Neutrophil extracellular traps in atherosclerosis and atherothrombosis

Circulation Research

Volumn 120, Issue 4, 2017, Pages 736-743

  Döring, Yvonne ^a   Soehnlein, Oliver ^a,b,c   Weber, Christian ^a,b,d  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

^d MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

atherosclerosis; coronary artery disease; extracellular trap; neutrophils; thrombosis

Indexed keywords

ARTERY THROMBOSIS; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; EXTRACELLULAR TRAP; HEART INFARCTION; HUMAN; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; METABOLISM; NEUTROPHIL; PATHOLOGY; THROMBOSIS;

ANIMALS; ATHEROSCLEROSIS; EXTRACELLULAR TRAPS; HUMANS; NEUTROPHILS; THROMBOSIS;

EID: 85013271871     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.309692     Document Type: Review

References (103)

1. Soehnlein O, Lindbom L, Phagocyte partnership during the onset and resolution of inflammation. Nat Rev Immunol 2010 10 427 439. doi: 10.1038/nri2779
2. Nauseef WM, Borregaard N, Neutrophils at work. Nat Immunol 2014 15 602 611. doi: 10.1038/ni.2921
3. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A, Neutrophil extracellular traps kill bacteria. Science 2004 303 1532 1535. doi: 10.1126/science.1092385
4. Brinkmann V, Zychlinsky A, Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol 2007 5 577 582. doi: 10.1038/nrmicro1710
5. Branzk N, Lubojemska A, Hardison SE, Wang Q, Gutierrez MG, Brown GD, Papayannopoulos V, Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat Immunol 2014 15 1017 1025. doi: 10.1038/ni.2987
6. Boe DM, Curtis BJ, Chen MM, Ippolito JA, Kovacs EJ, Extracellular traps and macrophages: new roles for the versatile phagocyte. J Leukoc Biol 2015 97 1023 1035. doi: 10.1189/jlb.4RI1014-521R.
7. Möllerherm H, Von Köckritz-Blickwede M, Branitzki-Heinemann K, Antimicrobial activity of mast cells: role and relevance of extracellular DNA traps. Front Immunol 2016 7 265. doi: 10.3389/fimmu.2016.00265
8. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A, Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007 176 231 241. doi: 10.1083/jcb.200606027
9. Olsson AK, Cedervall J, NETosis in cancer-platelet-neutrophil crosstalk promotes tumor-associated pathology. Front Immunol 2016 7 373. doi: 10.3389/fimmu.2016.00373
10. Grayson PC, Kaplan MJ, At the bench: neutrophil extracellular traps (NETs) highlight novel aspects of innate immune system involvement in autoimmune diseases. J Leukoc Biol 2016 99 253 264. doi: 10.1189/jlb.5BT0615-247R.
11. Pinegin B, Vorobjeva N, Pinegin V, Neutrophil extracellular traps and their role in the development of chronic inflammation and autoimmunity. Autoimmun Rev 2015 14 633 640. doi: 10.1016/j.autrev.2015.03.002
12. Weber C, Noels H, Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 2011 17 1410 1422. doi: 10.1038/nm.2538
13. Lippi G, Franchini M, Targher G, Arterial thrombus formation in cardiovascular disease. Nat Rev Cardiol 2011 8 502 512. doi: 10.1038/nrcardio.2011.91
14. Döring Y, Drechsler M, Wantha S, Kemmerich K, Lievens D, Vijayan S, Gallo RL, Weber C, Soehnlein O, Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice. Circ Res 2012 110 1052 1056. doi: 10.1161/CIRCRESAHA.112.265868
15. Drechsler M, Megens RT, Van Zandvoort M, Weber C, Soehnlein O, Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation 2010 122 1837 1845. doi: 10.1161/CIRCULATIONAHA.110.961714
16. Wantha S, Alard JE, Megens RT, Van Der Does AM, Döring Y, Drechsler M, Pham CT, Wang MW, Wang JM, Gallo RL, Von Hundelshausen P, Lindbom L, Hackeng T, Weber C, Soehnlein O, Neutrophil-derived cathelicidin promotes adhesion of classical monocytes. Circ Res 2013 112 792 801. doi: 10.1161/CIRCRESAHA.112.300666
17. Soehnlein O, Multiple roles for neutrophils in atherosclerosis. Circ Res 2012 110 875 888. doi: 10.1161/CIRCRESAHA.111.257535
18. Zernecke A, Bot I, Djalali-Talab Y, Shagdarsuren E, Bidzhekov K, Meiler S, Krohn R, Schober A, Sperandio M, Soehnlein O, Bornemann J, Tacke F, Biessen EA, Weber C, Protective role of CXC receptor 4/CXC ligand 12 unveils the importance of neutrophils in atherosclerosis. Circ Res 2008 102 209 217. doi: 10.1161/CIRCRESAHA.107.160697
19. Ionita MG, Van den Borne P, Catanzariti LM, Moll FL, de Vries JP, Pasterkamp G, Vink A, de Kleijn DP, High neutrophil numbers in human carotid atherosclerotic plaques are associated with characteristics of rupture-prone lesions. Arterioscler Thromb Vasc Biol 2010 30 1842 1848. doi: 10.1161/ATVBAHA.110.209296
20. Marino F, Tozzi M, Schembri L, Ferraro S, Tarallo A, Scanzano A, Legnaro M, Castelli P, Cosentino M, Production of IL-8, VEGF and elastase by circulating and intraplaque neutrophils in patients with carotid atherosclerosis. PLoS One 2015 10 e0124565. doi: 10.1371/journal.pone.0124565
21. Naruko T, Ueda M, Haze K, Van Der Wal AC, Van Der Loos CM, Itoh A, Komatsu R, Ikura Y, Ogami M, Shimada Y, Ehara S, Yoshiyama M, Takeuchi K, Yoshikawa J, Becker AE, Neutrophil infiltration of culprit lesions in acute coronary syndromes. Circulation 2002 106 2894 2900
22. Nencioni A, da Silva RF, Fraga-Silva RA, Nicotinamide phosphoribosyltransferase inhibition reduces intraplaque CXCL1 production and associated neutrophil infiltration in atherosclerotic mice. Thromb Haemost 2014 111 308 322. doi: 10.1160/TH13-07-0531
23. Pende A, Artom N, Bertolotto M, Montecucco F, Dallegri F, Role of neutrophils in atherogenesis: an update. Eur J Clin Invest 2016 46 252 263. doi: 10.1111/eci.12566
24. Quinn KL, Henriques M, Tabuchi A, Human neutrophil peptides mediate endothelial-monocyte interaction, foam cell formation, and platelet activation. Arterioscler Thromb Vasc Biol 2011 31 2070 2079. doi: 10.1161/ATVBAHA.111.227116
25. Rotzius P, Thams S, Soehnlein O, Kenne E, Tseng CN, Björkström NK, Malmberg KJ, Lindbom L, Eriksson EE, Distinct infiltration of neutrophils in lesion shoulders in ApoE-/- mice. Am J Pathol 2010 177 493 500. doi: 10.2353/ajpath.2010.090480
26. Van Leeuwen M, Gijbels MJ, Duijvestijn A, Smook M, Van de Gaar MJ, Heeringa P, de Winther MP, Tervaert JW, Accumulation of myeloperoxidase-positive neutrophils in atherosclerotic lesions in LDLR-/- mice. Arterioscler Thromb Vasc Biol 2008 28 84 89. doi: 10.1161/ATVBAHA.107.154807
27. Döring Y, Drechsler M, Soehnlein O, Weber C, Neutrophils in atherosclerosis: from mice to man. Arterioscler Thromb Vasc Biol 2015 35 288 295. doi: 10.1161/ATVBAHA.114.303564
28. Moreno JA, Ortega-Gómez A, Delbosc S, Beaufort N, Sorbets E, Louedec L, Esposito-Farèse M, Tubach F, Nicoletti A, Steg PG, Michel JB, Feldman L, Meilhac O, In vitro and in vivo evidence for the role of elastase shedding of CD163 in human atherothrombosis. Eur Heart J 2012 33 252 263. doi: 10.1093/eurheartj/ehr123
29. Sørensen OE, Borregaard N, Neutrophil extracellular traps-the dark side of neutrophils. J Clin Invest 2016 126 1612 1620. doi: 10.1172/JCI84538
30. Karlsson A, Dahlgren C, Assembly and activation of the neutrophil NADPH oxidase in granule membranes. Antioxid Redox Signal 2002 4 49 60. doi: 10.1089/152308602753625852
31. Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A, Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol 2010 191 677 691. doi: 10.1083/jcb.201006052
32. Wang Y, Li M, Stadler S, Correll S, Li P, Wang D, Hayama R, Leonelli L, Han H, Grigoryev SA, Allis CD, Coonrod SA, Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 2009 184 205 213. doi: 10.1083/jcb.200806072
33. Kolaczkowska E, Jenne CN, Surewaard BG, Thanabalasuriar A, Lee WY, Sanz MJ, Mowen K, Opdenakker G, Kubes P, Molecular mechanisms of NET formation and degradation revealed by intravital imaging in the liver vasculature. Nat Commun 2015 6 6673. doi: 10.1038/ncomms7673
34. Pilsczek FH, Salina D, Poon KK, Fahey C, Yipp BG, Sibley CD, Robbins SM, Green FH, Surette MG, Sugai M, Bowden MG, Hussain M, Zhang K, Kubes P, A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 2010 185 7413 7425. doi: 10.4049/jimmunol.1000675
35. Byrd AS, O'Brien XM, Johnson CM, Lavigne LM, Reichner JS, An extracellular matrix-based mechanism of rapid neutrophil extracellular trap formation in response to Candida albicans. J Immunol 2013 190 4136 4148. doi: 10.4049/jimmunol.1202671
36. Yipp BG, Kubes P, NETosis: how vital is it? Blood 2013 122 2784 2794. doi: 10.1182/blood-2013-04-457671
37. Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD, Pittman K, Asaduzzaman M, Wu K, Meijndert HC, Malawista SE, de Boisfleury Chevance A, Zhang K, Conly J, Kubes P, Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 2012 18 1386 1393. doi: 10.1038/nm.2847
38. Konig MF, Andrade F, A critical reappraisal of neutrophil extracellular traps and netosis mimics based on differential requirements for protein citrullination. Front Immunol 2016 7 461. doi: 10.3389/fimmu.2016.00461
39. Yousefi S, Mihalache C, Kozlowski E, Schmid I, Simon HU, Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ 2009 16 1438 1444. doi: 10.1038/cdd.2009.96.
40. Yousefi S, Gold JA, Andina N, Lee JJ, Kelly AM, Kozlowski E, Schmid I, Straumann A, Reichenbach J, Gleich GJ, Simon HU, Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med 2008 14 949 953. doi: 10.1038/nm.1855
41. Itagaki K, Kaczmarek E, Lee YT, Tang IT, Isal B, Adibnia Y, Sandler N, Grimm MJ, Segal BH, Otterbein LE, Hauser CJ, Mitochondrial DNA released by trauma induces neutrophil extracellular traps. PLoS One 2015 10 e0120549. doi: 10.1371/journal.pone.0120549
42. McIlroy DJ, Jarnicki AG, Au GG, Lott N, Smith DW, Hansbro PM, Balogh ZJ, Mitochondrial DNA neutrophil extracellular traps are formed after trauma and subsequent surgery. J Crit Care 2014 29 1133.e1 1133.e5. doi: 10.1016/j.jcrc.2014.07.013
43. Yang H, Biermann MH, Brauner JM, Liu Y, Zhao Y, Herrmann M, New insights into neutrophil extracellular traps: mechanisms of formation and role in inflammation. Front Immunol 2016 7 302. doi: 10.3389/fimmu.2016.00302
44. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR, Zychlinsky A, Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009 5 e1000639. doi: 10.1371/journal.ppat.1000639
45. Rochael NC, Guimarães-Costa AB, Nascimento MT, DeSouza-Vieira TS, Oliveira MP, Garcia e Souza LF, Oliveira MF, Saraiva EM, Classical ROS-dependent and early/rapid ROS-independent release of neutrophil extracellular traps triggered by Leishmania parasites. Sci Rep 2015 5 18302. doi: 10.1038/srep18302
46. Saitoh T, Komano J, Saitoh Y, Misawa T, Takahama M, Kozaki T, Uehata T, Iwasaki H, Omori H, Yamaoka S, Yamamoto N, Akira S, Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 2012 12 109 116. doi: 10.1016/j.chom.2012.05.015
47. Martinelli S, Urosevic M, Daryadel A, Oberholzer PA, Baumann C, Fey MF, Dummer R, Simon HU, Yousefi S, Induction of genes mediating interferon-dependent extracellular trap formation during neutrophil differentiation. J Biol Chem 2004 279 44123 44132. doi: 10.1074/jbc.M405883200
48. Khandpur R, Carmona-Rivera C, Vivekanandan-Giri A, Gizinski A, Yalavarthi S, Knight JS, Friday S, Li S, Patel RM, Subramanian V, Thompson P, Chen P, Fox DA, Pennathur S, Kaplan MJ, NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci Transl Med 2013 5 178ra40. doi: 10.1126/scitranslmed.3005580
49. Rossaint J, Herter JM, Van Aken H, Napirei M, Döring Y, Weber C, Soehnlein O, Zarbock A, Synchronized integrin engagement and chemokine activation is crucial in neutrophil extracellular trap-mediated sterile inflammation. Blood 2014 123 2573 2584. doi: 10.1182/blood-2013-07-516484
50. Warnatsch A, Ioannou M, Wang Q, Papayannopoulos V, Inflammation. Neutrophil extracellular traps license macrophages for cytokine production in atherosclerosis. Science 2015 349 316 320. doi: 10.1126/science.aaa8064
51. Schauer C, Janko C, Munoz LE, Aggregated neutrophil extracellular traps limit inflammation by degrading cytokines and chemokines. Nat Med 2014 20 511 517. doi: 10.1038/nm.3547
52. Kessenbrock K, Krumbholz M, Schönermarck U, Back W, Gross WL, Werb Z, Gröne HJ, Brinkmann V, Jenne DE, Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 2009 15 623 625. doi: 10.1038/nm.1959
53. Garcia-Romo GS, Caielli S, Vega B, Connolly J, Allantaz F, Xu Z, Punaro M, Baisch J, Guiducci C, Coffman RL, Barrat FJ, Banchereau J, Pascual V, Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med 2011 3 73ra20. doi: 10.1126/scitranslmed.3001201
54. Döring Y, Manthey HD, Drechsler M, Auto-antigenic protein-DNA complexes stimulate plasmacytoid dendritic cells to promote atherosclerosis. Circulation 2012 125 1673 1683. doi: 10.1161/CIRCULATIONAHA.111.046755
55. Massberg S, Grahl L, Von Bruehl ML, Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 2010 16 887 896. doi: 10.1038/nm.2184
56. Brinkmann V, Zychlinsky A, Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 2012 198 773 783. doi: 10.1083/jcb.201203170
57. Halverson TW, Wilton M, Poon KK, Petri B, Lewenza S, DNA is an antimicrobial component of neutrophil extracellular traps. PLoS Pathog 2015 11 e1004593. doi: 10.1371/journal.ppat.1004593
58. Kolaczkowska E, Kubes P, Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 2013 13 159 175. doi: 10.1038/nri3399
59. Jaillon S, Peri G, Delneste Y, Frémaux I, Doni A, Moalli F, Garlanda C, Romani L, Gascan H, Bellocchio S, Bozza S, Cassatella MA, Jeannin P, Mantovani A, The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. J Exp Med 2007 204 793 804. doi: 10.1084/jem.20061301
60. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR, Zychlinsky A, Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009 5 e1000639. doi: 10.1371/journal.ppat.1000639
61. Csomós K, Kristóf E, Jakob B, Csomós I, Kovács G, Rotem O, Hodrea J, Bagoly Z, Muszbek L, Balajthy Z, Cssz É Fésüs L, Protein cross-linking by chlorinated polyamines and transglutamylation stabilizes neutrophil extracellular traps. Cell Death Dis 2016 7 e2332. doi: 10.1038/cddis.2016.200
62. Knight JS, Carmona-Rivera C, Kaplan MJ, Proteins derived from neutrophil extracellular traps may serve as self-antigens and mediate organ damage in autoimmune diseases. Front Immunol 2012 3 380. doi: 10.3389/fimmu.2012.00380
63. Rahman S, Gadjeva M, Does NETosis contribute to the bacterial pathoadaptation in cystic fibrosis? Front Immunol 2014 5 378. doi: 10.3389/fimmu.2014.00378
64. Menegazzi R, Decleva E, Dri P, Killing by neutrophil extracellular traps: fact or folklore? Blood 2012 119 1214 1216. doi: 10.1182/blood-2011-07-364604
65. Xu Z, Cai J, Gao J, White GC 2nd, Chen F, Ma YQ, Interaction of kindlin-3 and β2-integrins differentially regulates neutrophil recruitment and NET release in mice. Blood 2015 126 373 377. doi: 10.1182/blood-2015-03-636720
66. Bianchi M, Hakkim A, Brinkmann V, Siler U, Seger RA, Zychlinsky A, Reichenbach J, Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 2009 114 2619 2622. doi: 10.1182/blood-2009-05-221606
67. Li P, Li M, Lindberg MR, Kennett MJ, Xiong N, Wang Y, PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med 2010 207 1853 1862. doi: 10.1084/jem.20100239
68. Martinod K, Fuchs TA, Zitomersky NL, Wong SL, Demers M, Gallant M, Wang Y, Wagner DD, PAD4-deficiency does not affect bacteremia in polymicrobial sepsis and ameliorates endotoxemic shock. Blood 2015 125 1948 1956. doi: 10.1182/blood-2014-07-587709
69. Mohanty T, Sjögren J, Kahn F, Abu-Humaidan AH, Fisker N, Assing K, Mörgelin M, Bengtsson AA, Borregaard N, Sørensen OE, A novel mechanism for NETosis provides antimicrobial defense at the oral mucosa. Blood 2015 126 2128 2137. doi: 10.1182/blood-2015-04-641142
70. Pham CT, Ivanovich JL, Raptis SZ, Zehnbauer B, Ley TJ, Papillon-Lefèvre syndrome: correlating the molecular, cellular, and clinical consequences of cathepsin C/dipeptidyl peptidase I deficiency in humans. J Immunol 2004 173 7277 7281
71. Sørensen OE, Clemmensen SN, Dahl SL, Østergaard O, Heegaard NH, Glenthøj A, Nielsen FC, Borregaard N, Papillon-Lefèvre syndrome patient reveals species-dependent requirements for neutrophil defenses. J Clin Invest 2014 124 4539 4548. doi: 10.1172/JCI76009
72. Finn AV, Nakano M, Narula J, Kolodgie FD, Virmani R, Concept of vulnerable/unstable plaque. Arterioscler Thromb Vasc Biol 2010 30 1282 1292. doi: 10.1161/ATVBAHA.108.179739
73. Megens RT, Vijayan S, Lievens D, Döring Y, Van Zandvoort MA, Grommes J, Weber C, Soehnlein O, Presence of luminal neutrophil extracellular traps in atherosclerosis. Thromb Haemost 2012 107 597 598. doi: 10.1160/TH11-09-0650
74. Quillard T, Araújo HA, Franck G, Shvartz E, Sukhova G, Libby P, TLR2 and neutrophils potentiate endothelial stress, apoptosis and detachment: implications for superficial erosion. Eur Heart J 2015 36 1394 1404. doi: 10.1093/eurheartj/ehv044
75. Macritchie N, Grassia G, Sabir SR, Maddaluno M, Welsh P, Sattar N, Ialenti A, Kurowska-Stolarska M, McInnes IB, Brewer JM, Garside P, Maffia P, Plasmacytoid dendritic cells play a key role in promoting atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2012 32 2569 2579. doi: 10.1161/ATVBAHA.112.251314
76. Carmona-Rivera C, Zhao W, Yalavarthi S, Kaplan MJ, Neutrophil extracellular traps induce endothelial dysfunction in systemic lupus erythematosus through the activation of matrix metalloproteinase-2. Ann Rheum Dis 2015 74 1417 1424. doi: 10.1136/annrheumdis-2013-204837
77. Villanueva E, Yalavarthi S, Berthier CC, Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol 2011 187 538 552. doi: 10.4049/jimmunol.1100450
78. Gupta AK, Joshi MB, Philippova M, Erne P, Hasler P, Hahn S, Resink TJ, Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death. FEBS Lett 2010 584 3193 3197. doi: 10.1016/j.febslet.2010.06.006
79. Knight JS, Luo W, O'Dell AA, Yalavarthi S, Zhao W, Subramanian V, Guo C, Grenn RC, Thompson PR, Eitzman DT, Kaplan MJ, Peptidylarginine deiminase inhibition reduces vascular damage and modulates innate immune responses in murine models of atherosclerosis. Circ Res 2014 114 947 956. doi: 10.1161/CIRCRESAHA.114.303312
80. Soehnlein O, Ortega-Gómez A, Döring Y, Weber C, Neutrophil-macrophage interplay in atherosclerosis: protease-mediated cytokine processing versus NET release. Thromb Haemost 2015 114 866 867. doi: 10.1160/TH15-08-0623
81. Joosten LA, Netea MG, Fantuzzi G, Koenders MI, Helsen MM, Sparrer H, Pham CT, Van Der Meer JW, Dinarello CA, Van den Berg WB, Inflammatory arthritis in caspase 1 gene-deficient mice: contribution of proteinase 3 to caspase 1-independent production of bioactive interleukin-1beta. Arthritis Rheum 2009 60 3651 3662. doi: 10.1002/art.25006
82. Borissoff JI, Joosen IA, Versteylen MO, Brill A, Fuchs TA, Savchenko AS, Gallant M, Martinod K, Ten Cate H, Hofstra L, Crijns HJ, Wagner DD, Kietselaer BL, Elevated levels of circulating DNA and chromatin are independently associated with severe coronary atherosclerosis and a prothrombotic state. Arterioscler Thromb Vasc Biol 2013 33 2032 2040. doi: 10.1161/ATVBAHA.113.301627
83. Kimball AS, Obi AT, Diaz JA, Henke PK, The emerging role of NETs in venous thrombosis and immunothrombosis. Front Immunol 2016 7 236. doi: 10.3389/fimmu.2016.00236
84. Von Brühl ML, Stark K, Steinhart A, Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012 209 819 835. doi: 10.1084/jem.20112322
85. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, Wrobleski SK, Wakefield TW, Hartwig JH, Wagner DD, Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci U S A 2010 107 15880 15885. doi: 10.1073/pnas.1005743107
86. Libby P, Ridker PM, Hansson GK, Progress and challenges in translating the biology of atherosclerosis. Nature 2011 473 317 325. doi: 10.1038/nature10146
87. Wyss CA, Neidhart M, Altwegg L, Spanaus KS, Yonekawa K, Wischnewsky MB, Corti R, Kucher N, Roffi M, Eberli FR, Amann-Vesti B, Gay S, Von Eckardstein A, Lüscher TF, Maier W, Cellular actors, Toll-like receptors, and local cytokine profile in acute coronary syndromes. Eur Heart J 2010 31 1457 1469. doi: 10.1093/eurheartj/ehq084
88. Horne BD, Anderson JL, John JM, Weaver A, Bair TL, Jensen KR, Renlund DG, Muhlestein JB, Intermountain Heart Collaborative Study Group Which white blood cell subtypes predict increased cardiovascular risk? J Am Coll Cardiol 2005 45 1638 1643. doi: 10.1016/j.jacc.2005.02.054
89. Distelmaier K, Winter MP, Dragschitz F, Redwan B, Mangold A, Gleiss A, Perkmann T, Maurer G, Adlbrecht C, Lang IM, Prognostic value of culprit site neutrophils in acute coronary syndrome. Eur J Clin Invest 2014 44 257 265. doi: 10.1111/eci.12228
90. Distelmaier K, Adlbrecht C, Jakowitsch J, Winkler S, Dunkler D, Gerner C, Wagner O, Lang IM, Kubicek M, Local complement activation triggers neutrophil recruitment to the site of thrombus formation in acute myocardial infarction. Thromb Haemost 2009 102 564 572. doi: 10.1160/TH09-02-0103
91. Riegger J, Byrne RA, Joner M, Prevention of Late Stent Thrombosis by an Interdisciplinary Global European Effort (PRESTIGE) Investigators Histopathological evaluation of thrombus in patients presenting with stent thrombosis. A multicenter European study: a report of the prevention of late stent thrombosis by an interdisciplinary global European effort consortium. Eur Heart J 2016 37 1538 1549. doi: 10.1093/eurheartj/ehv419
92. Oklu R, Albadawi H, Watkins MT, Monestier M, Sillesen M, Wicky S, Detection of extracellular genomic DNA scaffold in human thrombus: implications for the use of deoxyribonuclease enzymes in thrombolysis. J Vasc Interv Radiol 2012 23 712 718. doi: 10.1016/j.jvir.2012.01.072
93. Mangold A, Alias S, Scherz T, Coronary neutrophil extracellular trap burden and deoxyribonuclease activity in ST-elevation acute coronary syndrome are predictors of ST-segment resolution and infarct size. Circ Res 2015 116 1182 1192. doi: 10.1161/CIRCRESAHA.116.304944
94. Maugeri N, Campana L, Gavina M, Covino C, De Metrio M, Panciroli C, Maiuri L, Maseri A, D'Angelo A, Bianchi ME, Rovere-Querini P, Manfredi AA, 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 2074 2088. doi: 10.1111/jth.12710
95. Stark K, Philippi V, Stockhausen S, Disulfide HMGB1 derived from platelets coordinates venous thrombosis in mice. Blood 2016 128 2435 2449. doi: 10.1182/blood-2016-04-710632
96. de Boer OJ, Li X, Teeling P, Mackaay C, Ploegmakers HJ, Van Der Loos CM, Daemen MJ, de Winter RJ, Van Der Wal AC, Neutrophils, neutrophil extracellular traps and interleukin-17 associate with the organisation of thrombi in acute myocardial infarction. Thromb Haemost 2013 109 290 297. doi: 10.1160/TH12-06-0425
97. Darbousset R, Thomas GM, Mezouar S, Frère C, Bonier R, Mackman N, Renné T, Dignat-George F, Dubois C, Panicot-Dubois L, Tissue factor-positive neutrophils bind to injured endothelial wall and initiate thrombus formation. Blood 2012 120 2133 2143. doi: 10.1182/blood-2012-06-437772
98. Stakos DA, Kambas K, Konstantinidis T, Mitroulis I, Apostolidou E, Arelaki S, Tsironidou V, Giatromanolaki A, Skendros P, Konstantinides S, Ritis K, Expression of functional tissue factor by neutrophil extracellular traps in culprit artery of acute myocardial infarction. Eur Heart J 2015 36 1405 1414. doi: 10.1093/eurheartj/ehv007
99. Rangé H, Labreuche J, Louedec L, Rondeau P, Planesse C, Sebbag U, Bourdon E, Michel JB, Bouchard P, Meilhac O, Periodontal bacteria in human carotid atherothrombosis as a potential trigger for neutrophil activation. Atherosclerosis 2014 236 448 455. doi: 10.1016/j.atherosclerosis.2014.07.034
100. Ge L, Zhou X, Ji WJ, Lu RY, Zhang Y, Zhang YD, Ma YQ, Zhao JH, Li YM, Neutrophil extracellular traps in ischemia-reperfusion injury-induced myocardial no-reflow: therapeutic potential of DNase-based reperfusion strategy. Am J Physiol Heart Circ Physiol 2015 308 H500 H509. doi: 10.1152/ajpheart.00381.2014
101. Savchenko AS, Borissoff JI, Martinod K, De Meyer SF, Gallant M, Erpenbeck L, Brill A, Wang Y, Wagner DD, VWF-mediated leukocyte recruitment with chromatin decondensation by PAD4 increases myocardial ischemia/reperfusion injury in mice. Blood 2014 123 141 148. doi: 10.1182/blood-2013-07-514992
102. De Meyer SF, Suidan GL, Fuchs TA, Monestier M, Wagner DD, Extracellular chromatin is an important mediator of ischemic stroke in mice. Arterioscler Thromb Vasc Biol 2012 32 1884 1891. doi: 10.1161/ATVBAHA.112.250993
103. Vogel B, Shinagawa H, Hofmann U, Ertl G, Frantz S, Acute DNase1 treatment improves left ventricular remodeling after myocardial infarction by disruption of free chromatin. Basic Res Cardiol 2015 110 15. doi: 10.1007/s00395-015-0472-y.