Neutrophil extracellular traps in ischemic stroke thrombi

Annals of Neurology

Volumn 82, Issue 2, 2017, Pages 223-232

  Laridan, Elodie ^a   Denorme, Frederik ^a   Desender, Linda ^a   François, Olivier ^b   Andersson, Tommy ^b,c   Deckmyn, Hans ^a   Vanhoorelbeke, Karen ^a   De Meyer, Simon F ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b AZ GROENINGE   (Belgium)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CEACAM8 PROTEIN, HUMAN; CELL ADHESION MOLECULE; DNA; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; LEUKOCYTE ANTIGEN; LEUKOCYTE ELASTASE;

ADOLESCENT; ADULT; AGED; BRAIN ISCHEMIA; CELL COUNT; CEREBROVASCULAR ACCIDENT; COMPLICATION; EXTRACELLULAR TRAP; FEMALE; HUMAN; MALE; METABOLISM; MIDDLE AGED; STATISTICS AND NUMERICAL DATA; THROMBOSIS; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD; BIOMARKERS; BRAIN ISCHEMIA; CELL ADHESION MOLECULES; CELL COUNT; DNA; EXTRACELLULAR TRAPS; FEMALE; GPI-LINKED PROTEINS; HUMANS; LEUKOCYTE ELASTASE; MALE; MIDDLE AGED; STROKE; THROMBOSIS; YOUNG ADULT;

EID: 85027845960     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.24993     Document Type: Article

References (38)

1. Prabhakaran S, Ruff I, Bernstein RA. Acute stroke intervention. JAMA 2015;313:1451.
2. Mozaffarian D, Benjamin EJ, Go AS, et al. Heart disease and stroke statistics–2015 update: a report from the American Heart Association. Circulation 2014;131:e29–e322.
3. Powers WJ, Derdeyn CP, Biller J, et al. 2015 American Heart Association/American Stroke Association focused update of the 2013 Guidelines for the Early Management of Patients with Acute Ischemic Stroke Regarding Endovascular Treatment. Stroke 2015;46:3020–3035.
4. Seners P, Turc G, Maïer B, et al. Incidence and predictors of early recanalization after intravenous thrombolysis. Stroke 2016;47:2409–2412.
5. Jang IK, Gold HK, Ziskind AA, et al. Differential sensitivity of erythrocyte-rich and platelet-rich arterial thrombi to lysis with recombinant tissue-type plasminogen activator. A possible explanation for resistance to coronary thrombolysis. Circulation 1989;79:920–928.
6. Simons N, Mitchell P, Dowling R, et al. Thrombus composition in acute ischemic stroke: a histopathological study of thrombus extracted by endovascular retrieval. J Neuroradiol 2015;42:86–92.
7. Niesten JM, van der Schaaf IC, van Dam L, et al. Histopathologic composition of cerebral thrombi of acute stroke patients is correlated with stroke subtype and thrombus attenuation. PLoS One 2014;9:e88882.
8. Ahn SH, Hong R, Choo IS, et al. Histologic features of acute thrombi retrieved from stroke patients during mechanical reperfusion therapy. Int J Stroke 2016;11:1036–1044.
9. Kim SK, Yoon W, Kim TS, et al. Histologic analysis of retrieved clots in acute ischemic stroke: correlation with stroke etiology and gradient-echo MRI. AJNR Am J Neuroradiol 2015;36:1756–1762.
10. Liebeskind DS, Sanossian N, Yong WH, et al. CT and MRI early vessel signs reflect clot composition in acute stroke. Stroke 2011;42:1237–1243.
11. Marder VJ, Chute DJ, Starkman S, et al. Analysis of thrombi retrieved from cerebral arteries of patients with acute ischemic stroke. Stroke 2006;37:2086–2093.
12. Schuhmann MK, Gunreben I, Kleinschnitz C, Kraft P. Immunohistochemical analysis of cerebral thrombi retrieved by mechanical thrombectomy from patients with acute ischemic stroke. Int J Mol Sci 2016;17:298.
13. Denorme F, Langhauser F, Desender L, et al. ADAMTS13-mediated thrombolysis of t-PA-resistant occlusions in ischemic stroke in mice. Blood 2016;127:2337–2345.
14. Martinod K, Wagner DD. Thrombosis: tangled up in NETs. Blood 2014;123:2768–2776.
15. Fuchs TA, Brill A, Duerschmied D, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci U S A 2010;107:15880–15885.
16. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004;303:1532–1535.
17. Massberg S, Grahl L, von Bruehl M-L, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 2010;16:887–896.
18. Adams HP, Bendixen BH, Kappelle LJ, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke 1993;24:35–41.
19. Kramer MCA, van der Wal AC, Koch KT, et al. Presence of older thrombus is an independent predictor of long-term mortality in patients with ST-elevation myocardial infarction treated with thrombus aspiration during primary percutaneous coronary intervention. Circulation 2008;118:1810–1816.
20. Rittersma SZH, van der Wal AC, Koch KT, et al. Plaque instability frequently occurs days or weeks before occlusive coronary thrombosis: a pathological thrombectomy study in primary percutaneous coronary intervention. Circulation 2005;111:1160–1165.
21. Kimura K, Iguchi Y, Shibazaki K, et al. Early stroke treatment with IV t-PA associated with early recanalization. J Neurol Sci 2010;295:53–57.
22. Boeckh-Behrens T, Schubert M, Förschler A, et al. The impact of histological clot composition in embolic stroke. Clin Neuroradiol 2016;26:189–197.
23. Boeckh-Behrens T, Kleine JF, Zimmer C, et al. Thrombus histology suggests cardioembolic cause in cryptogenic stroke. Stroke 2016;47:1864–1871.
24. Fuijkschot WW, Groothuizen WE, Appelman Y, et al. Inflammatory cell content of coronary thrombi is dependent on thrombus age in patients with ST-elevation myocardial infarction. J Cardiol 2017;69:394–400.
25. Riegger J, Byrne RA, Joner M, et al. Histopathological evaluation of thrombus in patients presenting with stent thrombosis. Eur Heart J 2016;37:1538–1549.
26. Darbousset R, Thomas GM, Mezouar S, et al. Tissue factor-positive neutrophils bind to injured endothelial wall and initiate thrombus formation. Blood 2012;120:2133–2143.
27. von Brühl M-L, 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.
28. Grässle S, Huck V, Pappelbaum KI, et al. von Willebrand factor directly interacts with DNA from neutrophil extracellular traps. Arterioscler Thromb Vasc Biol 2014;34:1382–1389.
29. Fuchs TA, Brill A, Wagner DD. Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscler Thromb Vasc Biol 2012;32:1777–1783.
30. Mangold A, Alias S, Scherz T, et al. 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.
31. de Boer OJ, Li X, Goebel H, van der Wal AC. Nuclear smears observed in H&E-stained thrombus sections are neutrophil extracellular traps. J Clin Pathol 2016;69:181–182.
32. 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;109:290–297.
33. Delbosc S, Alsac J-M, Journe C, et al. Porphyromonas gingivalis participates in pathogenesis of human abdominal aortic aneurysm by neutrophil activation. Proof of concept in rats. PLoS One 2011;6:e18679.
34. Oklu R, Albadawi H, Watkins MT, et al. 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.
35. Nakazawa D, Tomaru U, Yamamoto C, et al. Abundant neutrophil extracellular traps in thrombus of patient with microscopic polyangiitis. Front Immunol 2012;3:333.
36. Savchenko AS, Martinod K, Seidman MA, et al. Neutrophil extracellular traps form predominantly during the organizing stage of human venous thromboembolism development. J Thromb Haemost 2014;12:860–870.
37. Longstaff C, Varjú I, Sótonyi P, et al. Mechanical stability and fibrinolytic resistance of clots containing fibrin, DNA, and histones. J Biol Chem 2013;288:6946–6956.
38. De Meyer SF, Suidan GL, Fuchs TA, et al. Extracellular chromatin is an important mediator of ischemic stroke in mice. Arterioscler Thromb Vasc Biol 2012;32:1884–1891.