Interferon lambda1/IL-29 and inorganic polyphosphate are novel regulators of neutrophil-driven thromboinflammation

Journal of Pathology

Volumn 243, Issue 1, 2017, Pages 111-122

  Chrysanthopoulou, Akrivi ^a   Kambas, Konstantinos ^a   Stakos, Dimitrios ^a   Mitroulis, Ioannis ^b   Mitsios, Alexandros ^a   Vidali, Veroniki ^c   Angelidou, Iliana ^a   Bochenek, Magdalena ^d   Arelaki, Stella ^e   Arampatzioglou, Athanasios ^a   Galani, Ioanna Evdokia ^f   Skendros, Panagiotis ^a,e   Couladouros, Elias A ^c,g   Konstantinides, Stavros ^a,d   Andreakos, Evangelos ^f   Schäfer, Katrin ^d   Ritis, Konstantinos ^a,e  

^a DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c Institute of Nanoscience and Nanotechnology   (Greece)

^d UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^e UNIVERSITY GENERAL HOSPITAL OF ALEXANDROUPOLIS   (Greece)

^f Biomedical Research Foundation   (Greece)

^g AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

Author keywords

acute coronary syndrome; autophagy; inorganic polyphosphate; interferon lambda; neutrophil extracellular traps

Indexed keywords

CHLORIDE; FERRIC CHLORIDE; FERRIC ION; IL28A PROTEIN, MOUSE; IL29 PROTEIN, HUMAN; INTERLEUKIN DERIVATIVE; MTOR PROTEIN, HUMAN; POLYPHOSPHATE; TARGET OF RAPAMYCIN KINASE; THROMBIN;

ANIMAL; AUTOPHAGY; BLOOD; BLOOD CLOTTING; C57BL MOUSE; CASE CONTROL STUDY; CHEMICALLY INDUCED; DIAGNOSTIC IMAGING; DISEASE MODEL; EXTRACELLULAR TRAP; HUMAN; INFLAMMATION; MALE; METABOLISM; NEUTROPHIL; SIGNAL TRANSDUCTION; ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOSIS;

ANIMALS; AUTOPHAGY; BLOOD COAGULATION; BLOOD PLATELETS; CASE-CONTROL STUDIES; CHLORIDES; DISEASE MODELS, ANIMAL; EXTRACELLULAR TRAPS; FERRIC COMPOUNDS; HUMANS; INFLAMMATION; INTERLEUKINS; MALE; MICE, INBRED C57BL; NEUTROPHILS; PLATELET ACTIVATION; POLYPHOSPHATES; SIGNAL TRANSDUCTION; ST ELEVATION MYOCARDIAL INFARCTION; THROMBIN; THROMBOSIS; TOR SERINE-THREONINE KINASES;

EID: 85027514457     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4935     Document Type: Article

References (57)

1. Raskob GE, Angchaisuksiri P, Blanco AN, et al. ISTH Steering Committee for World Thrombosis Day. Thrombosis: a major contributor to global disease burden. Arterioscler Thromb Vasc Biol 2014; 34: 2363–2371.
2. Bentzon JF, Otsuka F, Virmani R, et al. Mechanisms of plaque formation and rupture. Circ Res 2014; 114: 1852–1866.
3. Sabatine MS, Cannon CP, Gibson CM, et al. CLARITY-TIMI 28 Investigators. Addition of clopidogrel to aspirin and fibrinolytic therapy for myocardial infarction with ST-segment elevation. N Engl J Med 2005; 352: 1179–1189.
4. Chai-Adisaksopha C, Crowther M, Isayama T, et al. The impact of bleeding complications in patients receiving target-specific oral anticoagulants: a systematic review and meta-analysis. Blood 2014; 124: 2450–2458.
5. Fuchs TA, Brill A, Duerschmied D, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci U S A 2010; 107: 15880–15885.
6. 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.
7. Stakos DA, Kambas K, Konstantinidis T, et al. Expression of functional tissue factor by neutrophil extracellular traps in culprit artery of acute myocardial infarction. Eur Heart J 2015; 36: 1405–1414.
8. Khandpur R, Carmona-Rivera C, Vivekanandan-Giri A, et al. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci Transl Med 2013; 5: 178ra40.
9. Kambas K, Mitroulis I, Apostolidou E, et al. Autophagy mediates the delivery of thrombogenic tissue factor to neutrophil extracellular traps in human sepsis. PLoS One 2012; 7: e45427.
10. Chrysanthopoulou A, Mitroulis I, Apostolidou E, et al. Neutrophil extracellular traps promote differentiation and function of fibroblasts. J Pathol 2014; 233: 294–307.
11. Apostolidou E, Skendros P, Kambas K, et al. Neutrophil extracellular traps regulate IL-1β-mediated inflammation in familial Mediterranean fever. Ann Rheum Dis 2016; 75: 269–277.
12. Knight JS, Luo W, O'Dell AA, et al. Peptidylarginine deiminase inhibition reduces vascular damage and modulates innate immune responses in murine models of atherosclerosis. Circ Res 2014; 114: 947–956.
13. Swystun LL, Liaw PC. The role of leukocytes in thrombosis. Blood 2016, 128: 753–762.
14. Subramanian V, Knight JS, Parelkar S, et al. Design, synthesis, and biological evaluation of tetrazole analogs of Cl-amidine as protein arginine deiminase inhibitors. J Med Chem 2015; 58: 1337–1344.
15. Remijsen Q, Vanden Berghe T, Wirawan E, et al. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Res 2011; 21: 290–304.
16. Mitroulis I, Kambas K, Chrysanthopoulou A, et al. Neutrophil extracellular trap formation is associated with IL-1β and autophagy-related signaling in gout. PLoS One 2011; 6: e29318.
17. Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 2016; 12: 1–222.
18. Blazek K, Eames HL, Weiss M, et al. IFN-λ resolves inflammation via suppression of neutrophil infiltration and IL-1β production. J Exp Med 2015; 212: 845–853.
19. Muir AJ, Shiffman ML, Zaman A, et al. Phase 1b study of pegylated interferon lambda 1 with or without ribavirin in patients with chronic genotype 1 hepatitis C virus infection. Hepatology 2010; 52: 822–832.
20. Miller DM, Klucher KM, Freeman JA, et al. Interferon lambda as a potential new therapeutic for hepatitis C. Ann N Y Acad Sci 2009; 1182: 80–87.
21. Freeman J, Baglino S, Friborg J, et al. Pegylated interferons Lambda-1a and alfa-2a display different gene induction and cytokine and chemokine release profiles in whole blood, human hepatocytes and peripheral blood mononuclear cells. J Viral Hepat 2014; 21: e1–e9.
22. Galani IE, Triantafyllia V, Eleminiadou EE, et al. Interferon-λ mediates non-redundant front-line antiviral protection against influenza virus infection without compromising host fitness. Immunity 2017; 46: 875–890.
23. Kotenko SV, Gallagher G, Baurin VV, et al. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 2003; 4: 69–77.
24. Sheppard P, Kindsvogel W, Xu W, et al. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat Immunol 2003; 4: 63–68.
25. Mennechet FJ, Uzé G. Interferon-lambda-treated dendritic cells specifically induce proliferation of FOXP3-expressing suppressor T cells. Blood 2006; 107: 4417–4423.
26. Koltsida O, Hausding M, Stavropoulos A, et al. IL-28A (IFN-λ2) modulates lung DC function to promote Th1 immune skewing and suppress allergic airway disease. EMBO Mol Med 2011; 3: 348–361.
27. Brown MR, Kornberg A. Inorganic polyphosphate in the origin and survival of species. Proc Natl Acad Sci U S A 2004; 101: 16085–16087.
28. Müller F, Mutch NJ, Schenk WA, et al. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 2009; 139: 1143–1156.
29. Ruiz FA, Lea CR, Oldfield E, et al. Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes. J Biol Chem 2004; 279: 44250–44257.
30. Morrissey JH, Choi SH, Smith SA. Polyphosphate: an ancient molecule that links platelets, coagulation, and inflammation. Blood 2012; 119: 5972–5979.
31. Choi SH, Smith SA, Morrissey JH. Polyphosphate is a cofactor for the activation of factor XI by thrombin. Blood 2011; 118: 6963–6970.
32. Mutch NJ, Engel R, Uitte de Willige S, et al. Polyphosphate modifies the fibrin network and down-regulates fibrinolysis by attenuating binding of tPA and plasminogen to fibrin. Blood 2010; 115: 3980–3988.
33. Kehrel BE, Fender AC. Resolving thromboinflammation in the brain after ischemic stroke? Circulation 2016; 133: 2128–2131.
34. Ekdahl KN, Teramura Y, Hamad OA, et al. Dangerous liaisons: complement, coagulation, and kallikrein/kinin cross-talk act as a linchpin in the events leading to thromboinflammation. Immunol Rev 2016; 274: 245–269.
35. Massberg S, Grahl L, von Bruehl ML, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 2010; 16: 887–896.
36. Ferrante A, Thong YH. Optimal conditions for simultaneous purification of mononuclear and polymorphonuclear leucocytes from human blood by the Hypaque-Ficoll method. J Immunol Methods 1980; 36: 109–117.
37. Kessenbrock K, Krumbholz M, Schönermarck U, et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 2009; 15: 623–625.
38. Caudrillier A, Kessenbrock K, Gilliss BM, et al. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest 2012; 122: 2661–2671.
39. Moreno-Sanchez D, Hernandez-Ruiz L, Ruiz FA, et al. Polyphosphate is a novel pro-inflammatory regulator of mast cells and is located in acidocalcisomes. J Biol Chem 2012; 287: 28435–28444.
40. Gavillet M, Martinod K, Renella R, et al. Flow cytometric assay for direct quantification of neutrophil extracellular traps in blood samples. Am J Hematol 2015; 90: 1155–1158.
41. Saito K, Ohtomo R, Kuga-Uetake Y, et al. Direct labeling of polyphosphate at the ultrastructural level in Saccharomyces cerevisiae by using the affinity of the polyphosphate binding domain of Escherichia coli exopolyphosphatase. Appl Environ Microbiol 2005; 71: 5692–5701.
42. Angelova PR, Agrawalla BK, Elustondo PA, et al. In situ investigation of mammalian inorganic polyphosphate localization using novel selective fluorescent probes JC-D7 and JC-D8. ACS Chem Biol 2014; 9: 2101–2110.
43. Konstantinides S, Schäfer K, Thinnes T, et al. Plasminogen activator inhibitor-1 and its cofactor vitronectin stabilize arterial thrombi after vascular injury in mice. Circulation 2001; 103: 576–583.
44. Kilkenny C, Browne WJ, Cuthill IC, et al. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010; 8: e1000412.
45. Badimon L, Chesebro JH, Badimon JJ. Thrombus formation on ruptured atherosclerotic plaques and rethrombosis on evolving thrombi. Circulation 1992; 86(6 suppl): III74–85.
46. Shenoi RA, Kalathottukaren MT, Travers RJ, et al. Affinity-based design of a synthetic universal reversal agent for heparin anticoagulants. Sci Transl Med 2014; 6: 260ra150.
47. Travers RJ, Shenoi RA, Kalathottukaren MT, et al. Nontoxic polyphosphate inhibitors reduce thrombosis while sparing hemostasis. Blood 2014; 124: 3183–3190.
48. Smith SA, Choi SH, Collins JN, et al. Inhibition of polyphosphate as a novel strategy for preventing thrombosis and inflammation. Blood 2012; 120: 5103–5110.
49. 3-induced arterial thrombosis. J Thromb Haemost 2011; 9: 779–789.
50. 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.
51. Martinod K, Fuchs TA, Zitomersky NL, et al. PAD4-deficiency does not affect bacteremia in polymicrobial sepsis and ameliorates endotoxemic shock. Blood 2015; 125: 1948–1956.
52. Saffarzadeh M, Juenemann C, Queisser MA, et al. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS One 2012; 7: e32366.
53. Urban CF, Ermert D, Schmid M, et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009; 5: e1000639.
54. Kambas K, Markiewski MM, Pneumatikos IA, et al. C5a and TNF-alpha up-regulate the expression of tissue factor in intra-alveolar neutrophils of patients with the acute respiratory distress syndrome. J Immunol 2008; 180: 7368–7375.
55. Jimenez-Nuñez MD, Moreno-Sanchez D, Hernandez-Ruiz L, et al. Myeloma cells contain high levels of inorganic polyphosphate which is associated with nucleolar transcription. Haematologica 2012; 97: 1264–1271.
56. Chang Y-T, Wang, S. Combinatorial synthesis of benzimidazolium dyes and its diversity directed application toward GTP-selective fluorescent chemosensors. J Am Chem Soc 2006; 128: 10380–10381.
57. Mitroulis I, Kourtzelis I, Kambas K, et al. Regulation of the autophagic machinery in human neutrophils. Eur J Immunol 2010; 40: 1461–1472.