Protease-activated receptor 1 (PAR1) and PAR4 heterodimers are required for PAR1-enhanced cleavage of PAR4 by α-thrombin

Journal of Biological Chemistry

Volumn 288, Issue 45, 2013, Pages 32553-32562

  Arachiche, Amal ^a   Mumaw, Michele M ^a   De La Fuente, María ^a   Nieman, Marvin T ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; DYNAMIC INTERACTION; G PROTEIN COUPLED RECEPTORS; HETERODIMER FORMATION; PLATELET AGONISTS; PROTEASE ACTIVATED RECEPTORS; STRONG INTERACTION; TRANSMEMBRANE HELICES;

CARDIOVASCULAR SYSTEM; CELL MEMBRANES; ENZYME ACTIVITY; PLATELETS;

BIOMOLECULES;

HETERODIMER; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 4; THROMBIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TRANSMEMBRANE HELIX 4;

BIOLUMINESCENCE RESONANCE ENERGY TRANSFER (BRET); G-PROTEIN-COUPLED RECEPTORS (GPCR); PAR1; PAR4; PROTEASE-ACTIVATED RECEPTOR; PROTEIN-PROTEIN INTERACTIONS; RECEPTOR REGULATION; THROMBIN;

ALLOSTERIC REGULATION; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; HEK293 CELLS; HELA CELLS; HIRUDINS; HUMANS; PEPTIDE FRAGMENTS; POINT MUTATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEOLYSIS; RECEPTOR, PAR-1; RECEPTORS, THROMBIN; THROMBIN;

EID: 84887491969     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.472373     Document Type: Article

References (49)

1. Coughlin, S. R. (2005) Protease-activated receptors in hemostasis, thrombosis, and vascular biology. J. Thromb. Haemost. 3, 1800-1814
2. Leger, A. J., Covic, L., and Kuliopulos, A. (2006) Protease-activated receptors in cardiovascular diseases. Circulation 114, 1070-1077
3. Riewald, M., and Ruf, W. (2005) Protease-activated receptor-1 signaling by activated protein C in cytokine-perturbed endothelial cells is distinct from thrombin signaling. J. Biol. Chem. 280, 19808-19814
4. Russo, A., Soh, U. J., Paing, M. M., Arora, P., and Trejo, J. (2009) Caveolae are required for protease-selective signaling by protease-activated receptor- 1. Proc. Natl. Acad. Sci. U.S.A. 106, 6393-6397
5. Soh, U. J., and Trejo, J. (2011) Activated protein C promotes proteaseactivated receptor-1 cytoprotective signaling through β-arrestin and dishevelled- 2 scaffolds. Proc. Natl. Acad. Sci. U.S.A. 108, E1372-E1380
6. Bae, J. S., Yang, L., Manithody, C., and Rezaie, A. R. (2007) The ligand occupancy of endothelial protein C receptor switches the protease-activated receptor 1-dependent signaling specificity of thrombin from a permeability- enhancing to a barrier-protective response in endothelial cells. Blood 110, 3909-3916
7. Tricoci, P., Huang, Z., Held, C., Moliterno, D. J., Armstrong, P. W., Van de Werf, F., White, H. D., Aylward, P. E., Wallentin, L., Chen, E., Lokhnygina, Y., Pei, J., Leonardi, S., Rorick, T. L., Kilian, A. M., Jennings, L. H., Ambrosio, G., Bode, C., Cequier, A., Cornel, J. H., Diaz, R., Erkan, A., Huber, K., Hudson, M. P., Jiang, L., Jukema, J. W., Lewis, B. S., Lincoff, A. M., Montalescot, G., Nicolau, J. C., Ogawa, H., Pfisterer, M., Prieto, J. C., Ruzyllo, W., Sinnaeve, P. R., Storey, R. F., Valgimigli, M., Whellan, D. J., Widimsky, P., Strony, J., Harrington, R. A., and Mahaffey, K. W. (2012) Thrombin- Receptor Antagonist Vorapaxar in Acute Coronary Syndromes. N. Engl. J. Med. 366, 20-33
8. Zhang, C., Srinivasan, Y., Arlow, D. H., Fung, J. J., Palmer, D., Zheng, Y., Green, H. F., Pandey, A., Dror, R. O., Shaw, D. E., Weis, W. I., Coughlin, S. R., and Kobilka, B. K. (2012) High-resolution crystal structure of human protease-activated receptor 1. Nature 492, 387-392
9. Holinstat, M., Voss, B., Bilodeau, M. L., McLaughlin, J. N., Cleator, J., and Hamm, H. E. (2006) PAR4, but not PAR1, signals human platelet aggregation via Ca2+ mobilization and synergistic P2Y12 receptor activation. J. Biol. Chem. 281, 26665-26674
10. 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
11. 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
12. Covic, L., Gresser, A. L., and Kuliopulos, A. (2000) Biphasic kinetics of activation and signaling for PAR1 and PAR4 thrombin receptors in platelets. Biochemistry 39, 5458-5467
13. 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 with Hermansky-Pudlak syndrome. Thromb. Haemost. 87, 722-727
14. Mazharian, A., Roger, S., Berrou, E., Adam, F., Kauskot, A., Nurden, P., Jandrot-Perrus, M., and Bryckaert, M. (2007) Protease-activating receptor- 4 induces full platelet spreading on a fibrinogen matrix. Involvement of ERK2 and p38 and Ca2+ mobilization. J. Biol. Chem. 282, 5478-5487
15. de la Fuente, M., Noble, D. N., Verma, S., and Nieman, M. T. (2012) Mapping human protease-activated receptor 4 (PAR4) homodimer interface to transmembrane helix 4. J. Biol. Chem. 287, 10414-10423
16. Nieman, M. T. (2008) Protease-activated receptor 4 uses anionic residues to interact with α-thrombin in the absence or presence of protease-activated receptor 1. Biochemistry 47, 13279-13286
17. 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
18. Nieman, M. T., and Schmaier, A. H. (2007) Interaction of thrombin with PAR1 and PAR4 at the thrombin cleavage site. Biochemistry 46, 8603-8610
19. 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
20. 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
21. Kamath, P., Huntington, J. A., and Krishnaswamy, S. (2010) Ligand binding shuttles thrombin along a continuum of zymogen- and proteinase-like states. J. Biol. Chem. 285, 28651-28658
22. Huntington, J. A. (2012) Thrombin plasticity. Biochim. Biophys. Acta 1824, 246-252
23. 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
24. Kahn, M. L., Zheng, Y. W., Huang, W., Bigornia, V., Zeng, D., Moff, S., Farese, R. V., Jr., Tam, C., and Coughlin, S. R. (1998) A dual thrombin receptor system for platelet activation. Nature 394, 690-694
25. 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
26. Schechter, I., and Berger, A. (1967) On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162
27. Ballesteros, J. A., and Weinstein, H. (1995) Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors. Methods Neurosci. 25, 366-428
28. Arachiche, A., de la Fuente, M., and Nieman, M. T. (2013) Calcium mobilization and protein kinase C activation downstream of protease-activated receptor 4 (PAR4) is negatively regulated by PAR3 in mouse platelets. PLoS ONE 8, e55740
29. Grynkiewicz, G., Poenie, M., and Tsien, R. Y. (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450
30. McLaughlin, J. N., Patterson, M. M., and Malik, A. B. (2007) Proteaseactivated receptor-3 (PAR3) regulates PAR1 signaling by receptor dimerization. Proc. Natl. Acad. Sci. U.S.A. 104, 5662-5667
31. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003) SWISSMODEL. An automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385
32. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISSMODEL workspace. A web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201
33. Bordoli, L., Kiefer, F., Arnold, K., Benkert, P., Battey, J., and Schwede, T. (2009) Protein structure homology modeling using SWISS-MODEL workspace. Nat. Protoc. 4, 1-13
34. Lopez-Gimenez, J. F., Canals, M., Pediani, J. D., and Milligan, G. (2007) The α1b-adrenoceptor exists as a higher-order oligomer. Effective oligomerization is required for receptor maturation, surface delivery, and function. Mol. Pharmacol. 71, 1015-1029
35. Guo, W., Urizar, E., Kralikova, M., Mobarec, J. C., Shi, L., Filizola, M., and Javitch, J. A. (2008) Dopamine D2 receptors form higher order oligomers at physiological expression levels. EMBO J. 27, 2293-2304
36. Patowary, S., Alvarez-Curto, E., Xu, T. R., Holz, J. D., Oliver, J. A., Milligan, G., and Raicu, V. (2013) The muscarinic M3 acetylcholine receptor exists as two differently sized complexes at the plasma membrane. Biochem. J. 452, 303-312
37. Whorton, M. R., Bokoch, M. P., Rasmussen, S. G., Huang, B., Zare, R. N., Kobilka, B., and Sunahara, R. K. (2007) A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein. Proc. Natl. Acad. Sci. U.S.A. 104, 7682-7687
38. Whorton, M. R., Jastrzebska, B., Park, P. S., Fotiadis, D., Engel, A., Palczewski, K., and Sunahara, R. K. (2008) Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J. Biol. Chem. 283, 4387-4394
39. Park, P. S., Filipek, S., Wells, J. W., and Palczewski, K. (2004) Oligomerization ofGprotein-coupled receptors. Past, present, and future. Biochemistry 43, 15643-15656
40. Birdsall, N. J. (2010) Class A GPCR heterodimers. Evidence from binding studies. Trends Pharmacol. Sci. 31, 499-508
41. Jastrzebska, B., Ringler, P., Lodowski, D. T., Moiseenkova-Bell, V., Golczak, M., Müller, S. A., Palczewski, K., and Engel, A. (2011) Rhodopsintransducin heteropentamer. Three-dimensional structure and biochemical characterization. J. Struct. Biol. 176, 387-394
42. Jastrzebska, B., Orban, T., Golczak, M., Engel, A., and Palczewski, K. (2013) Asymmetry of the rhodopsin dimer in complex with transducin. FASEB J. 27, 1572-1584
43. Lodowski, D. T., Salom, D., Le Trong, I., Teller, D. C., Ballesteros, J. A., Palczewski, K., and Stenkamp, R. E. (2007) Crystal packing analysis of rhodopsin crystals. J. Struct. Biol. 158, 455-462
44. Huang, J., Chen, S., Zhang, J. J., and Huang, X. Y. (2013) Crystal structure of oligomeric β1-adrenergic G protein-coupled receptors in ligand-free basal state. Nat. Struct. Mol. Biol. 20, 419-425
45. Kasai, R. S., Suzuki, K. G., Prossnitz, E. R., Koyama-Honda, I., Nakada, C., Fujiwara, T. K., and Kusumi, A. (2011) Full characterization of GPCR monomer-dimer dynamic equilibrium by single molecule imaging. J. Cell Biol. 192, 463-480
46. Prinster, S. C., Hague, C., and Hall, R. A. (2005) Heterodimerization of g protein-coupled receptors. Specificity and functional significance. Pharmacol. Rev. 57, 289-298
47. Wang, H. X., and Konopka, J. B. (2009) Identification of amino acids at two dimer interface regions of the α-factor receptor (Ste2). Biochemistry 48, 7132-7139
48. McMillin, S. M., Heusel, M., Liu, T., Costanzi, S., and Wess, J. (2011) Structural basis of M3 muscarinic receptor dimer/oligomer formation. J. Biol. Chem. 286, 28584-28598
49. Li, D., D'Angelo, L., Chavez, M., and Woulfe, D. S. (2011) Arrestin-2 differentially regulates PAR4 and ADP receptor signaling in platelets. J. Biol. Chem. 286, 3805-3814