Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality

Cell Death and Differentiation

Volumn 18, Issue 4, 2011, Pages 581-588

  Remijsen, Q ^a,b   Kuijpers, T W ^c,d   Wirawan, E ^a,b   Lippens, S ^a,b   Vandenabeele, P ^a,b   Vanden Berghe, T ^a,b  

^a GHENT UNIVERSITY   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c SANQUIN RESEARCH   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

autophagy; cell death; NADPH oxidase; NETosis; superoxide

Indexed keywords

HISTONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

APOPTOSIS; AUTOPHAGY; BIOCHEMISTRY; CALCIUM CELL LEVEL; CELL DEATH; CELL STRUCTURE; CHROMATIN; CHROMATIN STRUCTURE; HOMEOSTASIS; HUMAN; LEUKOCYTE ACTIVATION; NEUTROPHIL; NEUTROPHIL EXTRACELLULAR TRAP; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANTI-INFECTIVE AGENTS; APOPTOSIS; EXTRACELLULAR SPACE; HUMANS; NEUTROPHIL ACTIVATION; NEUTROPHILS; SUPEROXIDES;

BACTERIA (MICROORGANISMS);

EID: 79952622190     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2011.1     Document Type: Review

References (95)

1. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 2006; 6: 173-182. (Pubitemid 43290987)
2. Luo HR, Loison F. Constitutive neutrophil apoptosis: mechanisms and regulation. Am J Hematol 2008; 83: 288-295. (Pubitemid 351458006)
3. Segal AW. How neutrophils kill microbes. Annu Rev Immunol 2005; 23: 197-223. (Pubitemid 40563169)
4. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532-1535. (Pubitemid 38314426)
5. Klebanoff SJ. Myeloperoxidase: contribution to the microbicidal activity of intact leukocytes. Science 1970; 169: 1095-1097.
6. Meissner F, Seger RA, Moshous D, Fischer A, Reichenbach J, Zychlinsky A. Inflammasome activation in NADPH oxidase defective mononuclear phagocytes from patients with chronic granulomatous disease. Blood 2010; 116: 1570-1573.
7. Reeves EP, Lu H, Jacobs HL, Messina CG, Bolsover S, Gabella G et al. Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 2002; 416: 291-297. (Pubitemid 34260237)
8. Romani L, Fallarino F, De Luca A, Montagnoli C, D'Angelo C, Zelante T et al. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 2008; 451: 211-215.
9. Sadikot RT, Zeng H, Yull FE, Li B, Cheng DS, Kernodle DS et al. p47phox deficiency impairs NF-kappa B activation and host defense in Pseudomonas pneumonia. J Immunol 2004; 172: 1801-1808. (Pubitemid 38116828)
10. Siddiqui S, Anderson VL, Hilligoss DM, Abinun M, Kuijpers TW, Masur H et al. Fulminant mulch pneumonitis: an emergency presentation of chronic granulomatous disease. Clin Infect Dis 2007; 45: 673-681. (Pubitemid 47378879)
11. van den Berg JM, van Koppen E, Ahlin A, Belohradsky BH, Bernatowska E, Corbeel L et al. Chronic granulomatous disease: the European experience. PLoS ONE 2009; 4: e5234.
12. Remijsen Q, Vanden Berghe T, Wirawan E, Asselbergh B, Parthoens E, De Rycke R et al. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Res 2010; Epub ahead of print 9 November 2010.
13. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009; 5: e1000639.
14. Brinkmann V, Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol 2007; 5: 577-582. (Pubitemid 47074113)
15. Parseghian MH, Luhrs KA. Beyond the walls of the nucleus: the role of histones in cellular signaling and innate immunity. Biochem Cell Biol 2006; 84: 589-604. (Pubitemid 44703662)
16. Beiter K, Wartha F, Albiger B, Normark S, Zychlinsky A, Henriques-Normark B. An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr Biol 2006; 16: 401-407. (Pubitemid 43259351)
17. Buchanan JT, Simpson AJ, Aziz RK, Liu GY, Kristian SA, Kotb M et al. DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol 2006; 16: 396-400. (Pubitemid 43259350)
18. Wartha F, Beiter K, Albiger B, Fernebro J, Zychlinsky A, Normark S et al. Capsule and D-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell Microbiol 2007; 9: 1162-1171. (Pubitemid 46547136)
19. Yousefi S, Gold JA, Andina N, Lee JJ, Kelly AM, Kozlowski E et al. Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med 2008; 14: 949-953.
20. Kockritz-Blickwede M, Goldmann O, Thulin P, Heinemann K, Norrby-Teglund A, Rohde M et al. Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 2008; 111: 3070-3080.
21. Wartha F, Henriques-Normark B. ETosis: a novel cell death pathway. Sci Signal 2008; 1: e25.
22. Logters T, Margraf S, Altrichter J, Cinatl J, Mitzner S, Windolf J et al. The clinical value of neutrophil extracellular traps. Med Microbiol Immunol 2009; 198: 211-219.
23. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007; 176: 231-241. (Pubitemid 46143263)
24. Steinberg BE, Grinstein S. Unconventional roles of the NADPH oxidase: signaling, ion homeostasis, and cell death. Sci STKE 2007; 2007: e11.
25. Bruns S, Kniemeyer O, Hasenberg M, Aimanianda V, Nietzsche S, Thywissen A et al. Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog 2010; 6: e1000873.
26. Ermert D, Urban CF, Laube B, Goosmann C, Zychlinsky A, Brinkmann V. Mouse neutrophil extracellular traps in microbial infections. J Innate Immun 2009; 1: 181-193.
27. Jaillon S, Peri G, Delneste Y, Fremaux I, Doni A, Moalli F et al. The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. J Exp Med 2007; 204: 793-804. (Pubitemid 46631609)
28. McCormick A, Heesemann L, Wagener J, Marcos V, Hartl D, Loeffler J et al. NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microbes Infect 2010; 12: 928-936.
29. Urban CF, Reichard U, Brinkmann V, Zychlinsky A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol 2006; 8: 668-676. (Pubitemid 43372744)
30. Marcos V, Zhou Z, Yildirim AO, Bohla A, Hector A, Vitkov L et al. CXCR2 mediates NADPH oxidase-independent neutrophil extracellular trap formation in cystic fibrosis airway inflammation. Nat Med 2010; 16: 1018-1023.
31. Ramos-Kichik V, Mondragon-Flores R, Mondragon-Castelan M, Gonzalez-Pozos S, Muniz-Hernandez S, Rojas-Espinosa O et al. Neutrophil extracellular traps are induced by Mycobacterium tuberculosis. Tuberculosis (Edinb) 2009; 89: 29-37.
32. Baker VS, Imade GE, Molta NB, Tawde P, Pam SD, Obadofin MO et al. Cytokine-associated neutrophil extracellular traps and antinuclear antibodies in Plasmodium falciparum infected children under six years of age. Malar J 2008; 7: 41.
33. Guimaraes-Costa AB, Nascimento MT, Froment GS, Soares RP, Morgado FN, Conceicao-Silva F et al. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci USA 2009; 106: 6748-6753.
34. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 2010; 11: 700-714.
35. Palic D, Ostojic J, Andreasen CB, Roth JA. Fish cast NETs: neutrophil extracellular traps are released from fish neutrophils. Dev Comp Immunol 2007; 31: 805-816. (Pubitemid 46550690)
36. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007; 13: 463-469. (Pubitemid 46559832)
37. Kessenbrock K, Krumbholz M, Schonermarck U, Back W, Gross WL, Werb Z et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 2009; 15: 623-625.
38. Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci USA 2010; 107: 9813-9818.
39. Krautgartner WD, Klappacher M, Hannig M, Obermayer A, Hartl D, Marcos V et al. Fibrin mimics neutrophil extracellular traps in SEM. Ultrastruct Pathol 2010; 34: 226-231.
40. Neeli I, Khan SN, Radic M. Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol 2008; 180: 1895-1902.
41. Wang Y, Li M, Stadler S, Correll S, Li P, Wang D et al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 2009; 184: 205-213.
42. Anzilotti C, Pratesi F, Tommasi C, Migliorini P. Peptidylarginine deiminase 4 and citrullination in health and disease. Autoimmun Rev 2010; 9: 158-160.
43. Chang X, Yamada R, Suzuki A, Sawada T, Yoshino S, Tokuhiro S et al. Localization of peptidylarginine deiminase 4 (PADI4) and citrullinated protein in synovial tissue of rheumatoid arthritis. Rheumatology (Oxford) 2005; 44: 40-50. (Pubitemid 40124330)
44. Asaga H, Nakashima K, Senshu T, Ishigami A, Yamada M. Immunocytochemical localization of peptidylarginine deiminase in human eosinophils and neutrophils. J Leukoc Biol 2001; 70: 46-51. (Pubitemid 32613661)
45. Proost P, Loos T, Mortier A, Schutyser E, Gouwy M, Noppen S et al. Citrullination of CXCL8 by peptidylarginine deiminase alters receptor usage, prevents proteolysis, and dampens tissue inflammation. J Exp Med 2008; 205: 2085-2097.
46. Suzuki A, Yamada R, Chang X, Tokuhiro S, Sawada T, Suzuki M et al. Functional haplotypes of PADI4, encoding citrullinating enzyme peptidylarginine deiminase 4, are associated with rheumatoid arthritis. Nat Genet 2003; 34: 395-402. (Pubitemid 36935332)
47. Mastronardi FG, Wood DD, Mei J, Raijmakers R, Tseveleki V, Dosch HM et al. Increased citrullination of histone H3 in multiple sclerosis brain and animal models of demyelination: a role for tumor necrosis factor-induced peptidylarginine deiminase 4 translocation. J Neurosci 2006; 26: 11387-11396. (Pubitemid 44772168)
48. Cuthbert GL, Daujat S, Snowden AW, Erdjument-Bromage H, Hagiwara T, Yamada M et al. Histone deimination antagonizes arginine methylation. Cell 2004; 118: 545-553. (Pubitemid 39179708)
49. Marcos V, Nussbaum C, Vitkov L, Hector A, Wiedenbauer EM, Roos D et al. Delayed but functional neutrophil extracellular trap formation in neonates. Blood 2009; 114: 4908-4911.
50. Papayannopoulos V, Zychlinsky A. NETs: a new strategy for using old weapons. Trends Immunol 2009; 30: 513-521.
51. Bianchi M, Hakkim A, Brinkmann V, Siler U, Seger RA, Zychlinsky A et al. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 2009; 114: 2619-2622.
52. Remijsen Q, Vandenabeele P, Willems J, Kuijpers TW. Reconstitution of protection against Aspergillus infection in chronic granulomatous disease (CGD). Blood 2009; 114: 3497.
53. Fadeel B, Ahlin A, Henter JI, Orrenius S, Hampton MB. Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species. Blood 1998; 92: 4808-4818. (Pubitemid 29005884)
54. Hampton MB, Stamenkovic I, Winterbourn CC. Interaction with substrate sensitises caspase-3 to inactivation by hydrogen peroxide. FEBS Lett 2002; 517: 229-232. (Pubitemid 34327665)
55. Wilkie RP, Vissers MC, Dragunow M, Hampton MB. A functional NADPH oxidase prevents caspase involvement in the clearance of phagocytic neutrophils. Infect Immun 2007; 75: 3256-3263. (Pubitemid 47040926)
56. Arruda MA, Rossi AG, de Freitas MS, Barja-Fidalgo C, Graca-Souza AV. Heme inhibits human neutrophil apoptosis: involvement of phosphoinositide 3-kinase, MAPK, and NF-kappaB. J Immunol 2004; 173: 2023-2030. (Pubitemid 38971639)
57. Gupta AK, Joshi MB, Philippova M, Erne P, Hasler P, Hahn S et al. Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death. FEBS Lett 2010; 584: 3193-3197.
58. Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol 2010; 191: 677-691.
59. Yost CC, Cody MJ, Harris ES, Thornton NL, McInturff AM, Martinez ML et al. Impaired neutrophil extracellular trap (NET) formation: a novel innate immune deficiency of human neonates. Blood 2009; 113: 6419-6427.
60. Gupta AK, 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.
61. Sheppard FR, Kelher MR, Moore EE, McLaughlin NJ, Banerjee A, Silliman CC. Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation. J Leukoc Biol 2005; 78: 1025-1042. (Pubitemid 41572466)
62. Francois S, El Benna J, Dang PM, Pedruzzi E, Gougerot-Pocidalo MA, Elbim C. Inhibition of neutrophil apoptosis by TLR agonists in whole blood: involvement of the phosphoinositide 3-kinase/Akt and NF-kappaB signaling pathways, leading to increased levels of Mcl-1, A1, and phosphorylated Bad. J Immunol 2005; 174: 3633-3642. (Pubitemid 40354073)
63. Yousefi S, Mihalache C, Kozlowski E, Schmid I, Simon HU. Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ 2009; 16: 1438-1444.
64. Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F et al. Extracellular histones are major mediators of death in sepsis. Nat Med 2009; 15: 1318-1321.
65. Gabriel C, McMaster WR, Girard D, Descoteaux A. Leishmania donovani promastigotes evade the antimicrobial activity of neutrophil extracellular traps. J Immunol 2010; 185: 4319-4327.
66. Eskelinen EL, Saftig P. Autophagy: a lysosomal degradation pathway with a central role in health and disease. Biochim Biophys Acta 2009; 1793: 664-673.
67. Eskelinen EL. New insights into the mechanisms of macroautophagy in mammalian cells. Int Rev Cell Mol Biol 2008; 266: 207-247.
68. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132: 27-42.
69. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T et al. The role of autophagy during the early neonatal starvation period. Nature 2004; 432: 1032-1036. (Pubitemid 40052234)
70. Lee HK, Mattei LM, Steinberg BE, Alberts P, Lee YH, Chervonsky A et al. In vivo requirement for Atg5 in antigen presentation by dendritic cells. Immunity 2010; 32: 227-239.
71. Miller BC, Zhao Z, Stephenson LM, Cadwell K, Pua HH, Lee HK et al. The autophagy gene ATG5 plays an essential role in B lymphocyte development. Autophagy 2008; 4: 309-314. (Pubitemid 351458091)
72. Pua HH, Dzhagalov I, Chuck M, Mizushima N, He YW. A critical role for the autophagy gene Atg5 in T cell survival and proliferation. J Exp Med 2007; 204: 25-31. (Pubitemid 46148752)
73. Huang J, Canadien V, Lam GY, Steinberg BE, Dinauer MC, Magalhaes MA et al. Activation of antibacterial autophagy by NADPH oxidases. Proc Natl Acad Sci USA 2009; 106: 6226-6231.
74. Delgado MA, Elmaoued RA, Davis AS, Kyei G, Deretic V. Toll-like receptors control autophagy. EMBO J 2008; 27: 1110-1121. (Pubitemid 351508141)
75. Xu Y, Jagannath C, Liu XD, Sharafkhaneh A, Kolodziejska KE, Eissa NT. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 2007; 27: 135-144. (Pubitemid 47089027)
76. Mitroulis I, Kourtzelis I, Kambas K, Rafail S, Chrysanthopoulou A, Speletas M et al. Regulation of the autophagic machinery in human neutrophils. Eur J Immunol 2010; 40: 1461-1472.
77. Beertsen W, Willenborg M, Everts V, Zirogianni A, Podschun R, Schroder B et al. Impaired phagosomal maturation in neutrophils leads to periodontitis in lysosomal-associated membrane protein-2 knockout mice. J Immunol 2008; 180: 475-482.
78. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119: 753-766. (Pubitemid 40017683)
79. Uchiya K, Barbieri MA, Funato K, Shah AH, Stahl PD, Groisman EA. A Salmonella virulence protein that inhibits cellular trafficking. EMBO J 1999; 18: 3924-3933. (Pubitemid 29335845)
80. Chen Y, Azad MB, Gibson SB. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ 2009; 16: 1040-1052.
81. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007; 26: 1749-1760. (Pubitemid 46624042)
82. von Gunten S, Yousefi S, Seitz M, Jakob SM, Schaffner T, Seger R et al. Siglec-9 transduces apoptotic and nonapoptotic death signals into neutrophils depending on the proinflammatory cytokine environment. Blood 2005; 106: 1423-1431. (Pubitemid 41129611)
83. Zhang Q, Itagaki K, Hauser CJ. Mitochondrial DNA is released by shock and activates neutrophils via p38 map kinase. Shock 2010; 34: 55-59.
84. Jozsef L, Khreiss T, Filep JG. CpG motifs in bacterial DNA delay apoptosis of neutrophil granulocytes. FASEB J 2004; 18: 1776-1778. (Pubitemid 39561681)
85. Maianski NA, Geissler J, Srinivasula SM, Alnemri ES, Roos D, Kuijpers TW. Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis. Cell Death Differ 2004; 11: 143-153. (Pubitemid 38159638)
86. van Raam BJ, Sluiter W, de Wit E, Roos D, Verhoeven AJ, Kuijpers TW. Mitochondrial membrane potential in human neutrophils is maintained by complex III activity in the absence of supercomplex organisation. PLoS ONE 2008; 3: e2013.
87. Borregaard N, Herlin T. Energy metabolism of human neutrophils during phagocytosis. J Clin Invest 1982; 70: 550-557. (Pubitemid 12054579)
88. Fossati G, Moulding DA, Spiller DG, Moots RJ, White MR, Edwards SW. The mitochondrial network of human neutrophils: role in chemotaxis, phagocytosis, respiratory burst activation, and commitment to apoptosis. J Immunol 2003; 170: 1964-1972. (Pubitemid 36197416)
89. Brinkmann V, Laube B, Abu AU, Goosmann C, Zychlinsky A. Neutrophil extracellular traps: how to generate and visualize them. J Vis Exp 2010; 24: pii: 1724. doi:10.3791/1724.
90. Vitkov L, Klappacher M, Hannig M, Krautgartner WD. Extracellular neutrophil traps in periodontitis. J Periodontal Res 2009; 44: 664-672.
91. Lippolis JD, Reinhardt TA, Goff JP, Horst RL. Neutrophil extracellular trap formation by bovine neutrophils is not inhibited by milk. Vet Immunol Immunopathol 2006; 113: 248-255.
92. Lauth X, Kockritz-Blickwede M, McNamara CW, Myskowski S, Zinkernagel AS, Beall B et al. M1 protein allows Group A streptococcal survival in phagocyte extracellular traps through cathelicidin inhibition. J Innate Immun 2009; 1: 202-214.
93. Oehmcke S, Morgelin M, Herwald H. Activation of the human contact system on neutrophil extracellular traps. J Innate Immun 2009; 1: 225-230.
94. Grinberg N, Elazar S, Rosenshine I, Shpigel NY. Beta-hydroxybutyrate abrogates formation of bovine neutrophil extracellular traps and bactericidal activity against mammary pathogenic Escherichia coli. Infect Immun 2008; 76: 2802-2807.
95. Alghamdi AS, Foster DN. Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps. Biol Reprod 2005; 73: 1174-1181. (Pubitemid 41698607)