Protease-activated receptor 4 uses anionic residues to interact with α-thrombin in the absence or presence of protease-activated receptor 1

Biochemistry

Volumn 47, Issue 50, 2008, Pages 13279-13286

  Nieman, Marvin T ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSEL PROSTHESES; CALCIUM;

ACTIVATED RECEPTORS; ANIONIC CLUSTERS; CALCIUM FLUXES; LESSER EXTENTS; POINT MUTATIONS;

ELECTRIC CONDUCTIVITY MEASUREMENT;

ASPARTIC ACID; GAMMA THROMBIN; GLUTAMIC ACID; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 4; THROMBIN;

ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; HUMAN; HUMAN CELL; MUTATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; ANIONS; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; POINT MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, PAR-1; RECEPTORS, THROMBIN; THROMBIN;

EID: 57649115436     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801334s     Document Type: Article

References (31)

1. Coughlin, S. R. (2000) Thrombin signalling and protease-activated receptors. Nature 407, 258-264.
2. Steinhoff, M., Buddenkotte, J., Shpacovitch, V., Rattenholl, A., Moormann, C., Vergnolle, N., Luger, T. A., and Hollenberg, M. D. (2005) Proteinase-activated receptors: Transducers of proteinase-mediated signaling in inflammation and immune response. Endocr. Rev. 26, 1-43.
3. Kahn, M. L., Nakanishi-Matsui, M., Shapiro, M. J., Ishihara, H., and Coughlin, S. R. (1999) Protease-activated receptors 1 and 4 mediate activation of human platelets by thrombin. J. Clin. Invest. 103, 879-887.
4. 2+ mobilization. J. Biol. Chem. 282, 5478-5487.
5. Covic, L., Singh, C., Smith, H., and Kuliopulos, A. (2002) Role of the PAR4 thrombin receptor in stabilizing platelet-platelet aggregates as revealed by a patient wkh Hermansky-Pudlak syndrome. Thromb. Haemostasis 87, 722-727.
6. 2+ mobilization and synergistic P2Y12 receptor activation. J. Biol. Chem. 281, 26665-26674.
7. Holinstat, M., Voss, B., Bilodeau, M. L., and Hamm, H. E. (2007) Protease-activated receptors differentially regulate human platelet activation through a phosphatide acid-dependent pathway. Mol. Pharmacol. 71, 686-694.
8. Voss, B., McLaughlin, J. N., Holinstat, M., Zent, R., and Hamm, H. E. (2007) PAR1, but not PAR4, activates human platelets through a Gi/o/phosphoinositide-3 kinase signaling axis. Mol. Pharmacol. 71, 1399-1406.
9. Slofstra, S. H., Bijlsma, M. F., Groot, A. P., Reitsma, P. H., Lindhout, T., ten Cate, H., and Spek, C. A. (2007) Protease-activated receptor-4 inhibition protects from multiorgan failure in a murine model of systemic inflammation. Blood 110, 3176-3182.
10. Vergnolle, N., Derian, C. K., D'Andrea, M. R., Steinhoff, M., and Andrade-Gordon, P. (2002) Characterization of thrombin-induced leukocyte rolling and adherence: A potential proinflammatory role for proteinase-activated receptor-4. J. Immunol. 169, 1467-1473.
11. Vu, T. K., Hung, D. T., Wheaton, V. I., and Coughlin, S. R. (1991) Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64, 1057-1068.
12. Liu, L. W., Vu, T. K., Esmon, C. T., and Coughlin, S. R. (1991) The region of the thrombin receptor resembling hirudin binds to thrombin and alters enzyme specificity. J. Biol. Chem. 266, 16977- 16980.
13. Ayala, Y. M., Cantwell, A. M., Rose, T., Bush, L. A., Arosio, D., and Di Cera, E. (2001) Molecular mapping of thrombin-receptor interactions. Proteins 45, 107-116.
14. Jacques, S. L., LeMasurier, M., Sheridan, P. J., Seeley, S. K., and Kuliopulos, A. (2000) Substrate-assisted catalysis of the PAR1 thrombin receptor. Enhancement of macromolecular association and cleavage. J. Biol. Chem. 275, 40671-40678.
15. Vu, T. K., Wheaton, V. I., Hung, D. T., Charo, I., and Coughlin, S. R. (1991) Domains specifying thrombin-receptor interaction. Nature 353, 674-677.
16. Xu, W. F., Andersen, H., Whitmore, T. E., Presnell, S. R., Yee, D. P., Ching, A., Gilbert, T., Davie, E. W., and Foster, D. C. (1998) Cloning and characterization of human protease-activated receptor 4. Proc. Natl. Acad. Sci. U.S.A. 95, 6642-6646.
17. Nieman, M. T., and Schmaier, A. H. (2007) Interaction of thrombin widi PAR1 and PAR4 at the thrombin cleavage site. Biochemistry 46, 8603-8610.
18. Jacques, S. L., and Kuliopulos, A. (2003) Protease-activated receptor-4 uses dual prolines and an anionic retention motif for thrombin recognition and cleavage. Biochem. J. 376, 733-740.
19. Cleary, D. B., Trumbo, T. A., and Maurer, M. C. (2002) Protease-activated receptor 4-like peptides bind to thrombin through an optimized interaction widi the enzyme active site surface. Arch. Biochem. Biophys. 403, 179-188.
20. Leger, A. J., Jacques, S. L., Badar, J., Kaneider, N. C., Derian, C. K., Andrade-Gordon, P., Covic, L., and Kuliopulos, A. (2006) Blocking the protease-activated receptor 1-4 heterodimer in platelet-mediated thrombosis. Circulation 113, 1244-1254.
21. Nakanishi-Matsui, M., Zheng, Y. W., Sulciner, D. J., Weiss, E. J., Ludeman, M. J., and Coughlin, S. R. (2000) PAR3 is a cofactor for PAR4 activation by thrombin. Nature 404, 609-613.
22. Rydel, T. J., Yin, M., Padmanabhan, K. P., Blankenship, D. T., Cardin, A. D., Correa, P. E., Fenton, J. W., and Tulinsky, A. (1994) Crystallographic structure of human y-thrombin. J. Biol Chem. 269, 22000-22006.
23. Hasan, A. A., Warnock, M., Nieman, M., Srikandi, S., Mahdi, F., Krishnan, R., Tulinsky, A., and Schmaier, A. H. (2003) Mechanisms of Arg-Pro-Pro-Gly-Phe inhibition of thrombin. Am. J. Physiol. 285, H183-H193.
24. Nieman, M. T., Pagan-Ramos, E., Warnock, M., Krijanovski, Y., Hasan, A. A., and Schmaier, A. H. (2005) Mapping the interaction of bradykinin 1-5 with the exodomain of human protease activated receptor 4. FEBS Lett. 579, 25-29.
25. Hirt, R. P., Poulain-Godefroy, O., Billotte, J., Kraehenbuhl, J. P., and Fasel, N. (1992) Highly inducible synthesis of heterologous proteins in epithelial cells carrying a glucocorticoid-responsive vector. Gene 111, 199-206.
26. Islam, S., Carey, T. E., Wolf, G. T., Wheelock, M. J., and Johnson, K. R. (1996) Expression of N-cadherin by human squamous carcinoma cells induces a scattered fibroblastic phenotype with disrupted cell-cell adhesion. J. Cell Biol. 135, 1643-1654.
27. Nieman, M. T., Warnock, M., Hasan, A. A., Mahdi, F., Lucchesi, B. R., Brown, N. J., Murphey, L. J., and Schmaier, A. H. (2004) The preparation and characterization of novel peptide antagonists to thrombin and factor VIIa and activation of protease-activated receptor 1. J. Pharmacol Exp. Ther. 311, 492-501.
28. Johnson, M. L., and Faunt, L. M. (1992) Parameter estimation by least-squares mediods. Methods Enzymol 210, 1-37.
29. Beechem, J. M. (1992) Global analysis of biochemical and biophysical data. Methods Enzymol. 210, 37-54.
30. Myles, T., Le Bonniec, B. F., and Stone, S. R. (2001) The dual role of thrombin's anion-binding exosite-I in the recognition and cleavage of the protease-activated receptor 1. Eur. J. Biochem. 268, 70-77.
31. Bah, A., Chen, Z., Bush-Pelc, L. A., Mathews, F. S., and Di Cera, E. (2007) Crystal structures of murine thrombin in complex with the extracellular fragments of murine protease-activated receptors PAR3 and PAR4. Proc. Natl. Acad. Sci. U.S.A. 104, 11603-11608.