Promotion of Hypercoagulability in Antineutrophil Cytoplasmic Antibody–Associated Vasculitis by C5a-Induced Tissue Factor–Expressing Microparticles and Neutrophil Extracellular Traps

Arthritis and Rheumatology

Volumn 67, Issue 10, 2015, Pages 2780-2790

  Huang, Yi Min ^a   Wang, Huan ^a   Wang, Chen ^a   Chen, Min ^a   Zhao, Ming Hui ^a  

^a PEKING UNIVERSITY FIRST HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C5A; NEUTROPHIL CYTOPLASMIC ANTIBODY; NUCLEOSOME; THROMBIN; THROMBOPLASTIN;

ADULT; AGED; ANCA ASSOCIATED VASCULITIS; CASE CONTROL STUDY; CELL CULTURE; COMPLICATION; CONFOCAL MICROSCOPY; DRUG EFFECTS; EXTRACELLULAR TRAP; FEMALE; HUMAN; MALE; MEMBRANE MICROPARTICLE; METABOLISM; MIDDLE AGED; NEUTROPHIL; NUCLEOSOME; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; THROMBOPHILIA;

ADULT; AGED; ANTI-NEUTROPHIL CYTOPLASMIC ANTIBODY-ASSOCIATED VASCULITIS; ANTIBODIES, ANTINEUTROPHIL CYTOPLASMIC; CASE-CONTROL STUDIES; CELL-DERIVED MICROPARTICLES; CELLS, CULTURED; COMPLEMENT C5A; EXTRACELLULAR TRAPS; FEMALE; HUMANS; MALE; MICROSCOPY, CONFOCAL; MIDDLE AGED; NEUTROPHILS; NUCLEOSOMES; THROMBIN; THROMBOPHILIA; THROMBOPLASTIN;

EID: 84988837994     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/ART.39239     Document Type: Article

References (50)

1. Jennette JC, Falk RJ, Bacon PA, Basu N, Cid MC, Ferrario F, et al. 2012 revised International Chapel Hill Consensus Conference Nomenclature of Vasculitides. Arthritis Rheum 2013;65:1–11.
2. Segelmark M, Wieslander J. IgG subclasses of antineutrophil cytoplasm autoantibodies (ANCA). Nephrol Dial Transplant 1993;8:696–702.
3. Falk RJ, Jennette JC. ANCA small-vessel vasculitis. J Am Soc Nephrol 1997;8:314–22.
4. Merkel PA, Lo GH, Holbrook JT, Tibbs AK, Allen NB, Davis JC Jr, et al. Wegener’s Granulomatosis Etanercept Trial Research Group. High incidence of venous thrombotic events among patients with Wegener granulomatosis: the Wegener’s Clinical Occurrence of Thrombosis (WeCLOT) Study. Ann Intern Med 2005;142:620–6.
5. Weidner S, Hafezi-Rachti S, Rupprecht HD. Thromboembolic events as a complication of antineutrophil cytoplasmic antibody– associated vasculitis. Arthritis Rheum 2006;55:146–9.
6. Stassen PM, Derks RP, Kallenberg CG, Stegeman CA. Venous thromboembolism in ANCA-associated vasculitis: incidence and risk factors. Rheumatology (Oxford) 2008;47:530–4.
7. Allenbach Y, Seror R, Pagnoux C, Teixeira L, Guilpain P, Guillevin L, et al. High frequency of venous thromboembolic events in Churg-Strauss syndrome, Wegener’s granulomatosis and microscopic polyangiitis but not polyarteritis nodosa: a systematic retrospective study on 1130 patients. Ann Rheum Dis 2009;68:564–7.
8. Ma TT, Huang YM, Wang C, Zhao MH, Chen M. Coagulation and fibrinolysis index profile in patients with ANCA-associated vasculitis. PLoS One 2014;9:e97843.
9. Hewins P, Morgan MD, Holden N, Neil D, Williams JM, Savage CO, et al. IL-18 is upregulated in the kidney and primes neutrophil responsiveness in ANCA-associated vasculitis. Kidney Int 2006;69:605–15.
10. Mulder AH, Heeringa P, Brouwer E, Limburg PC, Kallenberg CG. Activation of granulocytes by anti-neutrophil cytoplasmic antibodies (ANCA): an FcgRII-dependent process. Clin Exp Immunol 1994;98:270–8.
11. Keogan MT, Esnault VL, Green AJ, Lockwood CM, Brown DL. Activation of normal neutrophils by anti-neutrophil cytoplasm antibodies. Clin Exp Immunol 1992;90:228–34.
12. Charles LA, Caldas ML, Falk RJ, Terrell RS, Jennette JC. Antibodies against granule proteins activate neutrophils in vitro. J Leukoc Biol 1991;50:539–46.
13. Falk RJ, Terrell RS, Charles LA, Jennette JC. Anti-neutrophil cytoplasmic autoantibodies induce neutrophils to degranulate and produce oxygen radicals in vitro. Proc Natl Acad Sci U S A 1990;87:4115–9.
14. Cartin-Ceba R, Peikert T, Specks U. Pathogenesis of ANCAassociated vasculitis. Curr Rheumatol Rep 2012;14:481–93.
15. Xiao H, Heeringa P, Hu P, Liu Z, Zhao M, Aratani Y, et al. Antineutrophil cytoplasmic autoantibodies specific for myeloperoxidase cause glomerulonephritis and vasculitis in mice. J Clin Invest 2002;110:955–63.
16. Xiao H, Heeringa P, Liu Z, Huugen D, Hu P, Maeda N, et al. The role of neutrophils in the induction of glomerulonephritis by anti-myeloperoxidase antibodies. Am J Pathol 2005;167:39–45.
17. Gou SJ, Yuan J, Chen M, Yu F, Zhao MH. Circulating complement activation in patients with anti-neutrophil cytoplasmic antibody-associated vasculitis. Kidney Int 2013;83:129–37.
18. Xing GQ, Chen M, Liu G, Heeringa P, Zhang JJ, Zheng X, et al. Complement activation is involved in renal damage in human antineutrophil cytoplasmic autoantibody associated pauci-immune vasculitis. J Clin Immunol 2009;29:282–91.
19. Xiao H, Schreiber A, Heeringa P, Falk RJ, Jennette JC. Alternative complement pathway in the pathogenesis of disease mediated by anti-neutrophil cytoplasmic autoantibodies. Am J Pathol 2007;170:52–64.
20. Huugen D, van Esch A, Xiao H, Peutz-Kootstra CJ, Buurman WA, Tervaert JW, et al. Inhibition of complement factor C5 protects against anti-myeloperoxidase antibody-mediated glomerulonephritis in mice. Kidney Int 2007;71:646–54.
21. Yuan J, Gou SJ, Huang J, Hao J, Chen M, Zhao MH. C5a and its receptors in human anti-neutrophil cytoplasmic antibody (ANCA)-associated vasculitis. Arthritis Res Ther 2012;14:R140.
22. Xiao H, Dairaghi DJ, Powers JP, Ertl LS, Baumgart T, Wang Y, et al. C5a receptor (CD88) blockade protects against MPO-ANCA GN. J Am Soc Nephrol 2014;25:225–31.
23. 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;15:75–89.
24. Kourtzelis I, Markiewski MM, Doumas M, Rafail S, Kambas K, Mitroulis I, et al. Complement anaphylatoxin C5a contributes to hemodialysis-associated thrombosis. Blood 2010;116:631–9.
25. Kambas K, Markiewski MM, Pneumatikos IA, Rafail SS, Theodorou V, Konstantonis D, et al. C5a and TNF-a up-regulate the expression of tissue factor in intra-alveolar neutrophils of patients with the acute respiratory distress syndrome. J Immunol 2008; 180:7368–75.
26. Redecha P, Tilley R, Tencati M, Salmon JE, Kirchhofer D, Mackman N, et al. Tissue factor: a link between C5a and neutrophil activation in antiphospholipid antibody induced fetal injury. Blood 2007;110:2423–31.
27. Kambas K, Chrysanthopoulou A, Vassilopoulos D, Apostolidou E, Skendros P, Girod A, 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;73:1854–63.
28. Von Bruhl ML, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012;209:819–35.
29. Kambas K, Mitroulis I, Apostolidou E, Girod A, Chrysanthopoulou A, Pneumatikos I, et al. Autophagy mediates the delivery of thrombogenic tissue factor to neutrophil extracellular traps in human sepsis. PLoS One 2012;7:e45427.
30. Luqmani RA, Bacon PA, Moots RJ, Janssen BA, Pall A, Emery P, et al. Birmingham Vasculitis Activity Score (BVAS) in systemic necrotizing vasculitis. QJM 1994;87:671–8.
31. Hao J, Meng LQ, Xu PC, Chen M, Zhao MH. p38MAPK, ERK and PI3K signaling pathways are involved in C5a-primed neutrophils for ANCA-mediated activation. PLoS One 2012;7:e38317.
32. Schreiber A, Rolle S, Peripelittchenko L, Rademann J, Schneider W, Luft FC, et al. Phosphoinositol 3-kinase-g mediates antineutrophil cytoplasmic autoantibody-induced glomerulonephritis. Kidney Int 2010;77:118–28.
33. Choi M, Rolle S, Rane M, Haller H, Luft FC, Kettritz R. Extracellular signal-regulated kinase inhibition by statins inhibits neutrophil activation by ANCA. Kidney Int 2003;63:96–106.
34. Theilgaard-Monch K, Jacobsen LC, Rasmussen T, Niemann CU, Udby L, Borup R, et al. Highly glycosylated a1-acid glycoprotein is synthesized in myelocytes, stored in secondary granules, and released by activated neutrophils. J Leukoc Biol 2005;78:462–70.
35. Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol 2010;191:677–91.
36. Jacobsen LC, Theilgaard-Monch K, Christensen EI, Borregaard N. Arginase 1 is expressed in myelocytes/metamyelocytes and localized in gelatinase granules of human neutrophils. Blood 2007;109:3084–7.
37. Hao J, Wang C, Yuan J, Chen M, Zhao MH. A pro-inflammatory role of C5L2 in C5a-primed neutrophils for ANCA-induced activation. PLoS One 2013;8:e66305.
38. Hong Y, Eleftheriou D, Hussain AA, Price-Kuehne FE, Savage CO, Jayne D, et al. Anti-neutrophil cytoplasmic antibodies stimulate release of neutrophil microparticles. J Am Soc Nephrol 2012;23:49–62.
39. Wang JG, Williams JC, Davis BK, Jacobson K, Doerschuk CM, Ting JP, et al. Monocytic microparticles activate endothelial cells in an IL-1b-dependent manner. Blood 2011;118:2366–74.
40. Gyorgy B, Modos K, Pallinger E, Paloczi K, Pasztoi M, Misjak P, et al. Detection and isolation of cell-derived microparticles are compromised by protein complexes resulting from shared biophysical parameters. Blood 2011;117:e39–48.
41. Metzler KD, Fuchs TA, Nauseef WM, Reumaux D, Roesler J, Schulze I, et al. Myeloperoxidase is required for neutrophil extracellular trap formation: implications for innate immunity. Blood 2011;117:953–9.
42. Gonzalez AS, Bardoel BW, Harbort CJ, Zychlinsky A. Induction and quantification of neutrophil extracellular traps. Methods Mol Biol 2014;1124:307–18.
43. Massberg S, Grahl L, von Bruehl ML, Manukyan D, Pfeiler S, Goosmann C, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 2010; 16:887–96.
44. Petri M. Hopkins Lupus Cohort: 1999 update. Rheum Dis Clin North Am 2000;26:199–213.
45. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science 2004;303:1532–5.
46. Brill A, Fuchs TA, Savchenko AS, Thomas GM, Martinod K, De Meyer SF, et al. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost 2012;10:136–44.
47. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci U S A 2010;107:15880–5.
48. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007;13:463–9.
49. Nakazawa D, Tomaru U, Yamamoto C, Jodo S, Ishizu A. Abundant neutrophil extracellular traps in thrombus of patient with microscopic polyangiitis. Front Immunol 2012;3:333.
50. Fuchs TA, Kremer Hovinga JA, Schatzberg D, Wagner DD, Lammle B. Circulating DNA and myeloperoxidase indicate disease activity in patients with thrombotic microangiopathies. Blood 2012;120:1157–64.