Cellular fibronectin containing extra domain A promotes arterial thrombosis in mice through platelet Toll-like receptor 4

Blood

Volumn 125, Issue 20, 2015, Pages 3164-3172

  Prakash, Prem ^a   Kulkarni, Paresh P ^a   Lentz, Steven R ^a   Chauhan, Anil K ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Fn EDA1 promotes arterial thrombosis; Platelet tlr4 mediates the prothrombotic effect of cellular fn

Indexed keywords

COLLAGEN; FIBRONECTIN; FIBRONECTIN CONTAINING EXTRA DOMAIN A; GENOMIC DNA; THROMBIN; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; EXTRA DOMAIN A FIBRONECTIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING TIME; BLOOD CLOTTING; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CAROTID ARTERY THROMBOSIS; CELL INTERACTION; CONTROLLED STUDY; DISEASE PREDISPOSITION; FEMALE; FERRIC CHLORIDE-INDUCED THROMBOSIS; GENE DELETION; HEMATOPOIETIC CELL; IN VITRO STUDY; INNATE IMMUNITY; INTRAVITAL MICROSCOPY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE COUNT; ANIMAL; COMMON CAROTID ARTERY; DISEASE MODEL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; THROMBOCYTE; THROMBOSIS;

ANIMALS; BLOOD PLATELETS; CAROTID ARTERY, COMMON; DISEASE MODELS, ANIMAL; FEMALE; FIBRONECTINS; IMMUNITY, INNATE; MALE; MICE; MICE, KNOCKOUT; PLATELET AGGREGATION; THROMBOSIS; TOLL-LIKE RECEPTOR 4;

EID: 84964693394     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-10-608653     Document Type: Article

References (53)

1. White ES, Baralle FE, Muro AF. New insights into form and function of fibronectin splice variants. J Pathol. 2008;216(1):1-14.
2. Maurer LM, Tomasini-Johansson BR, Mosher DF. Emerging roles of fibronectin in thrombosis. Thromb Res. 2010;125(4):287-291.
3. Ni H, Yuen PS, Papalia JM, et al. Plasma fibronectin promotes thrombus growth and stability in injured arterioles. Proc Natl Acad Sci USA. 2003;100(5):2415-2419.
4. Cho J, Mosher DF. Role of fibronectin assembly in platelet thrombus formation. J Thromb Haemost. 2006;4(7):1461-1469.
5. Cho J, Mosher DF. Impact of fibronectin assembly on platelet thrombus formation in response to type I collagen and von Willebrand factor. Blood. 2006; 108(7):2229-2236.
6. Cho J, Mosher DF. Characterization of fibronectin assembly by platelets adherent to adsorbed laminin-111. J Thromb Haemost. 2006;4(5): 943-951.
7. Cho J, Mosher DF. Enhancement of thrombogenesis by plasma fibronectin crosslinked to fibrin and assembled in platelet thrombi. Blood. 2006;107(9):3555-3563.
8. Yang H, Reheman A, Chen P, et al. Fibrinogen and von Willebrand factor-independent platelet aggregation in vitro and in vivo. J Thromb Haemost. 2006;4(10):2230-2237.
9. Wang Y, Reheman A, Spring CM, et al. Plasma fibronectin supports hemostasis and regulates thrombosis. J Clin Invest. 2014;124(10): 4281-4293.
10. Reheman A, Yang H, Zhu G, et al. Plasma fibronectin depletion enhances platelet aggregation and thrombus formation in mice lacking fibrinogen and von Willebrand factor. Blood. 2009;113(8):1809-1817.
11. Tomasini-Johansson B, Mosher DF. Plasma fibronectin concentration in inbred mouse strains. Thromb Haemost. 2009;102(6):1278-1280.
12. Matuskova J, Chauhan AK, Cambien B, et al. Decreased plasma fibronectin leads to delayed thrombus growth in injured arterioles. Arterioscler Thromb Vasc Biol. 2006;26(6):1391-1396.
13. Kanters SD, Banga JD, Algra A, Frijns RC, Beutler JJ, Fijnheer R. Plasma levels of cellular fibronectin in diabetes. Diabetes Care. 2001; 24(2):323-327.
14. Castellanos M, Leira R, Serena J, et al. Plasma cellular-fibronectin concentration predicts hemorrhagic transformation after thrombolytic therapy in acute ischemic stroke. Stroke. 2004; 35(7):1671-1676.
15. Chauhan AK, Kisucka J, Cozzi MR, et al. Prothrombotic effects of fibronectin isoforms containing the EDA domain. Arterioscler Thromb Vasc Biol. 2008;28(2):296-301.
16. Okamura Y, Watari M, Jerud ES, et al. The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem. 2001;276(13):10229-10233.
17. Lasarte JJ, Casares N, Gorraiz M, et al. The extra domain A from fibronectin targets antigens to TLR4-expressing cells and induces cytotoxic T cell responses in vivo. J Immunol. 2007;178(2): 748-756.
18. Lefebvre JS, Lévesque T, Picard S, et al. Extra domain A of fibronectin primes leukotriene biosynthesis and stimulates neutrophil migration through activation of Toll-like receptor 4. Arthritis Rheum. 2011;63(6):1527-1533.
19. Saito S, Yamaji N, Yasunaga K, et al. The fibronectin extra domain A activates matrix metalloproteinase gene expression by an interleukin-1-dependent mechanism. J Biol Chem. 1999;274(43):30756-30763.
20. Khan MM, Gandhi C, Chauhan N, et al. Alternatively-spliced extra domain A of fibronectin promotes acute inflammation and brain injury after cerebral ischemia in mice. Stroke. 2012;43(5): 1376-1382.
21. Semeraro F, Ammollo CT, Morrissey JH, et al. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood. 2011;118(7):1952-1961.
22. Rumbaut RE, Bellera RV, Randhawa JK, et al. Endotoxin enhances microvascular thrombosis in mouse cremaster venules via a TLR4-dependent, neutrophil-independent mechanism. Am J Physiol Heart Circ Physiol. 2006;290(4):H1671-H1679.
23. Stark RJ, Aghakasiri N, Rumbaut RE. Plateletderived Toll-like receptor 4 (Tlr-4) is sufficient to promote microvascular thrombosis in endotoxemia. PLoS ONE. 2012;7(7):e41254.
24. Xie H, Sheng L, Zhou H, Yan J. The role of TLR4 in pathophysiology of antiphospholipid syndromeassociated thrombosis and pregnancy morbidity. Br J Haematol. 2014;164(2):165-176.
25. Muro AF, Chauhan AK, Gajovic S, et al. Regulated splicing of the fibronectin EDA exon is essential for proper skin wound healing and normal lifespan. J Cell Biol. 2003;162(1):149-160.
26. Chauhan AK, Motto DG, Lamb CB, et al. Systemic antithrombotic effects of ADAMTS13. J Exp Med. 2006;203(3):767-776.
27. Prakash P, Kulkarni PP, Chauhan AK. Thrombospondin 1 requires von Willebrand factor to modulate arterial thrombosis in mice. Blood. 2015;125(2):399-406.
28. Boulaftali Y, Hess PR, Kahn ML, Bergmeier W. Platelet immunoreceptor tyrosine-based activation motif (ITAM) signaling and vascular integrity. Circ Res. 2014;114(7):1174-1184.
29. Gandhi C, Khan MM, Lentz SR, Chauhan AK. ADAMTS13 reduces vascular inflammation and the development of early atherosclerosis in mice. Blood. 2012;119(10):2385-2391.
30. Clark SR, Ma AC, Tavener SA, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007; 13(4):463-469.
31. Wilson CL, Schwarzbauer JE. The alternatively spliced V region contributes to the differential incorporation of plasma and cellular fibronectins into fibrin clots. J Cell Biol. 1992;119(4):923-933.
32. Andonegui G, Kerfoot SM, McNagny K, Ebbert KV, Patel KD, Kubes P. Platelets express functional Toll-like receptor-4. Blood. 2005; 106(7):2417-2423.
33. Berthet J, Damien P, Hamzeh-Cognasse H, Pozzetto B, Garraud O, Cognasse F. Toll-like receptor 4 signal transduction in platelets: novel pathways. Br J Haematol. 2010;151(1):89-92.
34. Zhang G, Han J, Welch EJ, et al. Lipopolysaccharide stimulates platelet secretion and potentiates platelet aggregation via TLR4/ MyD88 and the cGMP-dependent protein kinase pathway. J Immunol. 2009;182(12):7997-8004.
35. Rivadeneyra L, Carestia A, Etulain J, et al. Regulation of platelet responses triggered by Toll-like receptor 2 and 4 ligands is another non-genomic role of nuclear factor-kappaB. Thromb Res. 2014;133(2):235-243.
36. Bergmeier W, Boulaftali Y. Adoptive transfer method to study platelet function in mouse models of disease. Thromb Res. 2014;133(suppl 1): S3-S5.
37. Kanaji T, Russell S, Ware J. Amelioration of the macrothrombocytopenia associated with the murine Bernard-Soulier syndrome. Blood. 2002; 100(6):2102-2107.
38. Rondina MT, Weyrich AS, Zimmerman GA. Platelets as cellular effectors of inflammation in vascular diseases. Circ Res. 2013;112(11): 1506-1519.
39. Li C, Li J, Li Y, et al. Crosstalk between platelets and the immune system: old systems with new discoveries. Adv Hematol. 2012;2012:384685.
40. Patrignani P, Di Febbo C, Tacconelli S, et al. Reduced thromboxane biosynthesis in carriers of toll-like receptor 4 polymorphisms in vivo. Blood. 2006;107(9):3572-3574.
41. Ameziane N, Beillat T, Verpillat P, et al. Association of the Toll-like receptor 4 gene Asp299Gly polymorphism with acute coronary events. Arterioscler Thromb Vasc Biol. 2003; 23(12):e61-e64.
42. Brown GT, Narayanan P, Li W, Silverstein RL, McIntyre TM. Lipopolysaccharide stimulates platelets through an IL-1β autocrine loop. J Immunol. 2013;191(10):5196-5203.
43. Brown GT, McIntyre TM. Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL-1β-rich microparticles. J Immunol. 2011;186(9): 5489-5496.
44. Guan JL, Trevithick JE, Hynes RO. Retroviral expression of alternatively spliced forms of rat fibronectin. J Cell Biol. 1990;110(3):833-847.
45. Aslam R, Speck ER, Kim M, et al. Platelet Toll-like receptor expression modulates lipopolysaccharide-induced thrombocytopenia and tumor necrosis factor-alpha production in vivo. Blood. 2006;107(2):637-641.
46. Malaver E, Romaniuk MA, D'Atri LP, et al. NF-kappaB inhibitors impair platelet activation responses. J Thromb Haemost. 2009;7(8): 1333-1343.
47. Spinelli SL, Casey AE, Pollock SJ, et al. Platelets and megakaryocytes contain functional nuclear factor-kappaB. Arterioscler Thromb Vasc Biol. 2010;30(3):591-598.
48. Karim ZA, Zhang J, Banerjee M, et al. IkB kinase phosphorylation of SNAP-23 controls platelet secretion. Blood. 2013;121(22):4567-4574.
49. Wei S, Wang H, Zhang G, et al. Platelet IkB kinase-b deficiency increases mouse arterial neointima formation via delayed glycoprotein Iba shedding. Arterioscler Thromb Vasc Biol. 2013; 33(2):241-248.
50. Rondina MT, Schwertz H, Harris ES, et al. The septic milieu triggers expression of spliced tissue factor mRNA in human platelets. J Thromb Haemost. 2011;9(4):748-758.
51. 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.
52. 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.
53. Massberg S, Grahl L, von Bruehl ML, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med. 2010;16(8):887-896.