Neutrophil extracellular traps and their role in the development of chronic inflammation and autoimmunity

Autoimmunity Reviews

Volumn 14, Issue 7, 2015, Pages 633-640

  Pinegin, Boris ^a   Vorobjeva, Nina ^b   Pinegin, Vladimir ^c  

^a FEDERAL BIOMEDICAL AGENCY OF RUSSIA   (Russian Federation)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c I M SECHENOV FIRST MOSCOW STATE MEDICAL UNIVERSITY   (Russian Federation)

Author keywords

Alarmins; Atherosclerosis; LL 37 DNA complex; NETosis; Neutrophil extracellular traps; Neutrophils; Psoriasis

Indexed keywords

CATHELICIDIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; DEOXYRIBONUCLEASE; PEPTIDOGLYCAN RECOGNITION PROTEIN; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 9;

ANKYLOSING SPONDYLITIS; ANTIMICROBIAL ACTIVITY; ATHEROSCLEROSIS; AUTOIMMUNE UVEITIS; AUTOIMMUNITY; CELL MEMBRANE; CELL NUCLEUS MEMBRANE; CROHN DISEASE; EXTRACELLULAR TRAP; HUMAN; INFLAMMATION; MULTIPLE SCLEROSIS; PSORIASIS; REVIEW; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; CHRONIC DISEASE; IMMUNOLOGY; NEUTROPHIL;

ANIMALS; AUTOIMMUNITY; CHRONIC DISEASE; EXTRACELLULAR TRAPS; HUMANS; INFLAMMATION; NEUTROPHILS; PSORIASIS;

EID: 84928925863     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2015.03.002     Document Type: Review

References (70)

1. Janeway C.A. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 1989, 54(Pt 1):1-13.
2. Bianchi M.E. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 2007, 81:1-5.
3. Lotze M.T., Zeh H.J., Rubartelli A., Sparvero L.J., Amoscato A.A., Washburn N.R., et al. The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 2007, 220:60-81.
4. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., et al. Neutrophil extracellular traps kill bacteria. Science 2004, 303:1532-1535.
5. Brinkmann V., Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol 2007, 5:577-582.
6. Boehncke W.H. Epidemiology and potential pathomechanisms of cardiovascular comorbidities in psoriasis: a report from the GRAPPA 2010 annual meeting. J Rheumatol 2012, 39:441-444.
7. Armstrong A.W., Schupp C., Bebo B. Psoriasis comorbidities: results from the National Psoriasis Foundation surveys 2003 to 2011. Dermatology 2012, 225:121-126.
8. Boehncke W.H. GRAPPA 2013 basic/translational/clinical science update: comorbidity monitoring. J Rheumatol 2014, 41:1224-1226.
9. Steinberg B.E., Grinstein S. Unconventional roles of the NADPH oxidase: signaling, ion homeostasis, and cell death. Sci STKE 2007, 2007. pe11.
10. Yousefi S., Gold J.A., Andina N., Lee J.J., Kelly A.M., Kozlowski E., et al. Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med 2008, 14:949-953.
11. von 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.
12. Chow O.A., von Kockritz-Blickwede M., Bright A.T., Hensler M.E., Zinkernagel A.S., Cogen A.L., et al. Statins enhance formation of phagocyte extracellular traps. Cell Host Microbe 2010, 8:445-454.
13. Urban C.F., 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. Papayannopoulos V., Zychlinsky A. NETs: a new strategy for using old weapons. Trends Immunol 2009, 30:513-521.
15. Averhoff P., Kolbe M., Zychlinsky A., Weinrauch Y. Single residue determines the specificity of neutrophil elastase for Shigella virulence factors. J Mol Biol 2008, 377:1053-1066. [23].
16. Parker H., Albrett A.M., Kettle A.J., Winterbourn C.C. Myeloperoxidase associated with neutrophil extracellular traps is active and mediates bacterial killing in the presence of hydrogen peroxide. J Leukoc Biol 2012, 91:369-376.
17. 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. [e7].
18. Cui B.B., Tan C.Y., Schorn C., Tang H.H., Liu Y., Zhao Y. Neutrophil extracellular traps in sterile inflammation: the story after dying?. Autoimmunity 2012, 45:593-596.
19. Vorobjeva N.V. NADPH oxidase of neutrophils and diseases associated with its dysfunction. Immunol (Russ) 2013, 34:232-238.
20. Fuchs T.A., 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.
21. Pinegin B.V., Maianski A.N. The neutrophils: structure and functions. Immunol (Russ) 2007, 6:374-382.
22. Bianchi M., Hakkim A., Brinkmann V., Siler U., Seger R.A., Zychlinsky A., et al. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 2009, 114:2619-2622.
23. Hakkim A., Fuchs T.A., Martinez N.E., Hess S., Prinz H., Zychlinsky A., et al. Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat Chem Biol 2011, 7:75-77.
24. Lim M.B.H., Kuiper J.W.P., Katchky A., Goldberg H., Glogauer M. Rac2 is required for the formation of neutrophil extracellular traps. J Leukoc Biol 2011, 90:771-776.
25. 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.
26. Metzler K.D., Fuchs T.A., Nauseef W.M., Reumaux D., Roesler J., Schulze I., et al. Myeloperoxidase is required for neutrophil extracellular trap formation: implications for innate immunity. Blood 2011, 117:953-959.
27. Neeli I., Dwivedi N., Khan S., Radic M. Regulation of extracellular chromatin release from neutrophils. J Innate Immun 2009, 1:194-201.
28. Neeli I., Khan S.N., Radic M. Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol 2008, 180:1895-1902.
29. 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.
30. 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 2011, 21:290-304.
31. Yipp B.G., Kubes P. NETosis: how vital is it?. Blood 2013, 122:2784-2794.
32. Pilsczek F.H., Salina D., Poon K.K., Fahey C., Yipp B.G., Sibley C.D., et al. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 2010, 185:7413-7425.
33. Yipp B.G., Petri B., Salina D., Jenne C.N., Scott B.N., Zbytnuik L.D., et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 2012, 18:1386-1393.
34. Clark S.R., Ma A.C., Tavener S.A., McDonald B., Goodarzi Z., Kelly M.M., et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007, 13:463-469.
35. 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.
36. 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.
37. 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.
38. Yost C.C., Cody M.J., Harris E.S., Thornton N.L., McInturff A.M., Martinez M.L., et al. Impaired neutrophil extracellular trap (NET) formation: a novel innate immune deficiency of human neonates. Blood 2009, 113:6419-6427.
39. Sumby P., Barbian K.D., Gardner D.J., Whitney A.R., Welty D.M., Long R.D., et al. Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc Natl Acad Sci U S A 2005, 102:1679-1684.
40. Buchanan J.T., Simpson A.J., Aziz R.K., Liu G.Y., Kristian S.A., 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.
41. Menegazzi R., Decleva E., Dri P. Killing by neutrophil extracellular traps: fact or folklore?. Blood 2012, 119:1214-1216.
42. Weiss S.J. Tissue destruction by neutrophils. N Engl J Med 1989, 320:365-376.
43. Matzinger P. The danger model: a renewed sense of self. Science 2002, 296:301-305.
44. Pinegin B.V., Karsonova M.I. Alarmins - the endogenous activators of inflammation and innate immunity. Immunol 2010, 31:246-255.
45. Theofilopoulos A.N., Kono D.H., Beutler B., Baccala R. Intracellular nucleic acid sensors and autoimmunity. J Interferon Cytokine Res 2011, 31:867-886.
46. Theofilopoulos A.N., Baccala R., Beutler B., Kono D.H. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 2005, 23:307-336.
47. Schittek B., Paulmann M., Senyürek I., Steffen H. The role of antimicrobial peptides in human skin and in skin infectious diseases. Infect Disord Drug Targets 2008, 8:135-143.
48. Schröder J.M. The role of keratinocytes in defense against infection. Curr Opin Infect Dis 2010, 23:106-110.
49. Heilborn J.D., Nilsson M.F., Kratz G., Weber G., Sørensen O., Borregaard N., et al. The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J Invest Dermatol 2003, 120:379-389.
50. Lande R., Gregorio J., Facchinetti V., Chatterjee B., Wang Y.H., Homey B., et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007, 449:564-569.
51. Lande R., Ganguly D., Facchinetti V., Frasca L., Conrad C., Gregorio J., et al. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci Transl Med 2011, 3:73.
52. Ganguly D., Chamilos G., Lande R., Gregorio J., Meller S., Facchinetti V., et al. Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J Exp Med 2009, 206:1983-1994.
53. Morizane S., Yamasaki K., Mühleisen B., Kotol P.F., Murakami M., Aoyama Y., et al. Cathelicidin antimicrobial peptide LL-37 in psoriasis enables keratinocyte reactivity against TLR9 ligands. J Invest Dermatol 2012, 132:135-143.
54. Skrzeczynska-Moncznik J., Wlodarczyk A., Zabieglo K., Kapinska-Mrowiecka M., Marewicz E., Dubin A., et al. Secretory leukocyte proteinase inhibitor-competent DNA deposits are potent stimulators of plasmacytoid dendritic cells: implication for psoriasis. J Immunol 2012, 189:1611-1617.
55. Lin A.M., Rubin C.J., Khandpur R., Wang J.Y., Riblett M., Yalavarthi S., et al. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J Immunol 2011, 187:490-500.
56. Yamamoto T., Matsuuchi M., Irimajiri J., Otoyama K., Nishioka K. Topical anthralin for psoriasis vulgaris: evaluation of 70 Japanese patients. J Dermatol 2000, 27:482-485.
57. Töyry S., Fräki J., Tammi R. Mast cell density in psoriatic skin. The effect of PUVA and corticosteroid therapy. Arch Dermatol Res 1988, 280:282-285.
58. Toichi E., Tachibana T., Furukawa F. Rapid improvement of psoriasis vulgaris during drug-induced agranulocytosis. J Am Acad Dermatol 2000, 43:391-395.
59. Atherton D.J., Wells R.S., Laurent M.R., Williams Y.F. Razoxane (ICRF 159) in the treatment of psoriasis. Br J Dermatol 1980, 102:307-317.
60. Garcia-Romo G.S., Caielli S., Vega B., Connolly J., Allantaz F., Xu Z., et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med 2011, 3:73.
61. Liu C.L., Tangsombatvisit S., Rosenberg J.M., Mandelbaum G., Gillespie E.C., Gozani O.P., et al. Specific post-translational histone modifications of neutrophil extracellular traps as immunogens and potential targets of lupus autoantibodies. Arthritis Res Ther 2012, 14:R25.
62. Price J.V., Tangsombatvisit S. On silico peptide microarrays for high-resolution mapping of antibody epitopes and diverse protein-protein interactions. Nat Med 2012, 18:1434-1440.
63. Döring Y., Drechsler M., Wantha S., Kemmerich K., Lievens D., Vijayan S., et al. Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice. Circ Res 2012, 110:1052-1056.
64. Döring Y., Manthey H.D., Drechsler M., Lievens D., Megens R.T., Soehnlein O., et al. Auto-antigenic protein-DNA complexes stimulate plasmacytoid dendritic cells to promote atherosclerosis. Circulation 2012, 125:1673-1683.
65. Borissoff J.I., Joosen I.A., Versteylen M.O., Brill A., Fuchs T.A., Savchenko A.S., et al. Elevated levels of circulating DNA and chromatin are independently associated with severe coronary atherosclerosis and a prothrombotic state. Arterioscler Thromb Vasc Biol 2013, 33:2032-2040.
66. Carmona-Rivera C., Zhao W., Yalavarthi S., Kaplan M.J. Neutrophil extracellular traps induce endothelial dysfunction in systemic lupus erythematosus through the activation of matrix metalloproteinase-2. Ann Rheum Dis 2014, 10.1136/annrheumdis-2013-204837.
67. Frostegård J. Immune mechanisms in atherosclerosis, especially in diabetes type 2. Front Endocrinol (Lausanne) 2013, 4:162.
68. Rönnblom L. The type I interferon system in the etiopathogenesis of autoimmune diseases. Ups J Med Sci 2011, 116:227-237.
69. Dombrowski Y., Peric M., Koglin S., Kammerbauer C., Göss C., Anz D., et al. Cytosolic DNA triggers inflammasome activation in keratinocytes in psoriatic lesions. Sci Transl Med 2011, 3:82.
70. Knight J.S., Carmona-Rivera C., Kaplan M.J. Proteins derived from neutrophil extracellular traps may serve as self-antigens and mediate organ damage in autoimmune diseases. Front Immunol 2012, 3:380.