Tissue Factor Expressed by Neutrophils: Another Piece in the Vascular Inflammation Puzzle

Norma Maugeri; Angelo A. Manfredi

doi:10.1055/s-0035-1564043

Seminars in Thrombosis and Hemostasis, Inhaltsverzeichnis

Semin Thromb Hemost 2015; 41(07): 728-736
DOI: 10.1055/s-0035-1564043

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Tissue Factor Expressed by Neutrophils: Another Piece in the Vascular Inflammation Puzzle

Norma Maugeri

¹Autoimmunity and Vascular Inflammation Unit, Division of Immunology, Transplantation and Infectious Diseases, San Raffaele Scientific Institute, Milan, Italy

,

Angelo A. Manfredi

¹Autoimmunity and Vascular Inflammation Unit, Division of Immunology, Transplantation and Infectious Diseases, San Raffaele Scientific Institute, Milan, Italy

²Vita-Salute San Raffaele University, Milan, Italy

› Institutsangaben

Abstract

The transition from the classic role of neutrophils as the first line of defense of the immune system to that of physiological regulators of intravascular thrombosis took nearly three decades to emerge. This transition needed time to unravel the complex links between the mechanisms that regulate hemostasis and inflammation and the innate immune response, multicellular and multifactorial processes that interact with each other. The present review is focused on the expression of tissue factor by neutrophils, a critical event in their inflammatory and thrombotic function.

Keywords

neutrophils - tissue factor - autoimmune diseases - immunothrombosis - thromboinflammation

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Referenzen

References
1 Zhao P, Metcalf M, Bunnett NW. Biased signaling of protease-activated receptors. Front Endocrinol (Lausanne) 2014; 5: 67
2 Pawlinski R, Mackman N. Tissue factor, coagulation proteases, and protease-activated receptors in endotoxemia and sepsis. Crit Care Med 2004; 32 (5, Suppl): S293-S297
3 Mitroulis I, Kambas K, Anyfanti P, Doumas M, Ritis K. The multivalent activity of the tissue factor-thrombin pathway in thrombotic and non-thrombotic disorders as a target for therapeutic intervention. Expert Opin Ther Targets 2011; 15 (1) 75-89
4 Maugeri N, Rovere-Querini P, Evangelista V , et al. An intense and short-lasting burst of neutrophil activation differentiates early acute myocardial infarction from systemic inflammatory syndromes. PLoS ONE 2012; 7 (6) e39484
5 Borregaard N, Sørensen OE, Theilgaard-Mönch K. Neutrophil granules: a library of innate immunity proteins. Trends Immunol 2007; 28 (8) 340-345
6 Pham CT. Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol 2006; 6 (7) 541-550
7 Mócsai A. Diverse novel functions of neutrophils in immunity, inflammation, and beyond. J Exp Med 2013; 210 (7) 1283-1299
8 Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 2011; 11 (8) 519-531
9 Maugeri N, Campana L, Gavina M , et al. Activated platelets present high mobility group box 1 to neutrophils, inducing autophagy and promoting the extrusion of neutrophil extracellular traps. J Thromb Haemost 2014; 12 (12) 2074-2088
10 Leshner M, Wang S, Lewis C , et al. PAD4 mediated histone hypercitrullination induces heterochromatin decondensation and chromatin unfolding to form neutrophil extracellular trap-like structures. Front Immunol 2012; 3: 307
11 Manfredi AA, Covino C, Rovere-Querini P, Maugeri N. Instructive influences of phagocytic clearance of dying cells on neutrophil extracellular trap generation. Clin Exp Immunol 2015; 179 (1) 24-29
12 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
13 Yipp BG, Kubes P. NETosis: how vital is it?. Blood 2013; 122 (16) 2784-2794
14 Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol 2010; 191 (3) 677-691
15 Radic M, Marion TN. Neutrophil extracellular chromatin traps connect innate immune response to autoimmunity. Semin Immunopathol 2013; 35 (4) 465-480
16 Kaplan MJ, Radic M. Neutrophil extracellular traps: double-edged swords of innate immunity. J Immunol 2012; 189 (6) 2689-2695
17 Dale DC, Boxer L, Liles WC. The phagocytes: neutrophils and monocytes. Blood 2008; 112 (4) 935-945
18 Zemans RL, Colgan SP, Downey GP. Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury. Am J Respir Cell Mol Biol 2009; 40 (5) 519-535
19 Zarbock A, Ley K. Mechanisms and consequences of neutrophil interaction with the endothelium. Am J Pathol 2008; 172 (1) 1-7
20 Sreeramkumar V, Leiva M, Stadtmann A , et al. Coordinated and unique functions of the E-selectin ligand ESL-1 during inflammatory and hematopoietic recruitment in mice. Blood 2013; 122 (24) 3993-4001
21 Totani L, Evangelista V. Platelet-leukocyte interactions in cardiovascular disease and beyond. Arterioscler Thromb Vasc Biol 2010; 30 (12) 2357-2361
22 Manfredi AA, Rovere-Querini P, Maugeri N. Dangerous connections: neutrophils and the phagocytic clearance of activated platelets. Curr Opin Hematol 2010; 17 (1) 3-8
23 Maugeri N, Rovere-Querini P, Baldini M, Sabbadini MG, Manfredi AA. Translational mini-review series on immunology of vascular disease: mechanisms of vascular inflammation and remodelling in systemic vasculitis. Clin Exp Immunol 2009; 156 (3) 395-404
24 Ramirez GA, Maugeri N, Sabbadini MG, Rovere-Querini P, Manfredi AA. Intravascular immunity as a key to systemic vasculitis: a work in progress, gaining momentum. Clin Exp Immunol 2014; 175 (2) 150-166
25 Cera MR, Fabbri M, Molendini C , et al. JAM-A promotes neutrophil chemotaxis by controlling integrin internalization and recycling. J Cell Sci 2009; 122 (Pt 2) 268-277
26 Sreeramkumar V, Adrover JM, Ballesteros I , et al. Neutrophils scan for activated platelets to initiate inflammation. Science 2014; 346 (6214) 1234-1238
27 Maugeri N, Baldini M, Ramirez GA, Rovere-Querini P, Manfredi AA. Platelet-leukocyte deregulated interactions foster sterile inflammation and tissue damage in immune-mediated vessel diseases. Thromb Res 2012; 129 (3) 267-273
28 Nacher M, Hidalgo A. Fire within the vessels: interactions between blood cells and inflammatory vascular injury. Front Biosci (Schol Ed) 2011; 3: 1089-1100
29 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
30 Kambas K, Mitroulis I, Ritis K. The emerging role of neutrophils in thrombosis-the journey of TF through NETs. Front Immunol 2012; 3: 385
31 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
32 Todoroki H, Nakamura S, Higure A , et al. Neutrophils express tissue factor in a monkey model of sepsis. Surgery 2000; 127 (2) 209-216
33 Higure A, Okamoto K, Hirata K , et al. Macrophages and neutrophils infiltrating into the liver are responsible for tissue factor expression in a rabbit model of acute obstructive cholangitis. Thromb Haemost 1996; 75 (5) 791-795
34 Maugeri N, Brambilla M, Camera M , et al. Human polymorphonuclear leukocytes produce and express functional tissue factor upon stimulation. J Thromb Haemost 2006; 4 (6) 1323-1330
35 Ritis K, Doumas M, Mastellos D , et al. A novel C5a receptor-tissue factor cross-talk in neutrophils links innate immunity to coagulation pathways. J Immunol 2006; 177 (7) 4794-4802
36 Baldini M, Manfredi AA, Maugeri N. Targeting platelet-neutrophil interactions in giant-cell arteritis. Curr Pharm Des 2014; 20 (4) 567-574
37 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
38 Rafail S, Ritis K, Schaefer K , et al. Leptin induces the expression of functional tissue factor in human neutrophils and peripheral blood mononuclear cells through JAK2-dependent mechanisms and TNFalpha involvement. Thromb Res 2008; 122 (3) 366-375
39 Maugeri N, Giordano G, Petrilli MP , et al. Inhibition of tissue factor expression by hydroxyurea in polymorphonuclear leukocytes from patients with myeloproliferative disorders: a new effect for an old drug?. J Thromb Haemost 2006; 4 (12) 2593-2598
40 Maugeri N, Malato S, Femia EA , et al. Clearance of circulating activated platelets in polycythemia vera and essential thrombocythemia. Blood 2011; 118 (12) 3359-3366
41 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
42 Palabrica T, Lobb R, Furie BC , et al. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature 1992; 359 (6398) 848-851
43 Furie B, Furie BC. Mechanisms of thrombus formation. N Engl J Med 2008; 359 (9) 938-949
44 Maugeri N, Baldini M, Rovere-Querini P, Maseri A, Sabbadini MG, Manfredi AA. Leukocyte and platelet activation in patients with giant cell arteritis and polymyalgia rheumatica: a clue to thromboembolic risks?. Autoimmunity 2009; 42 (4) 386-388
45 Maugeri N, Rovere-Querini P, Baldini M , et al. Oxidative stress elicits platelet/leukocyte inflammatory interactions via HMGB1: a candidate for microvessel injury in sytemic sclerosis. Antioxid Redox Signal 2014; 20 (7) 1060-1074
46 Maugeri N, Rovere-Querini P, Slavich M , et al. Early and transient release of leukocyte pentraxin 3 during acute myocardial infarction. J Immunol 2011; 187 (2) 970-979
47 Furman MI, Kereiakes DJ, Krueger LA , et al. Leukocyte-platelet aggregation, platelet surface P-selectin, and platelet surface glycoprotein IIIa after percutaneous coronary intervention: Effects of dalteparin or unfractionated heparin in combination with abciximab. Am Heart J 2001; 142 (5) 790-798
48 Gardiner EE, De Luca M, McNally T, Michelson AD, Andrews RK, Berndt MC. Regulation of P-selectin binding to the neutrophil P-selectin counter-receptor P-selectin glycoprotein ligand-1 by neutrophil elastase and cathepsin G. Blood 2001; 98 (5) 1440-1447
49 Michelson AD, Barnard MR, Krueger LA, Valeri CR, Furman MI. Circulating monocyte-platelet aggregates are a more sensitive marker of in vivo platelet activation than platelet surface P-selectin: studies in baboons, human coronary intervention, and human acute myocardial infarction. Circulation 2001; 104 (13) 1533-1537
50 Kambas K, Markiewski MM, Pneumatikos IA , et al. C5a and TNF-alpha up-regulate the expression of tissue factor in intra-alveolar neutrophils of patients with the acute respiratory distress syndrome. J Immunol 2008; 180 (11) 7368-7375
51 Maugeri N, Franchini S, Campana L , et al. Circulating platelets as a source of the damage-associated molecular pattern HMGB1 in patients with systemic sclerosis. Autoimmunity 2012; 45 (8) 584-587
52 Brambilla M, Camera M, Colnago D , et al. Tissue factor in patients with acute coronary syndromes: expression in platelets, leukocytes, and platelet-leukocyte aggregates. Arterioscler Thromb Vasc Biol 2008; 28 (5) 947-953
53 Camera M, Brambilla M, Facchinetti L , et al. Tissue factor and atherosclerosis: not only vessel wall-derived TF, but also platelet-associated TF. Thromb Res 2012; 129 (3) 279-284
54 Evangelista V, Pamuklar Z, Piccoli A , et al. Src family kinases mediate neutrophil adhesion to adherent platelets. Blood 2007; 109 (6) 2461-2469
55 Piccardoni P, Manarini S, Federico L , et al. SRC-dependent outside-in signalling is a key step in the process of autoregulation of beta2 integrins in polymorphonuclear cells. Biochem J 2004; 380 (Pt 1): 57-65
56 Piccardoni P, Sideri R, Manarini S , et al. Platelet/polymorphonuclear leukocyte adhesion: a new role for SRC kinases in Mac-1 adhesive function triggered by P-selectin. Blood 2001; 98 (1) 108-116
57 Maugeri N, de Gaetano G, Barbanti M, Donati MB, Cerletti C. Prevention of platelet-polymorphonuclear leukocyte interactions: new clues to the antithrombotic properties of parnaparin, a low molecular weight heparin. Haematologica 2005; 90 (6) 833-839
58 Maugeri N, Rovere-Querini P, Evangelista V , et al. Neutrophils phagocytose activated platelets in vivo: a phosphatidylserine, P-selectin, and beta2 integrin-dependent cell clearance program. Blood 2009; 113 (21) 5254-5265
59 Maugeri N, Di Fabio G, Barbanti M, de Gaetano G, Donati MB, Cerletti C. Parnaparin, a low-molecular-weight heparin, prevents P-selectin-dependent formation of platelet-leukocyte aggregates in human whole blood. Thromb Haemost 2007; 97 (6) 965-973
60 Stakos DA, Kambas K, Konstantinidis T , et al. Expression of functional tissue factor by neutrophil extracellular traps in culprit artery of acute myocardial infarction. Eur Heart J 2015; 36 (22) 1405-1414
61 Kambas K, Mitroulis I, Apostolidou E , et al. Autophagy mediates the delivery of thrombogenic tissue factor to neutrophil extracellular traps in human sepsis. PLoS ONE 2012; 7 (9) e45427
62 Kambas K, Chrysanthopoulou A, Vassilopoulos D , et al. Tissue factor expression in neutrophil extracellular traps and neutrophil derived microparticles in antineutrophil cytoplasmic antibody associated vasculitis may promote thromboinflammation and the thrombophilic state associated with the disease. Ann Rheum Dis 2014; 73 (10) 1854-1863
63 Brinkmann V, Reichard U, Goosmann C , et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303 (5663) 1532-1535
64 Urban CF, Reichard U, Brinkmann V, Zychlinsky A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol 2006; 8 (4) 668-676
65 Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol 2013; 13 (1) 34-45
66 Thomas GM, Carbo C, Curtis BR , et al. Extracellular DNA traps are associated with the pathogenesis of TRALI in humans and mice. Blood 2012; 119 (26) 6335-6343
67 Fuchs TA, Brill A, Duerschmied D , et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci U S A 2010; 107 (36) 15880-15885
68 Brill A, Fuchs TA, Savchenko AS , et al. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost 2012; 10 (1) 136-144
69 Pemberton AD, Brown JK, Inglis NF. Proteomic identification of interactions between histones and plasma proteins: implications for cytoprotection. Proteomics 2010; 10 (7) 1484-1493
70 Ward CM, Tetaz TJ, Andrews RK, Berndt MC. Binding of the von Willebrand factor A1 domain to histone. Thromb Res 1997; 86 (6) 469-477
71 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
72 Ammollo CT, Semeraro F, Xu J, Esmon NL, Esmon CT. Extracellular histones increase plasma thrombin generation by impairing thrombomodulin-dependent protein C activation. J Thromb Haemost 2011; 9 (9) 1795-1803
73 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
74 Esmon CT. Molecular circuits in thrombosis and inflammation. Thromb Haemost 2013; 109 (3) 416-420
75 Remijsen Q, Vanden Berghe T, Wirawan E , et al. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Res 2011; 21 (2) 290-304
76 de Boer OJ, Li X, Teeling P , et al. Neutrophils, neutrophil extracellular traps and interleukin-17 associate with the organisation of thrombi in acute myocardial infarction. Thromb Haemost 2013; 109 (2) 290-297
77 Giesen PL, Rauch U, Bohrmann B , et al. Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci U S A 1999; 96 (5) 2311-2315
78 Wang JG, Manly D, Kirchhofer D, Pawlinski R, Mackman N. Levels of microparticle tissue factor activity correlate with coagulation activation in endotoxemic mice. J Thromb Haemost 2009; 7 (7) 1092-1098
79 Furie B, Furie BC. Role of platelet P-selectin and microparticle PSGL-1 in thrombus formation. Trends Mol Med 2004; 10 (4) 171-178
80 Eleftheriou D, Hong Y, Klein NJ, Brogan PA. Thromboembolic disease in systemic vasculitis is associated with enhanced microparticle-mediated thrombin generation. J Thromb Haemost 2011; 9 (9) 1864-1867
81 Hergesell O, Andrassy K, Nawroth P. Elevated levels of markers of endothelial cell damage and markers of activated coagulation in patients with systemic necrotizing vasculitis. Thromb Haemost 1996; 75 (6) 892-898
82 Daniel L, Fakhouri F, Joly D , et al. Increase of circulating neutrophil and platelet microparticles during acute vasculitis and hemodialysis. Kidney Int 2006; 69 (8) 1416-1423
83 Delabranche X, Boisramé-Helms J, Asfar P , et al. Microparticles are new biomarkers of septic shock-induced disseminated intravascular coagulopathy. Intensive Care Med 2013; 39 (10) 1695-1703
84 Nieuwland R, Berckmans RJ, McGregor S , et al. Cellular origin and procoagulant properties of microparticles in meningococcal sepsis. Blood 2000; 95 (3) 930-935
85 Guervilly C, Lacroix R, Forel JM , et al. High levels of circulating leukocyte microparticles are associated with better outcome in acute respiratory distress syndrome. Crit Care 2011; 15 (1) R31
86 Gasser O, Schifferli JA. Microparticles released by human neutrophils adhere to erythrocytes in the presence of complement. Exp Cell Res 2005; 307 (2) 381-387
87 Girardi G, Redecha P, Salmon JE. Heparin prevents antiphospholipid antibody-induced fetal loss by inhibiting complement activation. Nat Med 2004; 10 (11) 1222-1226
88 McKeage K, Keating GM. Parnaparin : a review of its use in the management of venous thromboembolism, chronic venous disease and other vascular disorders. Drugs 2008; 68 (1) 105-122
89 Redecha P, Franzke CW, Ruf W, Mackman N, Girardi G. Neutrophil activation by the tissue factor/Factor VIIa/PAR2 axis mediates fetal death in a mouse model of antiphospholipid syndrome. J Clin Invest 2008; 118 (10) 3453-3461
90 Yarbro JW. Mechanism of action of hydroxyurea. Semin Oncol 1992; 19 (3) (Suppl. 09) 1-10
91 Habets KL, Huizinga TW, Toes RE. Platelets and autoimmunity. Eur J Clin Invest 2013; 43 (7) 746-757
92 Collins CE, Cahill MR, Newland AC, Rampton DS. Platelets circulate in an activated state in inflammatory bowel disease. Gastroenterology 1994; 106 (4) 840-845
93 Ertenli I, Kiraz S, Arici M , et al. P-selectin as a circulating molecular marker in rheumatoid arthritis with thrombocytosis. J Rheumatol 1998; 25 (6) 1054-1058
94 Gasparyan AY, Stavropoulos-Kalinoglou A, Mikhailidis DP, Douglas KM, Kitas GD. Platelet function in rheumatoid arthritis: arthritic and cardiovascular implications. Rheumatol Int 2011; 31 (2) 153-164
95 Apostolidou E, Skendros P, Kambas K , et al. Neutrophil extracellular traps regulate IL-1β-mediated inflammation in familial Mediterranean fever. Ann Rheum Dis 2014; ; doi: 10.1136/annrheumdis-2014-205958
96 Takeda I, Kaise S, Nishimaki T, Kasukawa R. Soluble P-selectin in the plasma of patients with connective tissue diseases. Int Arch Allergy Immunol 1994; 105 (2) 128-134
97 Tang S, Zhang Y, Yin SW , et al. Neutrophil extracellular trap formation is associated with autophagy-related signalling in ANCA-associated vasculitis. Clin Exp Immunol 2015; 180 (3) 408-418
98 Saffarzadeh M, Preissner KT. Fighting against the dark side of neutrophil extracellular traps in disease: manoeuvres for host protection. Curr Opin Hematol 2013; 20 (1) 3-9
99 Horita T. Recent advances in pathogenesis and pathophysiology in the antiphospholipid syndrome [in Japanese]. Nihon Rinsho Meneki Gakkai Kaishi 2012; 35 (6) 481-494
100 Rossaint J, Zarbock A. Platelets in leucocyte recruitment and function. Cardiovasc Res 2015; 107: 386-395
101 Lv B, Wang H, Tang Y, Fan Z, Xiao X, Chen F. High-mobility group box 1 protein induces tissue factor expression in vascular endothelial cells via activation of NF-kappaB and Egr-1. Thromb Haemost 2009; 102 (2) 352-359
102 Ramirez GA, Franchini S, Rovere-Querini P, Sabbadini MG, Manfredi AA, Maugeri N. The role of platelets in the pathogenesis of systemic sclerosis. Front Immunol 2012; 3: 160
103 Redecha P, Tilley R, Tencati M , et al. Tissue factor: a link between C5a and neutrophil activation in antiphospholipid antibody induced fetal injury. Blood 2007; 110 (7) 2423-2431