374
Views
20
CrossRef citations to date
0
Altmetric
Original Article

Neutrophil extracellular traps generation and degradation in patients with granulomatosis with polyangiitis and systemic lupus erythematosus

, , , , , , & show all
Pages 126-135 | Received 21 Oct 2018, Accepted 11 Jun 2019, Published online: 01 Jul 2019

References

  • Barnado A, Crofford LJ, Oates JC. At the bedside: neutrophil extracellular traps (NETs) as targets for biomarkers and therapies in autoimmune diseases. J Leukoc Biol. 2016;99:265–278.
  • Branzk N, Papayannopoulos V. Molecular mechanisms regulating NETosis in infection and disease. Semin Immunopathol. 2013;35:513–530.
  • Pinegin B, Vorobjeva N, Pinegin V. Neutrophil extracellular traps and their role in the development of chronic inflammation and autoimmunity. Autoimmun Rev. 2015;14:633–640.
  • Pruchniak M, Kotula I, Manda-Handzlik A. Neutrophil extracellular traps (NETs) impact upon autoimmune disorders. Centr Eur J Immunol.2015;40:217–224.
  • Zawrotniak M, Rapala-Kozik M. Neutrophil extracellular traps (NETs) - formation and implications. Acta Biochim Pol. 2013;60:277–284.
  • Boeltz S, Amini P, Anders H-J, et al. To NET or not to NET: current opinions and state of the science regarding the formation of neutrophil extracellular traps. Cell Death Differ. 2019;26:395–408.
  • Carmona-Rivera C, Zhao W, Yalavarthi S, et al. Neutrophil extracellular traps induce endothelial dysfunction in systemic lupus erythematosus through the activation of matrix metalloproteinase-2. Ann Rheum Dis. 2015;74:1417–1424.
  • Kessenbrock K, Krumbholz M, Schönermarck U, et al. Netting neutrophils in autoimmune small-vessel sel vasculitis. Nat Med. 2009;15:623–625.
  • 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.
  • Villanueva E, Yalavarthi S, Berthier CC, et al. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol. 2011;187:538–552.
  • Appelgren D, Dahle C, Knopf J, et al. Active NET formation in Libman–Sacks endocarditis without antiphospholipid antibodies: a dramatic onset of systemic lupus erythematosus. Autoimmunity. 2018;51:310–318.
  • Cojocaru M, et al. Manifestations of systemic lupus erythematosus. Maedica (Buchar). 2011;6:330–336.
  • Maidhof W, Hilas O. Lupus: an overview of the disease and management options. P T. 2012;37:240–249.
  • Yu Y, Su K. Neutrophil extracellular traps and systemic lupus erythematosus. J Clin Cell Immunol. 2013;4:pii: 139.
  • Seo P, Stone JH. The antineutrophil cytoplasmic antibody-associated vasculitides. Am J Med. 2004;117:39–50.
  • Surmiak M, et al. Neutrophil-related and serum biomarkers in granulomatosis with polyangiitis support extracellular traps mechanism of the disease. Clin Exp Rheumatol. 2016;34:S98–S104.
  • Tarzi RM, Pusey CD. Current and future prospects in the management of granulomatosis with polyangiitis (Wegener's granulomatosis). Ther Clin Risk Manag. 2014;10:279–293.
  • Courtney PA, Crockard AD, Williamson K, et al. Increased apoptotic peripheral blood neutrophils in systemic lupus erythematosus: relations with disease activity, antibodies to double stranded DNA, and neutropenia. Ann Rheum Dis. 1999;58:309–314.
  • Giaglis S, Hahn S, Hasler P. "The NET Outcome": are neutrophil extracellular traps of any relevance to the pathophysiology of autoimmune disorders in childhood? Front Pediatr. 2016;4:97.
  • Sangaletti S, Tripodo C, Chiodoni 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.
  • Schonermarck U, Csernok E, Gross WL. Pathogenesis of anti-neutrophil cytoplasmic antibody-associated vasculitis: challenges and solutions 2014. Nephrol Dial Transplant. 2015;30:i46–52.
  • Abi Abdallah DS, Denkers EY. Neutrophils cast extracellular traps in response to protozoan parasites. Front Immunol. 2012;3:382.
  • Baker VS, 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.
  • Panda R, et al. Neutrophil extracellular traps contain selected antigens of anti-neutrophil cytoplasmic antibodies. Front Immunol. 2017;8:439.
  • Soderberg D, et al. Increased levels of neutrophil extracellular trap remnants in the circulation of patients with small vessel vasculitis, but an inverse correlation to anti-neutrophil cytoplasmic antibodies during remission. Rheumatology (Oxford). 2015;54:2085–2094.
  • Tang S, Zhang Y, Yin S-W, et al. Neutrophil extracellular trap formation is associated with autophagy-related signalling in ANCA-associated vasculitis. Clin Exp Immunol. 2015;180:408–418.
  • Soderberg D, Segelmark M. Neutrophil extracellular traps in ANCA-associated vasculitis. Front Immunol. 2016;7:256.
  • Petri M, Orbai A-M, Alarcón GS, et al. Derivation and validation of the systemic lupus international collaborating clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 2012;64:2677–2686.
  • Leavitt RY, Fauci AS, Bloch DA, et al. The American College of Rheumatology 1990 criteria for the classification of Wegener's granulomatosis. Arthritis Rheum. 2010;33:1101–1107.
  • Knight JS, Carmona-Rivera C, Kaplan MJ. Proteins derived from neutrophil extracellular traps may serve as self-antigens and mediate organ damage in autoimmune diseases. Front Immunol. 2012;3:380.
  • Majewski P, et al. Inhibitors of serine proteases in regulating the production and function of neutrophil extracellular traps. Front Immunol. 2016;7:261.
  • Delgado-Rizo V, et al. Neutrophil extracellular traps and its implications in inflammation: an overview. Front Immunol. 2017;8:81.
  • Gupta S, Kaplan MJ. The role of neutrophils and NETosis in autoimmune and renal diseases. Nat Rev Nephrol. 2016;12:402–413.
  • Keshari RS, Jyoti A, Dubey M, et al. Cytokines induced neutrophil extracellular traps formation: implication for the inflammatory disease condition. PLoS One. 2012;7:e48111.
  • Kim J, Kang S, Kim J, et al. Elevated levels of T helper 17 cells are associated with disease activity in patients with rheumatoid arthritis. Ann Lab Med. 2013;33:52–59.
  • Remijsen Q, Kuijpers TW, Wirawan E, et al. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ. 2011;18:581–588.
  • Hu SC, et al. Neutrophil extracellular trap formation is increased in psoriasis and induces human beta-defensin-2 production in epidermal keratinocytes. Sci Rep. 2016;6:31119.
  • Sur Chowdhury C, Giaglis S, Walker UA, et al. Enhanced neutrophil extracellular trap generation in rheumatoid arthritis: analysis of underlying signal transduction pathways and potential diagnostic utility. Arthritis Res Ther. 2014;16:R122.
  • Demers M, Krause DS, Schatzberg D, et al. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proc Natl Acad Sci USA. 2012;109:13076–13081.
  • Garcia-Romo GS, Caielli S, Vega B, et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med. 2011;3:73ra20.
  • Gupta AK, Hasler P, Holzgreve W, et al. Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Hum Immunol. 2005;66:1146–1154.
  • Lande R, Ganguly D, Facchinetti V, et al. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci Transl Med. 2011;3:73ra19.
  • Ermert D, Urban CF, Laube B, et al. Mouse neutrophil extracellular traps in microbial infections. J Innate Immun. 2009;1:181–193.
  • Rodriguez-Espinosa O, et al. Metabolic requirements for neutrophil extracellular traps formation. Immunology. 2015;145:213–224.
  • Csernok E, Gross WL. Current understanding of the pathogenesis of granulomatosis with polyangiitis (Wegener's). Expert Rev Clin Immunol. 2013;9:641–648.
  • 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.
  • Dedkova EN, Sigova AA, Zinchenko VP. Mechanism of action of calcium ionophores on intact cells: ionophore-resistant cells. Membr Cell Biol. 2000;13:357–368.
  • Douda DN, Khan MA, Grasemann H, et al. SK3 channel and mitochondrial ROS mediate NADPH oxidase-independent NETosis induced by calcium influx. Proc Natl Acad Sci USA. 2015;112:2817–2822.
  • Naffah de Souza C, et al. Alkaline pH promotes NADPH oxidase-independent neutrophil extracellular trap formation: a matter of mitochondrial reactive oxygen species generation and citrullination and cleavage of histone. Front Immunol. 2017;8:1849.
  • Parker H, Dragunow M, Hampton MB, et al. Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus. J Leukoc Biol. 2012;92:841–849.
  • Ohlsson SM, Ohlsson S, Söderberg D, et al. Neutrophils from vasculitis patients exhibit an increased propensity for activation by anti-neutrophil cytoplasmic antibodies. Clin Exp Immunol. 2014;176:363–372.
  • Johansson AC, et al. Impaired phagocytosis and reactive oxygen species production in phagocytes is associated with systemic vasculitis. Arthritis Res Ther. 2016;18:92.
  • Bylund J, Brown KL, Movitz C, et al. Intracellular generation of superoxide by the phagocyte NADPH oxidase: how, where, and what for? Free Radic Biol Med. 2010;49:1834–1845.
  • Armstrong DL, Eisenstein M, Zidovetzki R, et al. Systemic lupus erythematosus-associated neutrophil cytosolic factor 2 mutation affects the structure of NADPH oxidase complex. J Biol Chem. 2015;290:12595–12602.
  • Bengtsson AA, Pettersson Å, Wichert S, et al. Low production of reactive oxygen species in granulocytes is associated with organ damage in systemic lupus erythematosus. Arthritis Res Ther. 2014;16:R120.
  • Jacob CO, Eisenstein M, Dinauer MC, et al. Lupus-associated causal mutation in neutrophil cytosolic factor 2 (NCF2) brings unique insights to the structure and function of NADPH oxidase. Proc Natl Acad Sci USA. 2012;109:E59–67.
  • Gray RD, Hardisty G, Regan KH, et al. Delayed neutrophil apoptosis enhances NET formation in cystic fibrosis. Thorax. 2018;73:134–144.
  • Jin L, Batra S, Jeyaseelan S. Diminished neutrophil extracellular trap (NET) formation is a novel innate immune deficiency induced by acute ethanol exposure in polymicrobial sepsis, which can be rescued by CXCL1. PLoS Pathog. 2017;13:e1006637.
  • Lindau D, Mussard J, Rabsteyn A, et al. TLR9 independent interferon alpha production by neutrophils on NETosis in response to circulating chromatin, a key lupus autoantigen. Ann Rheum Dis. 2014;73:2199–2207.
  • Dittmar M, Bischofs C, Matheis N, et al. A novel mutation in the DNASE1 gene is related with protein instability and decreased enzyme activity in thyroid autoimmunity. J Autoimmun. 2009;32:7–13.
  • Kim I, Hur NW, Shin HD, et al. Associations of DNase IV polymorphisms with autoantibodies in patients with systemic lupus erythematosus. Rheumatology (Oxford). 2008;47:996–999.
  • Malickova K, et al. Impaired deoxyribonuclease I activity in patients with inflammatory bowel diseases. Autoimmune Dis. 2011;2011:945861.
  • Leffler J, Gullstrand B, Jönsen A, et al. Degradation of neutrophil extracellular traps co-varies with disease activity in patients with systemic lupus erythematosus. Arthritis Res Ther. 2013;15:R84.
  • Leffler J, et al. A subset of patients with systemic lupus erythematosus fails to degrade DNA from multiple clinically relevant sources. Arthritis Res Ther. 2015;17:205.
  • Hakkim A, Fürnrohr BG, Amann K, et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci USA. 2010;107:9813–9818.
  • Gaipl US, Beyer TD, Heyder P, et al. Cooperation between C1q and DNase I in the clearance of necrotic cell-derived chromatin. Arthritis Rheum. 2004;50:640–649.
  • Leffler J, Martin M, Gullstrand B, et al. Neutrophil extracellular traps that are not degraded in systemic lupus erythematosus activate complement exacerbating the disease. J Immunol. 2012;188:3522–3531.
  • Kaplan MJ, Radic M. Neutrophil extracellular traps: double-edged swords of innate immunity. J Immunol. 2012;189:2689–2695.
  • Munoz LE, Gaipl US, Franz S, et al. SLE-a disease of clearance deficiency? Rheumatology (Oxford). 2005;44:1101–1107.
  • Napirei M, Wulf S, Mannherz HG. Chromatin breakdown during necrosis by serum Dnase1 and the plasminogen system. Arthritis Rheum. 2004;50:1873–1883.
  • Bodano A, et al. Association of a non-synonymous single-nucleotide polymorphism of DNASEI with SLE susceptibility. Rheumatology (Oxford). 2006;45:819–823.
  • Morgan AR, Lam W-J, Han D-Y, et al. DNase1: no association with Crohn's disease in a New Zealand population. ISRN Gastroenterol. 2012;2012:826323.
  • Yasuda T, Kishi K, Yanagawa Y, et al. Structure of the human deoxyribonuclease I (DNase I) gene: identification of the nucleotide substitution that generates its classical genetic polymorphism. Ann Human Genet. 1995;59:1–15.
  • Fujihara J, Ueki M, Kimura-Kataoka K, et al. Functional single nucleotide polymorphisms (SNPs) in the genes encoding the human deoxyribonuclease (DNase) family potentially relevant to autoimmunity. Immunol Invest. 2016;45:406–419.
  • Jo BS, Choi SS. Introns: the functional benefits of introns in genomes. Genomics Inform. 2015;13:112–118.
  • Agrawal A, Hamvas A, Cole FS, et al. An intronic ABCA3 mutation that is responsible for respiratory disease. Pediatr Res. 2012;71:633–637.
  • Anczukow O, Buisson M, Leone M, et al. BRCA2 deep intronic mutation causing activation of a cryptic exon: opening toward a new preventive therapeutic strategy. Clin Cancer Res. 2012;18:4903–4909.
  • Gupta AK, Giaglis S, Hasler P, et al. 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.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.