The role of reactive oxygen species (ROS) in the formation of extracellular traps (ETs) in humans

Biomolecules

Volumn 5, Issue 2, 2015, Pages 702-723

  Stoiber, Walter ^a   Obermayer, Astrid ^a   Steinbacher, Peter ^a   Krautgartner, Wolf Dietrich ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

Author keywords

Autophagy; Inflammation; MAPK ERK; NADPH oxidase; NETs; Neutrophils

Indexed keywords

REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

CYTOKINESIS; EXTRACELLULAR MATRIX; EXTRACELLULAR TRAP; HUMAN; INFLAMMATION; NEUTROPHIL CHEMOTAXIS; PATHOGENESIS; PHAGOCYTOSIS; REVIEW; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; AUTOPHAGY; METABOLISM; NEUTROPHIL; ULTRASTRUCTURE;

VERTEBRATA;

AUTOPHAGY; EXTRACELLULAR TRAPS; HUMANS; MAP KINASE SIGNALING SYSTEM; NADPH OXIDASE; NEUTROPHILS; REACTIVE OXYGEN SPECIES;

EID: 85012082556     PISSN: None     EISSN: 2218273X     Source Type: Journal    
DOI: 10.3390/biom5020702     Document Type: Review

References (138)

1. Von Kockritz-Blickwede, M.; Nizet, V. Innate immunity turned inside-out: Antimicrobial defense by phagocyte extracellular traps. J. Mol. Med. 2009, 87, 775-783.
2. Remijsen, Q.; Kuijpers, T.; Wirawan, E.; Lippens, S.; Vandenabeele, P.; Berghe, T.V. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ. 2011, 18, 581-588.
3. Guimaraes-Costa, A.B.; Nascimento, M.T.C.; Wardini, A.B.; Pinto-da-Silva, L.H.; Saraiva, E.M. ETosis: A microbicidal mechanism beyond Cell Death. J. Parasitol. Res. 2012, doi:10.1155/2012/929743.
4. Goldmann, O.; Medina, E. The expanding world of extracellular traps: Not only neutrophils but much more. Front. Immunol. 2013, doi:10.3389/fimmu.2012.00420.
5. Brinkmann, V.; Reichard, U.; Goosmann, C.; Fauler, B.; Uhlemann, Y.; Weiss, D.S.; Weinrauch, Y.; Zychlinsky, A. Neutrophil extracellular traps kill bacteria. Science 2004, 303, 1532-1535.
6. Chuammitri, P.; Ostojić, J.; Andreasen, C.B.; Redmond, S.B.; Lamont, S.J.; Palić, D. Chicken heterophil extracellular traps (HETs): Novel defense mechanism of chicken heterophils. Vet. Immunol. Immunopathol. 2009, 129, 126-131.
7. Palić, D.; Ostojić, J.; Andreasen, C.B.; Roth, J.A. Fish cast NETs: Neutrophil extracellular traps are released from fish neutrophils. Dev. Comp. Immunol. 2007, 31, 805-816.
8. Pijanowski, L.; Golbach, L.; Kolaczkowska, E.; Scheer, M.; Verburg-van Kemenade, B.M.L.; Chadzinska, M. Carp neutrophilic granulocytes form extracellular traps via ROS-dependent and independent pathways. Fish Shellfish Immunol. 2013, 34, 1244-1252.
9. Obermayer, A.; Stoiber, W.; Krautgartner, W.-D.; Klappacher, M.; Kofler, B.; Steinbacher, P.; Vitkov, L.; Grabcanovic-Musija, F.; Studnicka, M. New aspects on the structure of neutrophil extracellular traps from chronic obstructive pulmonary disease and in vitro generation. PLOS ONE 2014, 9, e97784.
10. Parseghian, M.H.; Luhrs, K.A. Beyond the walls of the nucleus: The role of histones in cellular signaling and innate immunity. Biochem. Cell Biol. 2006, 84, 589-604.
11. Brinkmann, V.; Zychlinsky, A. Beneficial suicide: Why neutrophils die to make NETs. Nat. Rev. Microbiol. 2007, 5, 577-582.
12. Urban, C.F.; Ermert, D.; Schmid, M.; Abu-Abed, U.; Goosmann, C.; Nacken, W.; Brinkmann, V.; Jungblut, P.R.; Zychlinsky, A. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLOS Pathog. 2009, 5, e1000639.
13. Papayannopoulos, V.; Metzler, K.D.; Hakkim, A.; Zychlinsky, A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 2010, 191, 677-691.
14. Reeves, E.P.; Lu, H.; Jacobs, H.L.; Messina, C.G.M.; Bolsover, S.; Gabella, G.; Potma, E.O.; Warley, A.; Roes, J.; Segal, A.W. Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 2002, 416, 291-297.
15. Ermert, D.; Zychlinsky, A.; Urban, C. Fungal and bacterial killing by neutrophils. Methods Mol. Biol. 2009, 470, 293-312.
16. Guimaraes-Costa, A.B.; Nascimento, M.T.C.; Froment, G.S.; Soares, R.P.P.; Morgado, F.N.; Conceicao-Silva, F.; Saraiva, E.M. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc. Natl. Acad. Sci. USA 2009, 106, 6748-6753.
17. Bonne-Annee, S.; Kerepesi, L.A.; Hess, J.A.; Wesolowski, J.; Paumet, F.; Lok, J.B.; Nolan, T.J.; Abraham, D. Extracellular traps are associated with human and mouse neutrophil and macrophage mediated killing of larval Strongyloides stercoralis. Microbes Infect. Inst. Pasteur 2014, 16, 502-511.
18. Rohm, M.; Grimm, M.J.; D'Auria, A.C.; Almyroudis, N.G.; Segal, B.H.; Urban, C.F. NADPH oxidase promotes neutrophil extracellular trap formation in pulmonary aspergillosis. Infect. Immun. 2014, 82, 1766-1777.
19. Galioto, A.M.; Hess, J.A.; Nolan, T.J.; Schad, G.A.; Lee, J.J.; Abraham, D. Role of eosinophils and neutrophils in innate and adaptive protective immunity to larval strongyloides stercoralis in mice. Infect. Immun. 2006, 74, 5730-5738.
20. Narasaraju, T.; Yang, E.; Samy, R.P.; Ng, H.H.; Poh, W.P.; Liew, A.-A.; Phoon, M.C.; Rooijen, N.; van; Chow, V.T. Excessive neutrophils and neutrophil extracellular traps contribute to acute lung injury of influenza pneumonitis. Am. J. Pathol. 2011, 179, 199-210.
21. Jenne, C.N.; Wong, C.H.Y.; Zemp, F.J.; McDonald, B.; Rahman, M.M.; Forsyth, P.A.; McFadden, G.; Kubes, P. Neutrophils recruited to sites of infection protect from virus challenge by releasing neutrophil extracellular traps. Cell Host Microbe 2013, 13, 169-180.
22. Marcos, V.; Zhou-Suckow, Z.; Yildirim, A.O.; Bohla, A.; Hector, A.; Vitkov, L.; Krautgartner, W.D.; Stoiber, W.; Griese, M.; Eickelberg, O.; et al. Free DNA in cystic fibrosis airway fluids correlates with airflow obstruction. Mediators Inflamm. 2015, doi:10.1155/2015/408935.
23. Sangaletti, S.; Tripodo, C.; Chiodoni, C.; Guarnotta, C.; Cappetti, B.; Casalini, P.; Piconese, S.; Parenza, M.; Guiducci, C.; Vitali, C.; et al. Neutrophil extracellular traps mediate transfer of cytoplasmic neutrophil antigens to myeloid dendritic cells toward ANCA induction and associated autoimmunity. Blood 2012, 120, 3007-3018.
24. Khandpur, R.; Carmona-Rivera, C.; Vivekanandan-Giri, A.; Gizinski, A.; Yalavarthi, S.; Knight, J.S.; Friday, S.; Li, S.; Patel, R.M.; Subramanian, V.; et al. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci. Transl. Med. 2013, doi:10.1126/scitranslmed.3005580.
25. Kaplan, M.J.; Radic, M. Neutrophil extracellular traps: Double-edged swords of innate immunity. J. Immunol. 2012, 189, 2689-2695.
26. Keshari, R.S.; Jyoti, A.; Dubey, M.; Kothari, N.; Kohli, M.; Bogra, J.; Barthwal, M.K.; Dikshit, M. Cytokines induced neutrophil extracellular traps formation: Implication for the inflammatory disease condition. PLOS ONE 2012, 7, e48111.
27. Gupta, A.K.; Hasler, P.; Holzgreve, W.; Gebhardt, S.; Hahn, S. Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Hum. Immunol. 2005, 66, 1146-1154.
28. Aleyd, E.; van Hout, M.W.M.; Ganzevles, S.H.; Hoeben, K.A.; Everts, V.; Bakema, J.E.; van Egmond, M. IgA enhances NETosis and release of neutrophil extracellular traps by polymorphonuclear cells via Fcα receptor I. J. Immunol. 2014, 192, 2374-2383.
29. Behnen, M.; Leschczyk, C.; Moller, S.; Batel, T.; Klinger, M.; Solbach, W.; Laskay, T. Immobilized immune complexes induce neutrophil extracellular trap release by human neutrophil granulocytes via FcαRIIIB and Mac-1. J. Immunol. 2014, 193, 1954-1965.
30. Yousefi, S.; Mihalache, C.; Kozlowski, E.; Schmid, I.; Simon, H.U. Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ. 2009, 16, 1438-1444.
31. Pilsczek, F.H.; Salina, D.; Poon, K.K.H.; Fahey, C.; Yipp, B.G.; Sibley, C.D.; Robbins, S.M.; Green, F.H.Y.; Surette, M.G.; Sugai, M.; et al. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J. Immunol. 2010, 185, 7413-7426.
32. Fuchs, T.A.; 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.
33. Yipp, B.G.; Petri, B.; Salina, D.; Jenne, C.N.; Scott, B.N.V.; Zbytnuik, L.D.; Pittman, K.; Asaduzzaman, M.; Wu, K.; Meijndert, H.C.; et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat. Med. 2012, 18, 1386-1393.
34. Boyum, A. Separation of leukocytes from blood and bone marrow. Introduction. Scand. J. Clin. Lab. Invest. 1968, 97, 7.
35. Brinkmann, V.; Laube, B.; Abed, U.A.; Goosmann, C.; Zychlinsky, A. Neutrophil extracellular traps: How to generate and visualize them. J. Vis. Exp. 2010, 36, 1724-1727.
36. Anzilotti, C.; Pratesi, F.; Tommasi, C.; Migliorini, P. Peptidylarginine deiminase 4 and citrullination in health and disease. Autoimmun. Rev. 2010, 9, 158-160.
37. Neeli, I.; Khan, S.N.; Radic, M. Histone deimination as a response to inflammatory stimuli in neutrophils. J. Immunol. 2008, 180, 1895-1902.
38. Thannickal, V.J.; Fanburg, B.L. Reactive oxygen species in cell signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 2000, 279, L1005-1028.
39. Holmstrom, K.M.; Finkel, T. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat. Rev. Mol. Cell Biol. 2014, 15, 411-421.
40. Bedard, K.; Krause, K.-H. The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology. Physiol. Rev. 2007, 87, 245-313.
41. Kirchner, T.; Moller, S.; Klinger, M.; Solbach, W.; Laskay, T.; Behnen, M. The impact of various reactive oxygen species on the formation of neutrophil extracellular traps. Mediators Inflamm. 2012, doi:10.1155/2012/849136. s
42. Arazna, M.; Pruchniak, M.P.; Demkow, U. Neutrophil extracellular traps in bacterial infections: Strategies for escaping from killing. Respir. Physiol. Neurobiol. 2013, 187, 74-77.
43. Mitroulis, I.; Kambas, K.; Chrysanthopoulou, A.; Skendros, P.; Apostolidou, E.; Kourtzelis, I.; Drosos, G.I.; Boumpas, D.T.; Ritis, K. Neutrophil extracellular trap formation is associated with IL-1β and autophagy-related signaling in gout. PLOS ONE 2011, 6, e29318.
44. Remijsen, Q.; Berghe, T.V.; Wirawan, E.; Asselbergh, B.; Parthoens, E.; de Rycke, R.; Noppen, S.; Delforge, M.; Willems, J.; Vandenabeele, P. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Res. 2011, 21, 290-304.
45. Deter, R.L.; Baudhuin, P.; de Duve, C. Participation of lysosomes in cellular autophagy induced in rat liver by glucagon. J. Cell Biol. 1967, 35, C11-C16.
46. Eskelinen, E.-L. New insights into the mechanisms of macroautophagy in mammalian cells. Int. Rev. Cell Mol. Biol. 2008, 266, 207-247.
47. Kroemer, G.; Marino, G.; Levine, B. Autophagy and the integrated stress response. Mol. Cell 2010, 40, 280-293.
48. Levine, B.; Abrams, J. p53: The Janus of autophagy? Nat. Cell Biol. 2008, 10, 637-639.
49. Bowman, C.J.; Ayer, D.E.; Dynlacht, B.D. Foxk proteins repress the initiation of starvation-induced atrophy and autophagy programs. Nat. Cell Biol. 2014, 16, 1202-1214.
50. Leidal, A.M.; Debnath, J. "Doubling down" on the autophagy pathway to suppress tumor growth. Genes Dev. 2014, 28, 1137-1139.
51. Gozuacik, D.; Kimchi, A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 2004, 23, 2891-2906.
52. Kondo, Y.; Kanzawa, T.; Sawaya, R.; Kondo, S. The role of autophagy in cancer development and response to therapy. Nat. Rev. Cancer 2005, 5, 726-734.
53. Liang, N.; Zhang, C.; Dill, P.; Panasyuk, G.; Pion, D.; Koka, V.; Gallazzini, M.; Olson, E.N.; Lam, H.; Henske, E.P.; et al. Regulation of YAP by mTOR and autophagy reveals a therapeutic target of tuberous sclerosis complex. J. Exp. Med. 2014, 211, 2249-2263.
54. Ogier-Denis, E.; Pattingre, S.; El Benna, J.; Codogno, P. Erk1/2-dependent phosphorylation of Galpha-interacting protein stimulates its GTPase accelerating activity and autophagy in human colon cancer cells. J. Biol. Chem. 2000, 275, 39090-39095.
55. Liu, Y.L.; Lai, F.; Wilmott, J.S.; Yan, X.G.; Liu, X.Y.; Luan, Q.; Guo, S.T.; Jiang, C.C.; Tseng, H.-Y.; Scolyer, R.A.; et al. Noxa upregulation by oncogenic activation of MEK/ERK through CREB promotes autophagy in human melanoma cells. Oncotarget 2014, 5, 11237-11251.
56. Mitroulis, I.; Kourtzelis, I.; Kambas, K.; Rafail, S.; Chrysanthopoulou, A.; Speletas, M.; Ritis, K. Regulation of the autophagic machinery in human neutrophils. Eur. J. Immunol. 2010, 40, 1461-1472.
57. Scherz-Shouval, R.; Elazar, Z. Regulation of autophagy by ROS: Physiology and pathology. Trends Biochem. Sci. 2011, 36, 30-38.
58. Chargui, A.; Cesaro, A.; Mimouna, S.; Fareh, M.; Brest, P.; Naquet, P.; Darfeuille-Michaud, A.; Hebuterne, X.; Mograbi, B.; Vouret-Craviari, V.; et al. Subversion of autophagy in adherent invasive Escherichia coli-infected neutrophils induces inflammation and cell death. PLOS ONE 2012, 7, e51727.
59. Chargui, A.; El May, M.V. Autophagy mediates neutrophil responses to bacterial infection. Acta Pathol. Microbiol. Immunol. Scand. 2014, 122, 1047-1058.
60. Kroemer, G.; Levine, B. Autophagic cell death: The story of a misnomer. Nat. Rev. Mol. Cell Biol. 2008, 9, 1004-1010.
61. Drummond, G.R.; Selemidis, S.; Griendling, K.K.; Sobey, C.G. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat. Rev. Drug Discov. 2011, 10, 453-471.
62. Gao, H.-M.; Zhou, H.; Hong, J.-S. NADPH oxidases: Novel therapeutic targets for neurodegenerative diseases. Trends Pharmacol. Sci. 2012, 33, 295-303.
63. Chen, K.; Kirber, M.T.; Xiao, H.; Yang, Y.; Keaney, J.F. Regulation of ROS signal transduction by NADPH oxidase 4 localization. J. Cell Biol. 2008, 181, 1129-1139.
64. Rabelo, L.A.; de Souza, V.N.; da Fonseca, L.J.S.; Sampaio, W.O. Redox unbalance: NADPH oxidase as therapeutic target in blood pressure control. Arq. Bras. Cardiol. 2010, 94, 684-693.
65. El-Benna, J.; Dang, P.M.-C.; Gougerot-Pocidalo, M.-A. Priming of the neutrophil NADPH oxidase activation: Role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin. Immunopathol. 2008, 30, 279-289.
66. Sheppard, F.R.; Kelher, M.R.; Moore, E.E.; McLaughlin, N.J.D.; Banerjee, A.; Silliman, C.C. Structural organization of the neutrophil NADPH oxidase: Phosphorylation and translocation during priming and activation. J. Leukoc. Biol. 2005, 78, 1025-1042.
67. Dang, P.M.-C.; Stensballe, A.; Boussetta, T.; Raad, H.; Dewas, C.; Kroviarski, Y.; Hayem, G.; Jensen, O.N.; Gougerot-Pocidalo, M.-A.; El-Benna, J. A specific p47phox-serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites. J. Clin. Invest. 2006, 116, 2033-2043.
68. El-Benna, J.; Dang, P.M.-C.; Gougerot-Pocidalo, M.A.; Marie, J.C.; Braut-Boucher, F. p47phox, the phagocyte NADPH oxidase/NOX2 organizer: Structure, phosphorylation and implication in diseases. Exp. Mol. Med. 2009, 41, 217-225.
69. Wittmann, S.; Frohlich, D.; Daniels, S. Characterization of the human fMLP receptor in neutrophils and in Xenopus oocytes. Br. J. Pharmacol. 2002, 135, 1375-1382.
70. Kuiper, J.W.P.; Sun, C.; Magalhaes, M.A.O.; Glogauer, M. Rac regulates PtdInsP3 signaling and the chemotactic compass through a redox-mediated feedback loop. Blood 2011, 118, 6164-6171.
71. Karlsson, A.; Nixon, J.B.; McPhail, L.C. Phorbol myristate acetate induces neutrophil NADPH-oxidase activity by two separate signal transduction pathways: Dependent or independent of phosphatidylinositol 3-kinase. J. Leukoc. Biol. 2000, 67, 396-404.
72. Wang, Y.-H.; Shen, Y.-C.; Liao, J.-F.; Lee, C.-H.; Li, C.-H.; Chou, C.-Y.; Liou, K.-T.; Chou, Y.-C. Anti-inflammatory effects of dimemorfan on inflammatory cells and LPS-induced endotoxin shock in mice. Br. J. Pharmacol. 2008, 154, 1327-1338.
73. Klebanoff, S.J. Myeloperoxidase: Friend and foe. J. Leukoc. Biol. 2005, 77, 598-625.
74. Nishinaka, Y.; Arai, T.; Adachi, S.; Takaori-Kondo, A.; Yamashita, K. Singlet oxygen is essential for neutrophil extracellular trap formation. Biochem. Biophys. Res. Commun. 2011, 413, 75-79.
75. Klebanoff, S.J.; Kettle, A.J.; Rosen, H.; Winterbourn, C.C.; Nauseef, W.M. Myeloperoxidase: A front-line defender against phagocytosed microorganisms. J. Leukoc. Biol. 2013, 93, 185-198.
76. Miyamoto, S.; Martinez, G.R.; Rettori, D.; Augusto, O.; Medeiros, M.H.G.; di Mascio, P. Linoleic acid hydroperoxide reacts with hypochlorous acid, generating peroxyl radical intermediates and singlet molecular oxygen. Proc. Natl. Acad. Sci. USA 2006, 103, 293-298.
77. Garcia-Bonilla, L.; Moore, J.M.; Racchumi, G.; Zhou, P.; Butler, J.M.; Iadecola, C.; Anrather, J. Inducible Nitric Oxide Synthase in Neutrophils and Endothelium Contributes to Ischemic Brain Injury in Mice. J. Immunol. 2014, 193, 2531-2537.
78. Forman, H.J.; Torres, M. Reactive oxygen species and cell signaling: Respiratory burst in macrophage signaling. Am. J. Respir. Crit. Care Med. 2002, 166, S4-S8.
79. Rybicka, J.M.; Balce, D.R.; Khan, M.F.; Krohn, R.M.; Yates, R.M. NADPH oxidase activity controls phagosomal proteolysis in macrophages through modulation of the lumenal redox environment of phagosomes. Proc. Natl. Acad. Sci. USA 2010, 107, 10496-10501.
80. Moriguchi, K.; Ohno, N. Electron microscopic identification of hydrogen peroxide detected in fixed human polymorphonuclear leukocytes during phagocytosis. Okajimas Folia Anat. Jpn. 2014, 90, 97-100.
81. Pham, C.T.N. Neutrophil serine proteases: Specific regulators of inflammation. Nat. Rev. Immunol. 2006, 6, 541-550.
82. Nauseef, W.M. How human neutrophils kill and degrade microbes: An integrated view. Immunol. Rev. 2007, 219, 88-102.
83. Sorensen, O.E.; Clemmensen, S.N.; Dahl, S.L.; Ostergaard, O.; Heegaard, N.H.; Glenthoj, A.; Nielsen, F.C.; Borregaard, N. Papillon-Lefevre syndrome patient reveals species-dependent requirements for neutrophil defenses. J. Clin. Invest. 2014, 124, 4539-4548.
84. Keshari, R.S.; Verma, A.; Barthwal, M.K.; Dikshit, M. Reactive oxygen species-induced activation of ERK and p38 MAPK mediates PMA-induced NETs release from human neutrophils. J. Cell. Biochem. 2013, 114, 532-540.
85. Bianchi, M.; Hakkim, A.; Brinkmann, V.; Siler, U.; Seger, R.A.; Zychlinsky, A.; Reichenbach, J. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 2009, 114, 2619-2622.
86. Bianchi, M.; Niemiec, M.J.; Siler, U.; Urban, C.F.; Reichenbach, J. Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin-dependent. J. Allergy Clin. Immunol. 2011, 127, 1243-1252.
87. Papayannopoulos, V.; Staab, D.; Zychlinsky, A. Neutrophil elastase enhances sputum solubilization in cystic fibrosis patients receiving DNase therapy. PLOS ONE 2011, 6, e28526.
88. Branzk, N.; Papayannopoulos, V. Molecular mechanisms regulating NETosis in infection and disease. Semin. Immunopathol. 2013, 35, 513-530.
89. Kawakami, T.; He, J.; Morita, H.; Yokoyama, K.; Kaji, H.; Tanaka, C.; Suemori, S.; Tohyama, K.; Tohyama, Y. Rab27a is essential for the formation of neutrophil extracellular traps (NETs) in neutrophil-like differentiated HL60 cells. PLOS ONE 2014, 9, e84704.
90. Gupta, A.K.; Giaglis, S.; Hasler, P.; Hahn, S. Efficient neutrophil extracellular trap induction requires mobilization of both intracellular and extracellular calcium pools and is modulated by cyclosporine A. PLOS ONE 2014, 9, e97088.
91. Parker, H.; Dragunow, M.; Hampton, M.B.; Kettle, A.J.; Winterbourn, C.C. Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus. J. Leukoc. Biol. 2012, 92, 841-849.
92. Metzler, K.D.; Fuchs, T.A.; Nauseef, W.M.; Reumaux, D.; Roesler, J.; Schulze, I.; Wahn, V.; Papayannopoulos, V.; Zychlinsky, A. Myeloperoxidase is required for neutrophil extracellular trap formation: Implications for innate immunity. Blood 2011, 117, 953-959.
93. Conus, S.; Perozzo, R.; Reinheckel, T.; Peters, C.; Scapozza, L.; Yousefi, S.; Simon, H.-U. Caspase-8 is activated by cathepsin D initiating neutrophil apoptosis during the resolution of inflammation. J. Exp. Med. 2008, 205, 685-698.
94. Lopes, F.; Coelho, F.M.; Costa, V.V.; Vieira, E.L.M.; Sousa, L.P.; Silva, T.A.; Vieira, L.Q.; Teixeira, M.M.; Pinho, V. Resolution of neutrophilic inflammation by H2O2 in antigen-induced arthritis. Arthritis Rheum. 2011, 63, 2651-2660.
95. Geering, B.; Simon, H.-U. Peculiarities of cell death mechanisms in neutrophils. Cell Death Differ. 2011, 18, 1457-1469.
96. Kunisaki, Y.; Nishikimi, A.; Tanaka, Y.; Takii, R.; Noda, M.; Inayoshi, A.; Watanabe, K.; Sanematsu, F.; Sasazuki, T.; Sasaki, T.; et al. DOCK2 is a Rac activator that regulates motility and polarity during neutrophil chemotaxis. J. Cell Biol. 2006, 174, 647-652.
97. Watanabe, M.; Terasawa, M.; Miyano, K.; Yanagihara, T.; Uruno, T.; Sanematsu, F.; Nishikimi, A.; Cote, J.-F.; Sumimoto, H.; Fukui, Y. DOCK2 and DOCK5 act additively in neutrophils to regulate chemotaxis, superoxide production, and extracellular trap formation. J. Immunol. 2014, 193, 5660-5667.
98. Hasan, R.; Rink, L.; Haase, H. Zinc signals in neutrophil granulocytes are required for the formation of neutrophil extracellular traps. Innate Immun. 2013, 19, 253-264.
99. Itakura, A.; McCarty, O.J.T. Pivotal role for the mTOR pathway in the formation of neutrophil extracellular traps via regulation of autophagy. Am. J. Physiol. Cell Physiol. 2013, 305, C348-C354.
100. Tang, B.; Cai, J.; Sun, L.; Li, Y.; Qu, J.; Snider, B.J.; Wu, S. Proteasome inhibitors activate autophagy involving inhibition of PI3K-Akt-mTOR pathway as an anti-oxidation defense in human RPE cells. PLOS ONE 2014, 9, e103364.
101. Wang, C.; Zhang, X.; Teng, Z.; Zhang, T.; Li, Y. Downregulation of PI3K/Akt/mTOR signaling pathway in curcumin-induced autophagy in APP/PS1 double transgenic mice. Eur. J. Pharmacol. 2014, 740, 312-320.
102. Eom, J.-M.; Seo, M.-J.; Baek, J.-Y.; Chu, H.; Han, S.H.; Min, T.S.; Cho, C.; Yun, C.-H. Alpha-eleostearic acid induces autophagy-dependent cell death through targeting AKT/mTOR and ERK1/2 signal together with the generation of reactive oxygen species. Biochem. Biophys. Res. Commun. 2010, 391, 903-908.
103. Zhang, L.; Wang, H.; Xu, J.; Zhu, J.; Ding, K. Inhibition of cathepsin S induces autophagy and apoptosis in human glioblastoma cell lines through ROS-mediated PI3K/AKT/mTOR/p70S6K and JNK signaling pathways. Toxicol. Lett. 2014, 228, 248-259.
104. Neeli, I.; Radic, M. Opposition between PKC isoforms regulates histone deimination and neutrophil extracellular chromatin release. Front. Immunol. 2013, doi:10.3389/fimmu.2013.00038.
105. Byrd, A.S.; O'Brien, X.M.; Johnson, C.M.; Lavigne, L.M.; Reichner, J.S. An extracellular matrix-based mechanism of rapid neutrophil extracellular trap formation in response to Candida albicans. J. Immunol. 2013, 190, 4136-4148.
106. Borgquist, J.D.; Quinn, M.T.; Swain, S.D. Adhesion to extracellular matrix proteins modulates bovine neutrophil responses to inflammatory mediators. J. Leukoc. Biol. 2002, 71, 764-774.
107. Begde, D.; Bundale, S.; Mashitha, P.; Rudra, J.; Nashikkar, N.; Upadhyay, A. Immunomodulatory efficacy of nisin-A bacterial lantibiotic peptide. J. Pept. Sci. 2011, 17, 438-444.
108. Arcaro, A.; Wymann, M.P. Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: The role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses. Biochem. J. 1993, 296, 297-301.
109. Ambruso, D.R.; Cusack, N.; Thurman, G. NADPH oxidase activity of neutrophil specific granules: Requirements for cytosolic components and evidence of assembly during cell activation. Mol. Genet. MeTable 2004, 81, 313-321.
110. Lamb, F.S.; Hook, J.S.; Hilkin, B.M.; Huber, J.N.; Volk, A.P.D.; Moreland, J.G. Endotoxin priming of neutrophils requires endocytosis and NADPH oxidase-dependent endosomal reactive oxygen species. J. Biol. Chem. 2012, 287, 12395-12404.
111. Karlsson, A.; Dahlgren, C. Assembly and activation of the neutrophil NADPH oxidase in granule membranes. Antioxid. Redox Signal. 2002, 4, 49-60.
112. Fisher, A.B. Redox signaling across cell membranes. Antioxid. Redox Signal. 2009, 11, 1349-1356.
113. Morre, D.J. Preferential inhibition of the plasma membrane NADH oxidase (NOX) activity by diphenyleneiodonium chloride with NADPH as donor. Antioxid. Redox Signal. 2002, 4, 207-212.
114. Kim, Y.; Kim, Y.-S.; Kim, D.E.; Lee, J.S.; Song, J.H.; Kim, H.-G.; Cho, D.-H.; Jeong, S.-Y.; Jin, D.-H.; Jang, S.J.; et al. BIX-01294 induces autophagy-associated cell death via EHMT2/G9a dysfunction and intracellular reactive oxygen species production. Autophagy 2013, 9, 2126-2139.
115. Riganti, C.; Gazzano, E.; Polimeni, M.; Costamagna, C.; Bosia, A.; Ghigo, D. Diphenyleneiodonium inhibits the cell redox metabolism and induces oxidative stress. J. Biol. Chem. 2004, 279, 47726-47731.
116. Douda, D.N.; Khan, M.A.; Grasemann, H.; Palaniyar, N. SK3 channel and mitochondrial ROS mediate NADPH oxidase-independent NETosis induced by calcium influx. Proc. Natl. Acad. Sci. USA 2015, 112, 2817-2822.
117. Vitte, J.; Michel, B.F.; Bongrand, P.; Gastaut, J.-L. Oxidative stress level in circulating neutrophils is linked to neurodegenerative diseases. J. Clin. Immunol. 2004, 24, 683-692.
118. Maianski, N.A.; Geissler, J.; Srinivasula, S.M.; Alnemri, E.S.; Roos, D.; Kuijpers, T.W. Functional characterization of mitochondria in neutrophils: A role restricted to apoptosis. Cell Death Differ. 2004, 11, 143-153.
119. Davies, M.J. Myeloperoxidase-derived oxidation: Mechanisms of biological damage and its prevention. J. Clin. Biochem. Nutr. 2011, 48, 8-19.
120. Edwards, S.W.; Nurcombe, H.L.; Hart, C.A. Oxidative inactivation of myeloperoxidase released from human neutrophils. Biochem. J. 1987, 245, 925-928.
121. Pullar, J.M.; Vissers, M.C.; Winterbourn, C.C. Living with a killer: The effects of hypochlorous acid on mammalian cells. IUBMB Life 2000, 50, 259-266.
122. Lloyd, M.M.; van Reyk, D.M.; Davies, M.J.; Hawkins, C.L. Hypothiocyanous acid is a more potent inducer of apoptosis and protein thiol depletion in murine macrophage cells than hypochlorous acid or hypobromous acid. Biochem. J. 2008, 414, 271-280.
123. Lane, A.E.; Tan, J.T.M.; Hawkins, C.L.; Heather, A.K.; Davies, M.J. The myeloperoxidase-derived oxidant HOSCN inhibits protein tyrosine phosphatases and modulates cell signalling via the mitogen-activated protein kinase (MAPK) pathway in macrophages. Biochem. J. 2010, 430, 161-169.
124. Augusto, O.; Miyamoto, S. Oxygen Radicals and Related Species. In Principles of Free Radical Biomedicine; Nova Science Publishers: Hauppauge, NY, USA, 2011; Volume 1, Chapter 2, p. 23.
125. Bauer, G. HOCl-dependent singlet oxygen and hydroxyl radical generation modulate and induce apoptosis of malignant cells. Anticancer Res. 2013, 33, 3589-3602.
126. Mylonas, C.; Kouretas, D. Lipid peroxidation and tissue damage. Vivo Athens Greece 1999, 13, 295-309.
127. Yoon, J.H.; Lee, M.S.; Kang, J.H. Reaction of ferritin with hydrogen peroxide induces lipid peroxidation. BMB Rep. 2010, 43, 219-224.
128. Wu, J.; Teuber, K.; Eibisch, M.; Fuchs, B.; Schiller, J. Chlorinated and brominated phosphatidylcholines are generated under the influence of the Fenton reagent at low pH-a MALDI-TOF MS study. Chem. Phys. Lipids 2011, 164, 1-8.
129. Wesselius, L.J.; Nelson, M.E.; Skikne, B.S. Increased release of ferritin and iron by iron-loaded alveolar macrophages in cigarette smokers. Am. J. Respir. Crit. Care Med. 1994, 150, 690-695.
130. Ponka, P.; Beaumont, C.; Richardson, D.R. Function and regulation of transferrin and ferritin. Semin. Hematol. 1998, 35, 35-54.
131. Yuan, X.-M.; Li, W.; Baird, S.K.; Carlsson, M.; Melefors, O. Secretion of ferritin by iron-laden macrophages and influence of lipoproteins. Free Radic. Res. 2004, 38, 1133-1142.
132. Recalcati, S.; Invernizzi, P.; Arosio, P.; Cairo, G. New functions for an iron storage protein: The role of ferritin in immunity and autoimmunity. J. Autoimmun. 2008, 30, 84-89.
133. Yousefi, S.; Gold, J.A.; Andina, N.; Lee, J.J.; Kelly, A.M.; Kozlowski, E.; Schmid, I.; Straumann, A.; Reichenbach, J.; Gleich, G.J.; Simon, H.-U. Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat. Med. 2008, 14, 949-953.
134. Sautin, Y.Y.; Johnson, R.J. Uric acid: The oxidant-antioxidant paradox. Nucleosides Nucleotides Nucleic Acids 2008, 27, 608-619.
135. Schorn, C.; Janko, C.; Krenn, V.; Zhao, Y.; Munoz, L.E.; Schett, G.; Herrmann, M. Bonding the foe-NETting neutrophils immobilize the pro-inflammatory monosodium urate crystals. Front. Immunol. 2012, doi:10.3389/fimmu.2012.00376.
136. Arai, Y.; Nishinaka, Y.; Arai, T.; Morita, M.; Mizugishi, K.; Adachi, S.; Takaori-Kondo, A.; Watanabe, T.; Yamashita, K. Uric acid induces NADPH oxidase-independent neutrophil extracellular trap formation. Biochem. Biophys. Res. Commun. 2014, 443, 556-561.
137. McDonald, P.P.; Bald, A.; Cassatella, M.A. Activation of the NF-κB pathway by inflammatory stimuli in human neutrophils. Blood 1997, 89, 3421-3433.
138. Lapponi, M.J.; Carestia, A.; Landoni, V.I.; Rivadeneyra, L.; Etulain, J.; Negrotto, S.; Pozner, R.G.; Schattner, M. Regulation of neutrophil extracellular trap formation by anti-inflammatory drugs. J. Pharmacol. Exp. Ther. 2013, 345, 430-437.