CLEC-2 is an essential platelet-activating receptor in hemostasis and thrombosis

Blood

Volumn 114, Issue 16, 2009, Pages 3464-3472

  May, Frauke ^a   Hagedorn, Ina ^a   Pleines, Irina ^a   Bender, Markus ^a   Vögtle, Timo ^a   Eble, Johannes ^b   Elvers, Margitta ^a   Nieswandt, Bernhard ^a  

^a UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

C TYPE LECTIN LIKE RECEPTOR 2; MONOCLONAL ANTIBODY; THROMBOCYTE RECEPTOR; UNCLASSIFIED DRUG; ANTIBODY; CLEC 2 PROTEIN, MOUSE; CLEC-2 PROTEIN, MOUSE; LECTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLEEDING TIME; CONTROLLED STUDY; FEMALE; HEMOSTASIS; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; RAT; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOGENESIS; THROMBOSIS; ANIMAL; DRUG ANTAGONISM; EXTRACELLULAR MATRIX; HUMAN; METABOLISM; THROMBOCYTE ADHESIVENESS; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIBODIES; BLOOD PLATELETS; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; HUMANS; LECTINS, C-TYPE; MICE; PLATELET ADHESIVENESS; PLATELET AGGREGATION; THROMBOSIS;

EID: 70350111448     PISSN: 00064971     EISSN: 15280020     Source Type: None    
DOI: 10.1182/blood-2009-05-222273     Document Type: Article

References (48)

1. Weiss HJ. Platelet physiology and abnormalities of platelet function (second of two parts). N Engl J Med. 1975;293(12):580-588.
2. Ruggeri ZM. Platelets in atherothrombosis. Nat Med. 2002;8(11):1227-1234.
3. Conti CR, Mehta JL. Acute myocardial ischemia: role of atherosclerosis, thrombosis, platelet activation, coronary vasospasm, and altered arachidonic acid metabolism. Circulation. 1987;75(6)(pt 2):V84-V95.
4. Bhatt DL, Topol EJ. Scientific and therapeutic advances in antiplatelet therapy. Nat Rev Drug Discov. 2003;2(1):15-28.
5. Savage B, Almus-Jacobs F, Ruggeri ZM. Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow. Cell. 1998;94(5):657-666. (Pubitemid 28427584)
6. Varga-Szabo D, Pleines I, Nieswandt B. Cell adhesion mechanisms in platelets. Arterioscler Thromb Vasc Biol. 2008;28(3):403-412.
7. Jackson SP, Nesbitt WS, Kulkarni S. Signaling events underlying thrombus formation. J Thromb Haemost. 2003;1(7):1602-1612.
8. Offermanns S. Activation of platelet function through G protein-coupled receptors. Circ Res. 2006;99(12):1293-1304. (Pubitemid 44949665)
9. Watson SP, Asazuma N, Atkinson B, et al. The role of ITAM- and ITIM-coupled receptors in platelet activation by collagen. Thromb Haemost. 2001;86(1):276-288. (Pubitemid 32663958)
10. Nieswandt B, Watson SP. Platelet-collagen interaction: is GPVI the central receptor? Blood. 2003;102(2):449-461. (Pubitemid 36841960)
11. Suzuki-Inoue K, Fuller GL, Garcia A, et al. A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2. Blood. 2006;107(2):542-549. (Pubitemid 43076377)
12. Fuller GL, Williams JA, Tomlinson MG, et al. The C-type lectin receptors CLEC-2 and Dectin-1, but not DC-SIGN, signal via a novel YXXL-dependent signaling cascade. J Biol Chem. 2007;282(17):12397-12409.
13. Colonna M, Samaridis J, Angman L. Molecular characterization of two novel C-type lectin-like receptors, one of which is selectively expressed in human dendritic cells. Eur J Immunol. 2000;30(2):697-704. (Pubitemid 30098866)
14. Sobanov Y, Bernreiter A, Derdak S, et al. A novel cluster of lectin-like receptor genes expressed in monocytic, dendritic and endothelial cells maps close to the NK receptor genes in the human NK gene complex. Eur J Immunol. 2001;31(12):3493-3503. (Pubitemid 34030962)
15. Navdaev A, Clemetson JM, Polgar J, et al. Aggretin, a heterodimeric C-type lectin from Calloselasma rhodostoma (malayan pit viper), stimulates platelets by binding to alpha 2beta 1 integrin and glycoprotein Ib, activating Syk and phospholipase Cgamma 2, but does not involve the glycoprotein VI/Fc receptor gamma chain collagen receptor. J Biol Chem. 2001;276(24):20882-20889. (Pubitemid 37413068)
16. Suzuki-Inoue K, Ozaki Y, Kainoh M, et al. Rhodocytin induces platelet aggregation by interacting with glycoprotein Ia/IIa (GPIa/IIa, Integrin alpha 2beta 1): involvement of GPIa/IIa-associated src and protein tyrosine phosphorylation. J Biol Chem. 2001;276(2):1643-1652. (Pubitemid 32096601)
17. Chung CH, Peng HC, Huang TF. Aggretin, a C-type lectin protein, induces platelet aggregation via integrin alpha(2)beta(1) and GPIb in a phosphatidylinositol 3-kinase independent pathway. Biochem Biophys Res Commun. 2001;285(3):689-695.
18. Bergmeier W, Bouvard D, Eble JA, et al. Rhodocytin (aggretin) activates platelets lacking alpha(2)beta(1) integrin, glycoprotein VI, and the ligand-binding domain of glycoprotein Ibalpha. J Biol Chem. 2001;276(27):25121- 25126. (Pubitemid 37412992)
19. O'Callaghan CA. Thrombomodulation via CLEC-2 targeting. Curr Opin Pharmacol. 2009;9(2):90-95.
20. Honn KV, Tang DG, Crissman JD. Platelets and cancer metastasis: a causal relationship? Cancer Metastasis Rev. 1992;11(3-4):325-351.
21. Nieswandt B, Hafner M, Echtenacher B, Mannel DN. Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res. 1999;59(6):1295-1300. (Pubitemid 29136261)
22. Suzuki-Inoue K, Kato Y, Inoue O, et al. Involvement of the snake toxin receptor CLEC-2 in podoplanin-mediated platelet activation by cancer cells. J Biol Chem. 2007;282(36):25993-26001. (Pubitemid 47443800)
23. Chaipan C, Soilleux EJ, Simpson P, et al. DC-SIGN and CLEC-2 mediate human immunodeficiency virus type 1 capture by platelets. J Virol. 2006;80(18):8951-8960. (Pubitemid 44359969)
24. Kerrigan AM, Dennehy KM, Mourao-Sa D, et al. CLEC-2 is a phagocytic activation receptor expressed on murine peripheral blood neutrophils. J Immunol. 2009;182(7):4150-4157.
25. Bergmeier W, Schulte V, Brockhoff G, et al. Flow cytometric detection of activated mouse integrin alphaIIbbeta3 with a novel monoclonal antibody. Cytometry. 2002;48(2):80-86. (Pubitemid 34591919)
26. Grüner S, Prostredna M, Koch M, et al. Relative antithrombotic effect of soluble GPVI dimer compared with anti-GPVI antibodies in mice. Blood. 2005;105(4):1492-1499. (Pubitemid 40223665)
27. Nieswandt B, Brakebusch C, Bergmeier W, et al. Glycoprotein VI but not alpha2beta1 integrin is essential for platelet interaction with collagen. EMBO J. 2001;20(9):2120-2130. (Pubitemid 32410582)
28. Varga-Szabo D, Braun A, Kleinschnitz C, et al. The calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. J Exp Med. 2008;205(7):1583-1591. (Pubitemid 351962022)
29. van der Meijden PE, Munnix IC, Auger JM, et al. Dual role of collagen in factor XII-dependent thrombus formation. Blood. 2009;114(4):881-890.
30. Clemetson JM, Polgar J, Magnenat E, Wells TN, Clemetson KJ. The platelet collagen receptor glycoprotein VI is a member of the immunoglobulin superfamily closely related to FcalphaR and the natural killer receptors. J Biol Chem. 1999;274(41):29019-29024. (Pubitemid 29477060)
31. Nieswandt B, Bergmeier W, Schulte V, et al. Expression and function of the mouse collagen receptor glycoprotein VI is strictly dependent on its association with the FcRgamma chain. J Biol Chem. 2000;275(31):23998-24002. (Pubitemid 30624690)
32. Ruggeri ZM, Mendolicchio GL. Adhesion mechanisms in platelet function. Circ Res. 2007;100(12):1673-1685.
33. Nieswandt B, Schulte V, Bergmeier W, et al. Long-term antithrombotic protection by in vivo depletion of platelet glycoprotein VI in Mice. J Exp Med. 2001;193(4):459-470. (Pubitemid 32524477)
34. Boylan B, Rathore V, Paddock C, et al. JAQ-2/3-like ITP: a newly recognized clinical syndrome caused by autoantibody-mediated clearance of the GPVI/FcR gamma-chain complex from the human platelet surface [abstract]. Blood. 2003;102(11):12A.
35. Xie J, Wu T, Guo L, et al. Molecular characterization of two novel isoforms and a soluble form of mouse CLEC-2. Biochem Biophys Res Commun. 2008;371(2):180-184.
36. Rabie T, Varga-Szabo D, Bender M, et al. Diverging signaling events control the pathway of GPVI down-regulation in vivo. Blood. 2007;110(2):529-535.
37. Schulte V, Rabie T, Prostredna M, et al. Targeting of the collagen-binding site on glycoprotein VI is not essential for in vivo depletion of the receptor. Blood. 2003;101(10):3948-3952. (Pubitemid 36857871)
38. Boylan B, Berndt MC, Kahn ML, Newman PJ. Activation-independent, antibody-mediated removal of GPVI from circulating human platelets: development of a novel NOD/SCID mouse model to evaluate the in vivo effectiveness of anti-human platelet agents. Blood. 2006;108(3):908-914. (Pubitemid 44154624)
39. Ault KA, Knowles C. In vivo biotinylation demonstrates that reticulated platelets are the youngest platelets in circulation. Exp Hematol. 1995;23(9):996-1001.
40. Schulte V, Reusch HP, Pozgajova M, et al. Two-phase antithrombotic protection after anti-glycoprotein VI treatment in mice. Arterioscler Thromb Vasc Biol. 2006;26(7):1640-1647. (Pubitemid 44288995)
41. Grosse J, Braun A, Varga-Szabo D, et al. An EF hand mutation in Stim1 causes premature platelet activation and bleeding in mice. J Clin Invest. 2007;117(11):3540-3550. (Pubitemid 350097009)
42. Judd BA, Myung PS, Obergfell A, et al. Differential requirement for LAT and SLP-76 in GPVI versus T cell receptor signaling. J Exp Med. 2002;195(6):705-717. (Pubitemid 34259716)
43. Mangin P, Nonne C, Eckly A, et al. A PLC gamma 2-independent platelet collagen aggregation requiring functional association of GPVI and integrin alpha2beta1. FEBS Lett. 2003;542(1-3):53-59. (Pubitemid 36555713)
44. Kleinschnitz C, Pozgajova M, Pham M, et al. Targeting platelets in acute experimental stroke: impact of glycoprotein Ib, VI, and IIb/IIIa blockade on infarct size, functional outcome, and intracranial bleeding. Circulation. 2007;115(17):2323-2330. (Pubitemid 46685900)
45. Léon C, Hechler B, Freund M, et al. Defective platelet aggregation and increased resistance to thrombosis in purinergic P2Y(1) receptor-null mice. J Clin Invest. 1999;104(12):1731-1737. (Pubitemid 30053190)
46. Pozgajová M, Sachs UJ, Hein L, Nieswandt B. Reduced thrombus stability in mice lacking the alpha2A-adrenergic receptor. Blood. 2006;108(2):510-514. (Pubitemid 44061349)
47. Rodgers RP, Levin J. A critical reappraisal of the bleeding time. Semin Thromb Hemost. 1990;16(1):1-20.
48. Moroi M, Jung SM, Okuma M, Shinmyozu K. A patient with platelets deficient in glycoprotein VI that lack both collagen-induced aggregation and adhesion. J Clin Invest. 1989;84(5):1440-1445. (Pubitemid 19272230)