Single platelets seal neutrophil-induced vascular breaches via GPVI during immune-complex-mediated inflammation in mice

Blood

Volumn 126, Issue 8, 2015, Pages 1017-1026

  Gros, Angèle ^a,b   Syvannarath, Varouna ^a,b   Lamrani, Lamia ^a,b   Ollivier, Véronique ^a,b   Loyau, Stéphane ^a,b   Goerge, Tobias ^c,d   Nieswandt, Bernhard ^e   Jandrot Perrus, Martine ^a,b   Ho Tin Noé, Benoît ^a,b  

^a INSERM   (France)

^b Site Xavier Bichat and Département Hospitalo Universitaire Fibrosis Inflammation and Remodeling   (France)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE B; GLYCOPROTEIN VI; LEUKOCYTE ELASTASE; MICROSPHERE; THROMBOCYTE FACTOR 4; AUTACOID; FIBRINOGEN RECEPTOR; PLATELET MEMBRANE GLYCOPROTEIN VI;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN ANTIBODY COMPLEX; ARTHUS PHENOMENON; ARTICLE; BINDING SITE; BLOOD VESSEL INJURY; BLOOD VESSEL WALL; CONTROLLED STUDY; CYTOTOXICITY; DEGRANULATION; DERMATITIS; EXTRAVASCULAR SPACE; MICROSCOPY; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL GRANULE; NONHUMAN; OXIDATIVE STRESS; PERITONEAL CAVITY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKIN BIOPSY; SKIN BLEEDING; THROMBOCYTE; THROMBOCYTE ADHESION; THROMBOCYTE FUNCTION; THROMBOCYTE RELEASE REACTION; THROMBOCYTOPENIA; VENULE; ANIMAL; C57BL MOUSE; COMPLICATION; DISEASE MODEL; IMMUNE COMPLEX DISEASE; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ANIMALS; BLOOD PLATELETS; DISEASE MODELS, ANIMAL; IMMUNE COMPLEX DISEASES; INFLAMMATION; INFLAMMATION MEDIATORS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; PLATELET MEMBRANE GLYCOPROTEINS;

EID: 84940063259     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-12-617159     Document Type: Article

References (37)

1. Petri B, Broermann A, Li H, et al. von Willebrand factor promotes leukocyte extravasation. Blood. 2010;116(22):4712-4719.
2. Cloutier N, Paré A, Farndale RW, et al. Platelets can enhance vascular permeability. Blood. 2012;120(6):1334-1343.
3. Duerschmied D, Suidan GL, Demers M, et al. Platelet serotonin promotes the recruitment of neutrophils to sites of acute inflammation in mice. Blood. 2013;121(6):1008-1015.
4. Massberg S, Konrad I, Schürzinger K, et al. Platelets secrete stromal cell-derived factor 1alpha and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo. J Exp Med. 2006;203(5):1221-1233.
5. Dole VS, Bergmeier W, Mitchell HA, Eichenberger SC, Wagner DD. Activated platelets induce Weibel-Palade-body secretion and leukocyte rolling in vivo: role of P-selectin. Blood. 2005;106(7):2334-2339.
6. Jenne CN, Urrutia R, Kubes P. Platelets: bridging hemostasis, inflammation, and immunity. Int J Lab Hematol. 2013;35(3):254-261.
7. Jenne CN, Wong CH, Zemp FJ, et al. Neutrophils recruited to sites of infection protect from virus challenge by releasing neutrophil extracellular traps. Cell Host Microbe. 2013;13(2):169-180.
8. von Brühl ML, Stark K, Steinhart A, et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med. 2012;209(4):819-835.
9. Martinod K, Wagner DD. Thrombosis: tangled up in NETs. Blood. 2013;123(18):2768-2776.
10. Fujimi S, MacConmara MP, Maung AA, et al. Platelet depletion in mice increases mortality after thermal injury. Blood. 2006;107(11):4399-4406.
11. Goerge T, Ho-Tin-Noe B, Carbo C, et al. Inflammation induces hemorrhage in thrombocytopenia. Blood. 2008;111(10):4958-4964.
12. Hirahashi J, Hishikawa K, Kaname S, et al. Mac-1 (CD11b/CD18) links inflammation and thrombosis after glomerular injury. Circulation. 2009;120(13):1255-1265.
13. Iannacone M, Sitia G, Isogawa M, et al. Platelets prevent IFN-alpha/beta-induced lethal hemorrhage promoting CTL-dependent clearance of lymphocytic choriomeningitis virus. Proc Natl Acad Sci USA. 2008;105(2):629-634.
14. Ho-Tin-Noé B, Demers M, Wagner DD. How platelets safeguard vascular integrity. J Thromb Haemost. 2011;9(suppl 1):56-65.
15. Boulaftali Y, Hess PR, Getz TM, et al. Platelet ITAM signaling is critical for vascular integrity in inflammation. J Clin Invest. 2013;123(2):908-916.
16. Ho-Tin-Noé B, Carbo C, Demers M, Cifuni SM, Goerge T, Wagner DD. Innate immune cells induce hemorrhage in tumors during thrombocytopenia. Am J Pathol. 2009;175(4):1699-1708.
17. Bender M, Hagedorn I, Nieswandt B. Genetic and antibody-induced glycoprotein VI deficiency equally protects mice from mechanically and FeCl(3) -induced thrombosis. J Thromb Haemost. 2011;9(7):1423-1426.
18. Mayadas TN, Tsokos GC, Tsuboi N. Mechanisms of immune complex-mediated neutrophil recruitment and tissue injury. Circulation. 2009;120(20):2012-2024.
19. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13(3):159-175.
20. Jandrot-Perrus M, Busfield S, Lagrue AH, et al. Cloning, characterization, and functional studies of human and mouse glycoprotein VI: a platelet-specific collagen receptor from the immunoglobulin superfamily. Blood. 2000;96(5):1798-1807.
21. McNicol A, Israels SJ. Platelet dense granules: structure, function and implications for haemostasis. Thromb Res. 1999;95(1):1-18.
22. Quek LS, Bolen J, Watson SP. A role for Bruton's tyrosine kinase (Btk) in platelet activation by collagen. Curr Biol. 1998;8(20):1137-1140.
23. Yanaga F, Poole A, Asselin J, et al. Syk interacts with tyrosine-phosphorylated proteins in human platelets activated by collagen and cross-linking of the Fc gamma-IIA receptor. Biochem J. 1995;311(Pt 2):471-478.
24. Poole A, Gibbins JM, Turner M, et al. The Fc receptor gamma-chain and the tyrosine kinase Syk are essential for activation of mouse platelets by collagen. EMBO J. 1997;16(9):2333-2341.
25. Shashidharamurthy R, Hennigar RA, Fuchs S, Palaniswami P, Sherman M, Selvaraj P. Extravasations and emigration of neutrophils to the inflammatory site depend on the interaction of immune-complex with Fcgamma receptors and can be effectively blocked by decoy Fcgamma receptors. Blood. 2008;111(2):894-904.
26. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell. 1994;76(3):519-529.
27. Hara T, Shimizu K, Ogawa F, et al. Platelets control leukocyte recruitment in a murine model of cutaneous arthus reaction. Am J Pathol. 2010;176(1):259-269.
28. Hidalgo A, Chang J, Jang JE, Peired AJ, Chiang EY, Frenette PS. Heterotypic interactions enabled by polarized neutrophil microdomains mediate thromboinflammatory injury. Nat Med. 2009;15(4):384-391.
29. Rossaint J, Herter JM, Van Aken H, et al. Synchronized integrin engagement and chemokine activation is crucial in neutrophil extracellular trap-mediated sterile inflammation. Blood. 2014;123(16):2573-2584.
30. Galt SW, Lindemann S, Medd D, et al. Differential regulation of matrix metalloproteinase-9 by monocytes adherent to collagen and platelets. Circ Res. 2001;89(6):509-516.
31. Boilard E, Nigrovic PA, Larabee K, et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science. 2010;327(5965):580-583.
32. Ho-Tin-Noé B, Goerge T, Cifuni SM, Duerschmied D, Wagner DD. Platelet granule secretion continuously prevents intratumor hemorrhage. Cancer Res. 2008;68(16):6851-6858.
33. Devi S, Kuligowski MP, Kwan RY, et al. Platelet recruitment to the inflamed glomerulus occurs via an alphaIIbbeta3/GPVI-dependent pathway. Am J Pathol. 2010;177(3):1131-1142.
34. Darbousset R, Thomas GM, Mezouar S, et al. Tissue factor-positive neutrophils bind to injured endothelial wall and initiate thrombus formation. Blood. 2012;120(10):2133-2143.
35. Schulz C, von Brühl ML, Barocke V, et al. EMMPRIN (CD147/basigin) mediates platelet-monocyte interactions in vivo and augments monocyte recruitment to the vascular wall. J Thromb Haemost. 2011;9(5):1007-1019.
36. Wang CH, Dai JY, Wang L, et al. Expression of CD147 (EMMPRIN) on neutrophils in rheumatoid arthritis enhances chemotaxis, matrix metalloproteinase production and invasiveness of synoviocytes. J Cell Mol Med. 2011;15(4):850-860.
37. Ollivier V, Syvannarath V, Gros A, et al. Collagen can selectively trigger a platelet secretory phenotype via glycoprotein VI. PLoS ONE. 2014;9(8):e104712.