Neutrophil extracellular traps induce aggregation of washed human platelets independently of extracellular DNA and histones

Cell Communication and Signaling

Volumn 16, Issue 1, 2018, Pages

  Elaskalani, Omar ^a   Abdol Razak, Norbaini Binti ^a   Metharom, Pat ^a  

^a CURTIN UNIVERSITY   (Australia)

Author keywords

Aggregation; Cathepsin G; DNA; Histones; Neutrophil; Neutrophil extracellular traps; Platelet

Indexed keywords

ALPHA INTEGRIN; ALPHA2BBETA3 INTEGRIN; CATHEPSIN G; CELL DNA; DUAL SPECIFICITY PHOSPHATASE 2; HISTONE; LEUKOCYTE ELASTASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PADGEM PROTEIN; PROTEIN KINASE B; PROTEIN KINASE SYK; PURINERGIC P2Y12 RECEPTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; UNCLASSIFIED DRUG; DNA; FIBRINOGEN RECEPTOR; MPO PROTEIN, HUMAN; PEROXIDASE; SYK PROTEIN, HUMAN;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA HISTONE INTERACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR TRAP; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE RELEASE REACTION; UPREGULATION; CYTOLOGY; METABOLISM; NEUTROPHIL;

DNA; EXTRACELLULAR TRAPS; HISTONES; HUMANS; NADPH OXIDASE 1; NEUTROPHILS; PEROXIDASE; PLATELET ACTIVATION; PLATELET AGGREGATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; SYK KINASE;

EID: 85047729308     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/s12964-018-0235-0     Document Type: Article

References (60)

1. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13:159-75.
2. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. Neutrophil extracellular traps kill Bacteria. Science. 2004;303:1532-5.
3. McDonald B, Urrutia R, Yipp Bryan G, Jenne Craig N, Kubes P. Intravascular neutrophil extracellular traps capture Bacteria from the bloodstream during Sepsis. Cell Host Microbe. 2012;12:324-33.
4. Jorch SK, Kubes P. An emerging role for neutrophil extracellular traps in noninfectious disease. Nat Med. 2017;23:279-87.
5. Wong SL, Demers M, Martinod K, Gallant M, Wang YM, Goldfine AB, Kahn CR, Wagner DD. Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nat Med. 2015;21:815.
6. Hakkim A, Furnrohr BG, Amann K, Laube B, Abu Abed U, Brinkmann V, Herrmann M, Voll RE, Zychlinsky A. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci U S A. 2010;107:9813-8.
7. Gupta A, Hasler P, Gebhardt S, Holzgreve W, Hahn S. Occurrence of neutrophil extracellular DNA traps (NETs) in pre-eclampsia: a link with elevated levels of cell-free DNA? Ann N Y Acad Sci. 2006;1075:118-22.
8. Demers M, Krause DS, Schatzberg D, Martinod K, Voorhees JR, Fuchs TA, Scadden DT, Wagner DD. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proc Natl Acad Sci U S A. 2012;109:13076-81.
9. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD, Wrobleski SK, Wakefield TW, Hartwig JH, Wagner DD. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci U S A. 2010;107:15880-5.
10. Martinod K, Demers M, Fuchs TA, Wong SL, Brill A, Gallant M, Hu J, Wang Y, Wagner DD. Neutrophil histone modification by peptidylarginine deiminase 4 is critical for deep vein thrombosis in mice. Proc Natl Acad Sci. 2013;110:8674-9.
11. von Brühl M-L, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, Khandoga A, Tirniceriu A, Coletti R, Köllnberger 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.
12. Abdol Razak N, Elaskalani O, Metharom P. Pancreatic Cancer-induced neutrophil extracellular traps: a potential contributor to Cancer-associated thrombosis. Int J Mol Sci. 2017;18:1-18.
13. Leal AC, Mizurini DM, Gomes T, Rochael NC, Saraiva EM, Dias MS, Werneck CC, Sielski MS, Vicente CP, Monteiro RQ. Tumor-derived Exosomes induce the formation of neutrophil extracellular traps: implications for the establishment of Cancer-associated thrombosis. Sci Rep. 2017;7:6438.
14. McDonald B, Davis RP, Kim S-J, Tse M, Esmon CT, Kolaczkowska E, Jenne CN. Platelets and neutrophil extracellular traps collaborate to promote intravascular coagulation during sepsis in mice. Blood. 2017;129:1357-67.
15. Gould TJ, Vu TT, Swystun LL, Dwivedi DJ, Mai SHC, Weitz JI, Liaw PC. Neutrophil extracellular traps promote thrombin generation through platelet-dependent and platelet-independent mechanisms. Arterioscler Thromb Vasc Biol. 2014;34:1977-84.
16. Swystun LL, Mukherjee S, Liaw PC. Breast cancer chemotherapy induces the release of cell-free DNA, a novel procoagulant stimulus. J Thromb Haemost. 2011;9:2313-21.
17. 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;9:1795-803.
18. Semeraro F, Ammollo CT, Morrissey JH, Dale GL, Friese P, Esmon NL, Esmon CT. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood. 2011;118:1952-61.
19. Fuchs TA, Bhandari AA, Wagner DD. Histones induce rapid and profound thrombocytopenia in mice. Blood. 2011;118:3708-14.
20. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, Patel KD, Chakrabarti S, McAvoy E, Sinclair GD, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13:463.
21. Massberg S, Grahl L, von Bruehl M-L, Manukyan D, Pfeiler S, Goosmann C, Brinkmann V, Lorenz M, Bidzhekov K, Khandagale AB, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med. 2010;16:887-96.
22. Gorudko IV, Sokolov AV, Shamova EV, Grudinina NA, Drozd ES, Shishlo LM, Grigorieva DV, Bushuk SB, Bushuk BA, Chizhik SA, et al. Myeloperoxidase modulates human platelet aggregation via actin cytoskeleton reorganization and store-operated calcium entry. Biology Open. 2013;2:916-23.
23. Carrim N, Arthur JF, Hamilton JR, Gardiner EE, Andrews RK, Moran N, Berndt MC, Metharom P. Thrombin-induced reactive oxygen species generation in platelets: a novel role for protease-activated receptor 4 and GPIbalpha. Redox Biol. 2015;6:640-7.
24. Radomski M, Moncada S. An improved method for washing of human platelets with prostacyclin. Thromb Res. 1983;30:383-9.
25. Najmeh S, Cools-Lartigue J, Giannias B, Spicer J, Ferri LE. Simplified human neutrophil extracellular traps (NETs) isolation and handling. J Vis Exp. 2015:1-6.
26. 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;5:1-18.
27. Bennett JS. Structure and function of the platelet integrin alphaIIbbeta3. J Clin Invest. 2005;115:3363-9.
28. Zwaal RF, Schroit AJ. Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood. 1997;89:1121-32.
29. Alshehri OM, Montague S, Watson S, Carter P, Sarker N, Manne BK, Miller JL, Herr AB, Pollitt AY, O'Callaghan CA, et al. Activation of glycoprotein VI (GPVI) and C-type lectin-like receptor-2 (CLEC-2) underlies platelet activation by diesel exhaust particles and other charged/hydrophobic ligands. Biochem J. 2015;468:459-73.
30. 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;107:15880-5.
31. Jansen MP, Emal D, Teske GJ, Dessing MC, Florquin S, Roelofs JJ. Release of extracellular DNA influences renal ischemia reperfusion injury by platelet activation and formation of neutrophil extracellular traps. Kidney Int. 2017;91:352-64.
32. Pal PK, Starr T, Gertler MM. Neutralization of heparin by histone and its subfractions. Thromb Res. 1983;31:69-79.
33. Taylor L, Vasudevan SR, Jones CI, Gibbins JM, Churchill GC, Campbell RD, Coxon CH. Discovery of novel GPVI receptor antagonists by structure-based repurposing. PLoS One. 2014;9:e101209.
34. Jiang P, Loyau S, Tchitchinadze M, Ropers J, Jondeau G, Jandrot-Perrus M. Inhibition of glycoprotein VI clustering by collagen as a mechanism of inhibiting collagen-induced platelet responses: the example of losartan. PLoS One. 2015;10:1-20.
35. Elaskalani O, Khan I, Morici M, Matthysen C, Sabale M, Martins RN, Verdile G, Metharom P. Oligomeric and fibrillar amyloid beta 42 induce platelet aggregation partially through GPVI. Platelets. 2017;29:415-20.
36. Faraday N, Schunke K, Saleem S, Fu J, Wang B, Zhang J, Morrell C, Dore S. Cathepsin G-dependent modulation of platelet thrombus formation in vivo by blood neutrophils. PLoS One. 2013;8:e71447.
37. Kolarova H, Klinke A, Kremserova S, Adam M, Pekarova M, Baldus S, Eiserich JP, Kubala L. Myeloperoxidase induces the priming of platelets. Free Radic Biol Med. 2013;61:357-69.
38. Walsh TG, Berndt MC, Carrim N, Cowman J, Kenny D, Metharom P. The role of Nox1 and Nox2 in GPVI-dependent platelet activation and thrombus formation. Redox Biol. 2014;2:178-86.
39. Metharom P, Berndt MC, Baker RI, Andrews RK. Current state and novel approaches of antiplatelet therapy. Arterioscler Thromb Vasc Biol. 2015;35:1327-38.
40. Estensen RD, White JG. Ultrastructural features on the platelet response to phorbol myristate acetate. Am J Pathol. 1974;74:441-52.
41. Lu Q, Clemetson JM, Clemetson KJ. Translocation of GP1b and fc receptor gamma-chain to cytoskeleton in mucetin-activated platelets. J Thromb Haemost. 2005;3:2065-76.
42. Bevers EM, Comfurius P, Zwaal RF. Changes in membrane phospholipid distribution during platelet activation. Biochim Biophys Acta. 1983;736:57-66.
43. Rosing J, van Rijn JL, Bevers EM, van Dieijen G, Comfurius P, Zwaal RF. The role of activated human platelets in prothrombin and factor X activation. Blood. 1985;65:319-32.
44. Tonon G, Luo X, Greco NJ, Chen W, Shi Y, Jamieson GA. Weak platelet agonists and U46619 induce apoptosis-like events in platelets, in the absence of phosphatidylserine exposure. Thromb Res. 2002;107:345-50.
45. Carestia A, Rivadeneyra L, Romaniuk MA, Fondevila C, Negrotto S, Schattner M. Functional responses and molecular mechanisms involved in histone-mediated platelet activation. Thromb Haemost. 2013;110:1035-45.
46. Dorsch CA. Binding of single-strand DNA to human platelets. Thromb Res. 1981;24:119-29.
47. Fiedel BA, Schoenberger JS, Gewurz H. Modulation of platelet activation by native DNA. J Immunol. 1979;123:2479-83.
48. Fiedel BA, Frenzke ME. Modulation of platelet aggregation by native DNA - initial description of platelet receptor type, number and discrimination for native DNA. Thromb Haemost. 1981;45:263-6.
49. Noubouossie DF, Whelihan MF, Yu Y-B, 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;129:1021-9.
50. Sambrano GR, Huang W, Faruqi T, Mahrus S, Craik C, Coughlin SR. Cathepsin G activates protease-activated receptor-4 in human platelets. J Biol Chem. 2000;275:6819-23.
51. Korkmaz B, Horwitz MS, Jenne DE, Gauthier F. Neutrophil Elastase, proteinase 3, and Cathepsin G as therapeutic targets in human diseases. Pharmacol Rev. 2010;62:726-59.
52. Si-Tahar M, Pidard D, Balloy V, Moniatte M, Kieffer N, VanDorsselaer A, Chignard M. Human neutrophil elastase proteolytically activates the platelet integrin alpha(IIb)beta(3) through cleavage of the carboxyl terminus of the alpha(IIB) subunit heavy chain - involvement in the potentiation of platelet aggregation. J Biol Chem. 1997;272:11636-47.
53. Horn M, Bertling A, Brodde MF, Muller A, Roth J, Van Aken H, Jurk K, Heilmann C, Peters G, Kehrel BE. Human neutrophil alpha-defensins induce formation of fibrinogen and thrombospondin-1 amyloid-like structures and activate platelets via glycoprotein IIb/IIIa. J Thromb Haemost. 2012;10:647-61.
54. Fuentes E, Rojas A, Palomo I. Role of multiligand/RAGE axis in platelet activation. Throm Res. 2014;133:308-14.
55. Papayannopoulos V. Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol. 2018;18:134-47.
56. Carmona-Rivera C, Zhao WP, 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;74:1417-24.
57. Rajagopalan S, Somers EC, Brook RD, Kehrer C, Pfenninger D, Lewis E, Chakrabarti A, Richardson BC, Shelden E, McCune WJ, Kaplan MJ. Endothelial cell apoptosis in systemic lupus erythematosus: a common pathway for abnormal vascular function and thrombosis propensity. Blood. 2004;103:3677-83.
58. Dovizio M, Alberti S, Guillem-Llobat P, Patrignani P. Role of platelets in inflammation and Cancer: novel therapeutic strategies. Basic Clin Pharmacol Toxicol. 2014;114:118-27.
59. Brill A, Fuchs TA, Savchenko AS, Thomas GM, Martinod K, De Meyer SF, Bhandari AA, Wagner DD. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost. 2012;10:136-44.
60. Cedervall J, Zhang Y, Huang H, Zhang L, Femel J, Dimberg A, Olsson A-K. Neutrophil extracellular traps accumulate in peripheral blood vessels and compromise organ function in tumor-bearing animals. Cancer Res. 2015;75:2653-62.