Neutrophil extracellular traps induce endothelial cell activation and tissue factor production through interleukin-1α and cathepsin G

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 38, Issue 8, 2018, Pages 1901-1912

  Folco, Eduardo J ^a   Mawson, Thomas L ^a   Vromman, Amélie ^a   Bernardes Souza, Breno ^a   Franck, Grégory ^a   Persson, Oscar ^a   Nakamura, Momotaro ^a   Newton, Gail ^a   Luscinskas, Francis W ^a   Libby, Peter ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Cathepsin G; Endothelial cells; Extracellular traps; Interleukin 1; Neutrophils; Vascular cell adhesion molecule 1

Indexed keywords

CATHEPSIN G; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1ALPHA; MESSENGER RNA; NEUTRALIZING ANTIBODY; THROMBOPLASTIN; VASCULAR CELL ADHESION MOLECULE 1; CTSG PROTEIN, HUMAN; ICAM1 PROTEIN, HUMAN; IL1A PROTEIN, HUMAN;

ARTICLE; BLOOD CLOTTING; CELL ACTIVATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR TRAP; HUMAN; HUMAN CELL; HUVEC CELL LINE; IN VITRO STUDY; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; THROMBOSIS; CELL ADHESION; COCULTURE; ENZYMOLOGY; GENETICS; METABOLISM; NEUTROPHIL; PARACRINE SIGNALING; SIGNAL TRANSDUCTION; THP-1 CELL LINE; UMBILICAL VEIN ENDOTHELIAL CELL;

BLOOD COAGULATION; CATHEPSIN G; CELL ADHESION; COCULTURE TECHNIQUES; EXTRACELLULAR TRAPS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; INTERLEUKIN-1ALPHA; NEUTROPHILS; PARACRINE COMMUNICATION; SIGNAL TRANSDUCTION; THP-1 CELLS; THROMBOPLASTIN; VASCULAR CELL ADHESION MOLECULE-1;

EID: 85055606442     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.118.311150     Document Type: Article

References (64)

1. Libby P. Mechanisms of acute coronary syndromes and their implications for therapy. N Engl J Med. 2013;368:2004-2013. doi: 10.1056/NEJMra1216063.
2. Quillard T, Franck G, Mawson T, Folco E, Libby P. Mechanisms of erosion of atherosclerotic plaques. Curr Opin Lipidol. 2017;28:434-441. doi: 10.1097/MOL.0000000000000440.
3. Partida RA, Libby P, Crea F, Jang IK. Plaque erosion: a new in vivo diagnosis and a potential major shift in the management of patients with acute coronary syndromes. Eur Heart J. 2018;39:2070-2076. doi: 10.1093/eurheartj/ehx786.
4. Farb A, Burke AP, Tang AL, Liang TY, Mannan P, Smialek J, Virmani R. Coronary plaque erosion without rupture into a lipid core. A frequent cause of coronary thrombosis in sudden coronary death. Circulation. 1996;93:1354-1363.
5. Kolodgie FD, Burke AP, Farb A, Weber DK, Kutys R, Wight TN, Virmani R. Differential accumulation of proteoglycans and hyaluronan in culprit lesions: insights into plaque erosion. Arterioscler Thromb Vasc Biol. 2002;22:1642-1648.
6. Franck G, Mawson T, Sausen G, et al. Flow perturbation mediates neutrophil recruitment and potentiates endothelial injury via TLR2 in mice: implications for superficial erosion. Circ Res. 2017;121:31-42. doi: 10.1161/CIRCRESAHA.117.310694.
7. 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.
8. Franck G, Mawson TL, Folco EJ, et al. Roles of PAD4 and NETosis in experimental atherosclerosis and arterial injury: implications for Superficial Erosion [published online ahead of print March 23, 2018]. Circ Res. doi: 10.1161/CIRCRESAHA.117.312494.
9. Edfeldt K, Swedenborg J, Hansson GK, Yan ZQ. Expression of toll-like receptors in human atherosclerotic lesions: a possible pathway for plaque activation. Circulation. 2002;105:1158-1161.
10. Jia H, Abtahian F, Aguirre AD, et al. In vivo diagnosis of plaque erosion and calcified nodule in patients with acute coronary syndrome by intravascular optical coherence tomography. J Am Coll Cardiol. 2013;62:1748-1758. doi: 10.1016/j.jacc.2013.05.071.
11. Mullick AE, Soldau K, Kiosses WB, Bell TA III, Tobias PS, Curtiss LK. Increased endothelial expression of Toll-like receptor 2 at sites of disturbed blood flow exacerbates early atherogenic events. J Exp Med. 2008;205:373-383. doi: 10.1084/jem.20071096.
12. Tricot O, Mallat Z, Heymes C, Belmin J, Lesèche G, Tedgui A. Relation between endothelial cell apoptosis and blood flow direction in human atherosclerotic plaques. Circulation. 2000;101:2450-2453.
13. Wang Y, Gao H, Kessinger CW, Schmaier A, Jaffer FA, Simon DI. Myeloid-related protein-14 regulates deep vein thrombosis. JCI Insight. 2017;2:91356.
14. 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.
15. 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.
16. 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 USA. 2010;107:15880-15885. doi: 10.1073/pnas.1005743107.
17. Gould TJ, Vu TT, Swystun LL, Dwivedi DJ, Mai SH, Weitz JI, Liaw PC. Neutrophil extracellular traps promote thrombin generation through platelet-dependent and platelet-independent mechanisms. Arterioscler Thromb Vasc Biol. 2014;34:1977-1984. doi: 10.1161/ATVBAHA.114.304114.
18. Martinod K, Wagner DD. Thrombosis: tangled up in NETs. Blood. 2014;123:2768-2776. doi: 10.1182/blood-2013-10-463646.
19. Massberg S, Brand K, Grüner S, Page S, Müller E, Müller I, Bergmeier W, Richter T, Lorenz M, Konrad I, Nieswandt B, Gawaz M. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J Exp Med. 2002;196:887-896.
20. McDonald B, Davis RP, Kim SJ, Tse M, Esmon CT, Kolaczkowska E, Jenne CN. Platelets and neutrophil extracellular traps collaborate to promote intravascular coagulation during sepsis in mice. Blood. 2017;129:1357-1367. doi: 10.1182/blood-2016-09-741298.
21. 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;209:819-835. doi: 10.1084/jem.20112322.
22. Haubitz M, Gerlach M, Kruse HJ, Brunkhorst R. Endothelial tissue factor stimulation by proteinase 3 and elastase. Clin Exp Immunol. 2001;126:584-588.
23. Kim JE, Yoo HJ, Gu JY, Kim HK. Histones induce the procoagulant phenotype of endothelial cells through tissue factor up-regulation and thrombomodulin down-regulation. PLoS One. 2016;11:e0156763. doi: 10.1371/journal.pone.0156763.
24. Sugiyama S, Kugiyama K, Aikawa M, Nakamura S, Ogawa H, Libby P. Hypochlorous acid, a macrophage product, induces endothelial apoptosis and tissue factor expression: involvement of myeloperoxidase-mediated oxidant in plaque erosion and thrombogenesis. Arterioscler Thromb Vasc Biol. 2004;24:1309-1314. doi: 10.1161/01.ATV.0000131784.50633.4f.
25. Yang X, Li L, Liu J, Lv B, Chen F. Extracellular histones induce tissue factor expression in vascular endothelial cells via TLR and activation of NF-κB and AP-1. Thromb Res. 2016;137:211-218. doi: 10.1016/j.thromres.2015.10.012.
26. Reichert JM. Antibodies to watch in 2013: mid-year update. MAbs. 2013;5:513-517. doi: 10.4161/mabs.24990.
27. Bevilacqua MP, Pober JS, Wheeler ME, Cotran RS, Gimbrone MA Jr. Interleukin 1 acts on cultured human vascular endothelium to increase the adhesion of polymorphonuclear leukocytes, monocytes, and related leukocyte cell lines. J Clin Invest. 1985;76:2003-2011. doi: 10.1172/JCI112200.
28. Libby P, Alroy J, Pereira ME. A neuraminidase from Trypanosoma cruzi removes sialic acid from the surface of mammalian myocardial and endothelial cells. J Clin Invest. 1986;77:127-135. doi: 10.1172/JCI112266.
29. Najmeh S, Cools-Lartigue J, Giannias B, Spicer J, Ferri LE. Simplified human neutrophil extracellular traps (NETs) isolation and handling. J Vis Exp. 2015.
30. Jindal HK, Folco EJ, Liu GX, Koren G. Posttranslational modification of voltage-dependent potassium channel Kv1.5: COOH-terminal palmi-toylation modulates its biological properties. Am J Physiol Heart Circ Physiol. 2008;294:H2012-H2021. doi: 10.1152/ajpheart.01374.2007.
31. Alcaide P, Lim YC, Luscinskas FW, Fresno M. Mucin AgC10 from Trypanosoma cruzi Interferes with L-selectin-mediated monocyte adhesion. Infect Immun. 2010;78:1260-1268. doi: 10.1128/IAI.00794-09.
32. Okamoto Y, Ishii S, Croce K, Katsumata H, Fukushima M, Kihara S, Libby P, Minami S. Adiponectin inhibits macrophage tissue factor, a key trigger of thrombosis in disrupted atherosclerotic plaques. Atherosclerosis. 2013;226:373-377. doi: 10.1016/j.atherosclerosis.2012.12.012.
33. Hoppenbrouwers T, Autar ASA, Sultan AR, Abraham TE, van Cappellen WA, Houtsmuller AB, van Wamel WJB, van Beusekom HMM, van Neck JW, de Maat MPM. In vitro induction of NETosis: Comprehensive live imaging comparison and systematic review. PLoS One. 2017;12:e0176472. doi: 10.1371/journal.pone.0176472.
34. Remijsen Q, Kuijpers TW, Wirawan E, Lippens S, Vandenabeele P, Vanden Berghe T. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ. 2011;18:581-588. doi: 10.1038/cdd.2011.1.
35. Ridker PM, Everett BM, Thuren T, et al; CANTOS Trial Group. Antiinflammatory therapy with canakinumab for atherosclerotic disease. N Engl J Med. 2017;377:1119-1131. doi: 10.1056/NEJMoa1707914.
36. Chistiakov DA, Bobryshev YV, Orekhov AN. Neutrophil's weapons in atherosclerosis. Exp Mol Pathol. 2015;99:663-671. doi: 10.1016/j.yexmp. 2015.11.011.
37. Korkmaz B, Horwitz MS, Jenne DE, Gauthier F. Neutrophil elastase, proteinase 3, and cathepsin G as therapeutic targets in human diseases. Pharmacol Rev. 2010;62:726-759. doi: 10.1124/pr.110.002733.
38. Pham CT. Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol. 2006;6:541-550. doi: 10.1038/nri1841.
39. Afonina IS, Müller C, Martin SJ, Beyaert R. Proteolytic processing of interleukin-1 family cytokines: variations on a common theme. Immunity. 2015;42:991-1004. doi: 10.1016/j.immuni.2015.06.003.
40. Dinarello CA. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood. 2011;117:3720-3732. doi: 10.1182/ blood-2010-07-273417.
41. Durand E, Scoazec A, Lafont A, Boddaert J, Al Hajzen A, Addad F, Mirshahi M, Desnos M, Tedgui A, Mallat Z. In vivo induction of endothelial apoptosis leads to vessel thrombosis and endothelial denudation: a clue to the understanding of the mechanisms of thrombotic plaque erosion. Circulation. 2004;109:2503-2506. doi: 10.1161/01.CIR.0000130172. 62481.90.
42. 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.
43. Tiku K, Tiku ML, Skosey JL. Interleukin 1 production by human polymorphonuclear neutrophils. J Immunol. 1986;136:3677-3685.
44. Goh K, Furusawa S, Kawa Y, Negishi-Okitsu S, Mizoguchi M. Production of interleukin-1-alpha and -beta by human peripheral polymorphonuclear neutrophils. Int Arch Allergy Appl Immunol. 1989;88:297-303.
45. Marucha PT, Zeff RA, Kreutzer DL. Cytokine regulation of IL-1 beta gene expression in the human polymorphonuclear leukocyte. J Immunol. 1990;145:2932-2937.
46. Quayle JA, Adams S, Bucknall RC, Edwards SW. Interleukin-1 expression by neutrophils in rheumatoid arthritis. Ann Rheum Dis. 1995;54:930-933.
47. Beltrami-Moreira M, Vromman A, Sukhova GK, Folco EJ, Libby P. Redundancy of IL-1 isoform signaling and its implications for arterial remodeling. PLoS One. 2016;11:e0152474. doi: 10.1371/journal. pone.0152474.
48. Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol. 2009;27:519-550. doi: 10.1146/annurev.immunol.021908.132612.
49. Chen CJ, Kono H, Golenbock D, Reed G, Akira S, Rock KL. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat Med. 2007;13:851-856. doi: 10.1038/nm1603.
50. Rider P, Carmi Y, Guttman O, Braiman A, Cohen I, Voronov E, White MR, Dinarello CA, Apte RN. IL-1α and IL-1β recruit different myeloid cells and promote different stages of sterile inflammation. J Immunol. 2011;187:4835-4843. doi: 10.4049/jimmunol.1102048.
51. Schönbeck U, Mach F, Libby P. Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J Immunol. 1998;161:3340-3346.
52. Afonina IS, Tynan GA, Logue SE, Cullen SP, Bots M, Lüthi AU, Reeves EP, McElvaney NG, Medema JP, Lavelle EC, Martin SJ. Granzyme B-dependent proteolysis acts as a switch to enhance the proinflammatory activity of IL-1α. Mol Cell. 2011;44:265-278. doi: 10.1016/j.molcel.2011.07.037.
53. Black RA, Kronheim SR, Cantrell M, Deeley MC, March CJ, Prickett KS, Wignall J, Conlon PJ, Cosman D, Hopp TP. Generation of biologically active interleukin-1 beta by proteolytic cleavage of the inactive precursor. J Biol Chem. 1988;263:9437-9442.
54. Clancy DM, Henry CM, Sullivan GP, Martin SJ. Neutrophil extracellular traps can serve as platforms for processing and activation of IL-1 family cytokines. FEBS J. 2017;284:1712-1725. doi: 10.1111/febs.14075.
55. Coeshott C, Ohnemus C, Pilyavskaya A, Ross S, Wieczorek M, Kroona H, Leimer AH, Cheronis J. Converting enzyme-independent release of tumor necrosis factor alpha and IL-1beta from a stimulated human monocytic cell line in the presence of activated neutrophils or purified proteinase 3. Proc Natl Acad Sci U S A. 1999;96:6261-6266.
56. Hazuda DJ, Strickler J, Kueppers F, Simon PL, Young PR. Processing of precursor interleukin 1 beta and inflammatory disease. J Biol Chem. 1990;265:6318-6322.
57. Li P, Allen H, Banerjee S, Franklin S, Herzog L, Johnston C, McDowell J, Paskind M, Rodman L, Salfeld J. Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell. 1995;80:401-411.
58. Kasperkiewicz P, Poreba M, Snipas SJ, Parker H, Winterbourn CC, Salvesen GS, Drag M. Design of ultrasensitive probes for human neutrophil elastase through hybrid combinatorial substrate library profiling. Proc Natl Acad Sci USA. 2014;111:2518-2523. doi: 10.1073/pnas.1318548111.
59. Toschi V, Gallo R, Lettino M, Fallon JT, Gertz SD, Fernández-Ortiz A, Chesebro JH, Badimon L, Nemerson Y, Fuster V, Badimon JJ. Tissue factor modulates the thrombogenicity of human atherosclerotic plaques. Circulation. 1997;95:594-599.
60. 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.
61. Noubouossie DF, Whelihan MF, Yu YB, Sparkenbaugh E, Pawlinski R, Monroe DM, Key NS. In vitro activation of coagulation by human neutrophil DNA and histone proteins but not neutrophil extracellular traps. Blood. 2017;129:1021-1029. doi: 10.1182/blood-2016-06-722298.
62. Chandran S, Watkins J, Abdul-Aziz A, Shafat M, Calvert PA, Bowles KM, Flather MD, Rushworth SA, Ryding AD. Inflammatory differences in plaque erosion and rupture in patients with ST-segment elevation myocardial infarction. J Am Heart Assoc. 2017;6:e005868.
63. Crea F, Libby P. Acute coronary syndromes: the way forward from mechanisms to precision treatment. Circulation. 2017;136:1155-1166. doi: 10.1161/CIRCULATIONAHA.117.029870.
64. Libby P. Superficial erosion and the precision management of acute coronary syndromes: not one-size-fits-all. Eur Heart J. 2017;38:801-803. doi: 10.1093/eurheartj/ehw599.