Supporting roles of platelet thrombospondin-1 and CD36 in thrombus formation on collagen

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 6, 2014, Pages 1187-1192

  Kuijpers, Marijke J E ^a   De Witt, Susanne ^a   Nergiz Unal, Reyhan ^a   Van Kruchten, Roger ^a   Korporaal, Suzanne J A ^b,c   Verhamme, Peter ^e   Febbraio, Maria ^d   Tjwa, Marc ^b,f   Voshol, Peter J ^b,g   Hoylaerts, Marc F ^e   Cosemans, Judith M E M ^a   Heemskerk, Johan W M ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF ALBERTA   (Canada)

^e UNIVERSITY OF LEUVEN   (Belgium)

^f UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

blood platelets; CD36; mice; thrombosis; thrombospondin 1

Indexed keywords

CD36 ANTIGEN; COLLAGEN; PHOSPHATIDYLSERINE; THROMBOSPONDIN 1;

ANIMAL EXPERIMENT; ARTICLE; ARTIFICIAL EMBOLISM; BLOOD CLOTTING; CONTROLLED STUDY; DISSOLUTION; GENE EXPRESSION; HYPOTHESIS; IN VIVO STUDY; MESENTERY BLOOD VESSEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; WILD TYPE;

BLOOD PLATELETS; CD36; MICE; THROMBOSIS; THROMBOSPONDIN 1;

ANIMALS; ANTIGENS, CD36; COLLAGEN; MICE; MICE, INBRED C57BL; PLATELET ACTIVATION; PLATELET ADHESIVENESS; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; THROMBOSIS; THROMBOSPONDIN 1;

EID: 84901364032     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.302917     Document Type: Article

References (34)

1. Ghosh A, Murugesan G, Chen K, Zhang L, Wang Q, Febbraio M, Anselmo RM, Marchant K, Barnard J, Silverstein RL. Platelet CD36 surface expression levels affect functional responses to oxidized LDL and are associated with inheritance of specific genetic polymorphisms. Blood. 2011;117:6355-6366.
2. Burkhart JM, Vaudel M, Gambaryan S, Radau S, Walter U, Martens L, Geiger J, Sickmann A, Zahedi RP. The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood. 2012;120:e73-e82.
3. Silverstein RL, Febbraio M. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal. 2009;2:re3.
4. Glatz JF, Luiken JJ, Bonen A. Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol Rev. 2010;90:367-417.
5. Nergiz-Unal R, Rademakers T, Cosemans JM, Heemskerk JW. CD36 as a multiple-ligand signaling receptor in atherothrombosis. Cardiovasc Hematol Agents Med Chem. 2011;9:42-55.
6. Tandon NN, Kralisz U, Jamieson GA. Identification of glycoprotein IV (CD36) as a primary receptor for platelet-collagen adhesion. J Biol Chem. 1989;264:7576-7583. (Pubitemid 19119175)
7. Diaz-Ricart M, Tandon NN, Carretero M, Ordinas A, Bastida E, Jamieson GA. Platelets lacking functional CD36 (glycoprotein IV) show reduced adhesion to collagen in flowing whole blood. Blood. 1993;82:491-496. (Pubitemid 23206112)
8. Daniel JL, Dangelmaier C, Strouse R, Smith JB. Collagen induces normal signal transduction in platelets deficient in CD36 (platelet glycoprotein IV). Thromb Haemost. 1994;71:353-356. (Pubitemid 24083747)
9. Kehrel B, Wierwille S, Clemetson KJ, Anders O, Steiner M, Knight CG, Farndale RW, Okuma M, Barnes MJ. Glycoprotein VI is a major collagen receptor for platelet activation: it recognizes the platelet-activating quaternary structure of collagen, whereas CD36, glycoprotein IIb/IIIa, and von Willebrand factor do not. Blood. 1998;91:491-499. (Pubitemid 28053371)
10. Leung LL, Li WX, McGregor JL, Albrecht G, Howard RJ. CD36 peptides enhance or inhibit CD36-thrombospondin binding. A two-step process of ligand-receptor interaction. J Biol Chem. 1992;267:18244-18250.
11. Frieda S, Pearce A, Wu J, Silverstein RL. Recombinant GST/CD36 fusion proteins define a thrombospondin binding domain. Evidence for a single calcium-dependent binding site on CD36. J Biol Chem. 1995;270:2981-2986.
12. Podrez EA, Byzova TV, Febbraio M, Salomon RG, Ma Y, Valiyaveettil M, Poliakov E, Sun M, Finton PJ, Curtis BR, Chen J, Zhang R, Silverstein RL, Hazen SL. Platelet CD36 links hyperlipidemia, oxidant stress and a prothrombotic phenotype. Nat Med. 2007;13:1086-1095. (Pubitemid 47517507)
13. Korporaal SJ, Van Eck M, Adelmeijer J, Ijsseldijk M, Out R, Lisman T, Lenting PJ, Van Berkel TJ, Akkerman JW. Platelet activation by oxidized low density lipoprotein is mediated by CD36 and scavenger receptor-A. Arterioscler Thromb Vasc Biol. 2007;27:2476-2483. (Pubitemid 350203967)
14. Chen K, Febbraio M, Li W, Silverstein RL. A specific CD36-dependent signaling pathway is required for platelet activation by oxidized low-density lipoprotein. Circ Res. 2008;102:1512-1519.
15. Nergiz-Unal R, Lamers MM, Van Kruchten R, Luiken JJ, Cosemans JM, Glatz JF, Kuijpers MJ, Heemskerk JW. Signaling role of CD36 in platelet activation and thrombus formation on immobilized thrombospondin or oxidized low-density lipoprotein. J Thromb Haemost. 2011;9:1835-1846.
16. Bornstein P. Thrombospondins as matricellular modulators of cell function. J Clin Invest. 2001;107:929-934. (Pubitemid 32323400)
17. Bonnefoy A, Hantgan R, Legrand C, Frojmovic MM. A model of platelet aggregation involving multiple interactions of thrombospondin-1, fibrinogen, and GPIIbIIIa receptor. J Biol Chem. 2001;276:5605-5612.
18. Tan K, Lawler J. The interaction of Thrombospondins with extracellular matrix proteins. J Cell Commun Signal. 2009;3:177-187.
19. Stomski FC, Gani JS, Bates RC, Burns GF. Adhesion to thrombospondin by human embryonic fibroblasts is mediated by multiple receptors and includes a role for glycoprotein 88 (CD36). Exp Cell Res. 1992;198:85-92.
20. Jurk K, Clemetson KJ, de Groot PG, Brodde MF, Steiner M, Savion N, Varon D, Sixma JJ, Van Aken H, Kehrel BE. Thrombospondin-1 mediates platelet adhesion at high shear via glycoprotein Ib (GPIb): an alternative/backup mechanism to von Willebrand factor. FASEB J. 2003;17:1490-1492.
21. Isenberg JS, Wink DA, Roberts DD. Thrombospondin-1 antagonizes nitric oxide-stimulated vascular smooth muscle cell responses. Cardiovasc Res. 2006;71:785-793. (Pubitemid 44848003)
22. Isenberg JS, Romeo MJ, Yu C, Yu CK, Nghiem K, Monsale J, Rick ME, Wink DA, Frazier WA, Roberts DD. Thrombospondin-1 stimulates platelet aggregation by blocking the antithrombotic activity of nitric oxide/cGMP signaling. Blood. 2008;111:613-623.
23. Bonnefoy A, Daenens K, Feys HB, De Vos R, Vandervoort P, Vermylen J, Lawler J, Hoylaerts MF. Thrombospondin-1 controls vascular platelet recruitment and thrombus adherence in mice by protecting (sub)endothelial VWF from cleavage by ADAMTS13. Blood. 2006;107:955-964. (Pubitemid 43156292)
24. Rosa JP, George JN, Bainton DF, Nurden AT, Caen JP, McEver RP. Gray platelet syndrome. Demonstration of alpha granule membranes that can fuse with the cell surface. J Clin Invest. 1987;80:1138-1146. (Pubitemid 18075653)
25. Gunay-Aygun M, Falik-Zaccai TC, Vilboux T, et al. NBEAL2 is mutated in gray platelet syndrome and is required for biogenesis of platelet alpha-granules. Nat Genet. 2011;43:732-734.
26. Albers CA, Cvejic A, Favier R, et al. Exome sequencing identifies NBEAL2 as the causative gene for gray platelet syndrome. Nat Genet. 2011;43:735-737.
27. Deppermann C, Cherpokova D, Nurden P, et al. Gray platelet syndrome and defective thrombo-inflammation in Nbeal2-deficient mice. J Clin Invest. 2013;123:3331-3342.
28. Ghosh A, Li W, Febbraio M, Espinola RG, McCrae KR, Cockrell E, Silverstein RL. Platelet CD36 mediates interactions with endothelial cell-derived microparticles and contributes to thrombosis in mice. J Clin Invest. 2008;118:1934-1943. (Pubitemid 351632395)
29. Brodde MF, Korporaal SJ, Herminghaus G, Fobker M, Van Berkel TJ, Tietge UJ, Robenek H, Van Eck M, Kehrel BE, Nofer JR. Native high-density lipoproteins inhibit platelet activation via scavenger receptor BI: role of negatively charged phospholipids. Atherosclerosis. 2011;215:374-382.
30. Cosemans JM, Munnix IC, Wetzker R, Heller R, Jackson SP, Heemskerk JW. Continuous signaling via PI3K isoforms beta and gamma is required for platelet ADP receptor function in dynamic thrombus stabilization. Blood. 2006;108:3045-3052.
31. Cosemans JM, Van Kruchten R, Olieslagers S, Schurgers LJ, Verheyen FK, Munnix IC, Waltenberger J, Angelillo-Scherrer A, Hoylaerts MF, Carmeliet P, Heemskerk JW. Potentiating role of Gas6 and Tyro3, Axl and Mer (TAM) receptors in human and murine platelet activation and thrombus stabilization. J Thromb Haemost. 2010;8:1797-1808.
32. Chu LY, Ramakrishnan DP, Silverstein RL. Thrombospondin-1 modulates VEGF signaling via CD36 by recruiting SHP-1 to VEGFR2 complex in microvascular endothelial cells. Blood. 2013;122:1822-1832.
33. Febbraio M, Podrez EA, Smith JD, Hajjar DP, Hazen SL, Hoff HF, Sharma K, Silverstein RL. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J Clin Invest. 2000;105:1049-1056. (Pubitemid 30217689)
34. Kauskot A, Di Michele M, Loyen S, Freson K, Verhamme P, Hoylaerts MF. A novel mechanism of sustained platelet alphaIIbbeta3 activation via PEAR1. Blood. 2012;119:4056-4065.