgado, E. G., Lizano, S., Sarkar, S., Brugge, J. S., Ginsberg, M. H., and Shattil, S. J. (2003) Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proc. Natl. Acad. Sci. U.S.A. 100, 13298-13302
4. Senis, Y. A., Mazharian, A., and Mori, J. (2014) Src family kinases: at the forefront of platelet activation. Blood 124, 2013-2024
5. Yeatman, T. J. (2004) A renaissance for SRC. Nat. Rev. Cancer 4, 470-480
6. Ingley, E. (2008) Src family kinases: regulation of their activities, levels and identification of new pathways. Biochim. Biophys. Acta 1784, 56-65
7. Kim, L. C., Song, L., and Haura, E. B. (2009) Src kinases as therapeutic targets for cancer. Nature Reviews. Clinical Oncology 6, 587-595
8. Lowell, C. A., and Soriano, P. (1996) Knockouts of Src-family kinases: stiff bones, wimpy T cells, and bad memories. Genes Dev. 10, 1845-1857
9. Stehelin, D., Varmus, H. E., Bishop, J. M., and Vogt, P. K. (1976) DNA related to the transforming gene (s) of avian sarcoma viruses is present in normal avian DNA. Nature 260, 170-173
10. Obergfell, A., Eto, K., Mocsai, A., Buensuceso, C., Moores, S. L., Brugge, J. S., Lowell, C. A., and Shattil, S. J. (2002) Coordinate interactions of Csk, Src, and Syk kinases with [alpha]IIb[beta]3 initiate integrin signaling to the cytoskeleton. J. Cell Biol. 157, 265-275
11. Pumiglia, K., and Feinstein, M. (1993) Thrombin and thrombin receptor agonist peptide induce tyrosine phosphorylation and tyrosine kinases in the platelet cytoskeleton. Translocation of pp60c-src and integrin αIIb β3 (glycoprotein IIb/IIIa) is not required for aggregation, but is dependent on formation of large aggregate structures. Biochem. J. 253, 253-260
12. Clark, E. A., and Brugge, J. S. (1993) Redistribution of activated pp60c-src to integrin-dependent cytoskeletal complexes in thrombin-stimulated platelets. Mol. Cell. Biol. 13, 1863-1871
13. Xu, W., Harrison, S. C., and Eck, M. J. (1997) Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595-602
14. Xu, W., Doshi, A., Lei, M., Eck, M. J., and Harrison, S. C. (1999) Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3, 629-638
15. Sicheri, F., Moarefi, I., and Kuriyan, J. (1997) Crystal structure of the Src family tyrosine kinase Hck. Nature 385, 602-609
16. Metcalf, D. G., Moore, D. T., Wu, Y., Kielec, J. M., Molnar, K., Valentine, K. G., Wand, A. J., Bennett, J. S., and DeGrado, W. F. (2010) NMR analysis of the αIIb β3 cytoplasmic interaction suggests a mechanism for integrin regulation. Proc. Natl. Acad. Sci. U.S.A. 107, 22481-22486
17. Li, S. S. (2005) Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Biochem. J. 390, 641-653
18. Katyal, P., Puthenveetil, R., and Vinogradova, O. (2013) Structural insights into the recognition of beta3 integrin cytoplasmic tail by the SH3 domain of Src kinase. Protein Sci 22, 1358-1365
19. Moore, D. T., Nygren, P., Jo, H., Boesze-Battaglia, K., Bennett, J. S., and DeGrado, W. F. (2012) Affinity of talin-1 for the β3-integrin cytosolic domain is modulated by its phospholipid bilayer environment. Proc. Natl. Acad. Sci. U.S.A. 109, 793-798
20. Ablooglu, A. J., Kang, J., Petrich, B. G., Ginsberg, M. H., and Shattil, S. J. (2009) Antithrombotic effects of targeting αIIbß3 signaling in platelets. Blood 113, 3585-3592
21. Liao, Z., Kato, H., Pandey, M., Cantor, J. M., Ablooglu, A. J., Ginsberg, M. H., and Shattil, S. J. (2015) Interaction of kindlin-2 with integrin β3 promotes outside-in signaling responses by the αVβ3 vitronectin receptor. Blood 125, 1995-2004
22. Sparks, A. B., Quilliam, L. A., Thorn, J. M., Der, C. J., and Kay, B. K. (1994) Identification and characterization of Src SH3 ligands from phage-displayed random peptide libraries. J. Biol. Chem. 269, 23853-23856
23. Rickles, R. J., Botfield, M. C., Zhou, X. M., Henry, P. A., Brugge, J. S., and Zoller, M. J. (1995) Phage display selection of ligand residues important for Src homology 3 domain binding specificity. Proc. Natl. Acad. Sci. U.S.A. 92, 10909-10913
24. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol NMR 6, 277-293
25. Yu, H., Rosen, M. K., and Schreiber, S. L. (1993) 1H and 15N assignments and secondary structure of the Src SH3 domain. FEBS Lett. 324, 87-92
26. Schumann, F. H., Riepl, H., Maurer, T., Gronwald, W., Neidig, K. P., and Kalbitzer, H. R. (2007) Combined chemical shift changes and amino acid specific chemical shift mapping of protein-protein interactions. J. Biomol NMR 39, 275-289
27. Williamson, M. P. (2013) Using chemical shift perturbation to characterise ligand binding. Progress in Nuclear Magnetic Resonance Spectroscopy 73, 1-16
28. Yu, H., Chen, J. K., Feng, S., Dalgarno, D. C., Brauer, A. W., and Schreiber, S. L. (1994) Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76, 933-945
29. Xiao, R., Xi, X. D., Chen, Z., Chen, S. J., and Meng, G. (2013) Structural framework of c-Src activation by integrin β3. Blood 121, 700-706
30. Law, D. A., DeGuzman, F. R., Heiser, P., Ministri-Madrid, K., Killeen, N., and Phillips, D. R. (1999) Integrin cytoplasmic tyrosine motif is required for outside-in αIIbß3 signaling and platelet function. Nature 401, 808-911
31. Arias-Salgado, E. G., Haj, F., Dubois, C., Moran, B., Kasirer-Friede, A., Furie, B. C., Furie, B., Neel, B. G., and Shattil, S. J. (2005) PTP-1B is an essential positive regulator of platelet integrin signaling. J. Cell Biol. 170, 837-845
32. Resh, M. D. (1999) Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta 1451, 1-16
33. Satoh, K., Matsuki-Fukushima, M., Qi, B., Guo, M. Y., Narita, T., Fujita-Yoshigaki, J., and Sugiya, H. (2009) Phosphorylation of myristoylated alanine-rich C kinase substrate is involved in the cAMP-dependent amylase release in parotid acinar cells. American Journal of Physiology. Gastrointestinal and Liver Physiology 296, G1382-1390
34. Pérez, Y., Maffei, M., Igea, A., Amata, I., Gairí, M., Nebreda, A. R., Bernadó, P., and Pons, M. (2013) Lipid binding by the Unique and SH3 domains of c-Src suggests a new regulatory mechanism. Scientific Reports 3, 1295