Treatment with DNases rescues hidden neutrophil elastase from aggregated NETs

. 2019 Dec ; 106 (6) : 1359-1366. [epub] 20190902

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31478257

The release of neutrophil extracellular traps (NETs) is one of the weapons neutrophils have in their armory. NETs consist of extracellular chromatin fibers decorated with a plethora of cytoplasmic and granular proteins, such as the antimicrobial serine protease neutrophil elastase (NE). Because the first description of NETs as beneficial to the host, reports on their double-faced role in health and disease have considerably increased recently. On one hand, NETs reportedly trap and kill bacteria and also participate in the resolution of the acute inflammation associated with infection and with tissue damage. On the other hand, numerous negative aspects of NETs contribute to the etiopathogenesis of autoimmune disorders. Employing soluble and solid fluorescent substrates, we demonstrate the interaction of NE with aggregated NETs (aggNETs), the limitation of its enzymatic activity and the containment of the enzyme from surrounding tissues. These events prevent the spread of inflammation and tissue damage. The detection of DNase 1-dependent elevation of NE activity attests the continuous presence of patrolling neutrophils forming NETs and aggNETs even under conditions physiologic conditions.

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Witko-Sarsat V, Rieu P, Descamps-Latscha B, Lesavre P, Halbwachs-Mecarelli L. Neutrophils: molecules, functions and pathophysiological aspects. Lab Invest. 2000;80:617-653.

Iba T, Hashiguchi N, Nagaoka I, Tabe Y, Murai M. Neutrophil cell death in response to infection and its relation to coagulation. J Intensive Care. 2013;1:13.

Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303:1532-1535.

Fuchs TA, Abed U, Goosmann C, et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol. 2007;176:231-241.

Phillipson M, Kubes P. The neutrophil in vascular inflammation. Nat Med. 2011;17:1381-1390.

Schauer C, Janko C, Munoz LE, et al. Aggregated neutrophil extracellular traps limit inflammation by degrading cytokines and chemokines. Nat Med. 2014;20:511-517.

Schorn C, Janko C, Latzko M, Chaurio R, Schett G, Herrmann M. Monosodium urate crystals induce extracellular DNA traps in neutrophils, eosinophils, and basophils but not in mononuclear cells. Front Immunol. 2012;3:277.

Mahajan A, Herrmann M, Munoz LE. Clearance deficiency and cell death pathways: a model for the pathogenesis of SLE. Front Immunol. 2016;7:35.

Munoz LE, Leppkes M, Fuchs TA, Hoffmann M, Herrmann M. Missing in action-the meaning of cell death in tissue damage and inflammation. Immunol Rev. 2017;280:26-40.

Podolska MJ, Biermann MH, Maueroder C, Hahn J, Herrmann M. Inflammatory etiopathogenesis of systemic lupus erythematosus: an update. J Inflamm Res. 2015;8:161-171.

Munoz LE, Lauber K, Schiller M, Manfredi AA, Herrmann M. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat Rev Rheumatol. 2010;6:280-289.

Kessenbrock K, Krumbholz M, Schonermarck U, et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med. 2009;15:623-625.

Nakazawa D, Shida H, Tomaru U, et al. Enhanced formation and disordered regulation of NETs in myeloperoxidase-ANCA-associated microscopic polyangiitis. JASN. 2014;25:990-997.

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.

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.

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.

Podolska MJ, Mahajan A, Knopf J, et al. Autoimmune, rheumatic, chronic inflammatory diseases: neutrophil extracellular traps on parade. Autoimmunity. 2018;51:281-287.

Leppkes M, Maueroder C, Hirth S, et al. Externalized decondensed neutrophil chromatin occludes pancreatic ducts and drives pancreatitis. Nat Commun. 2016;7:10973.

Fuchs TA, Brill A, Wagner DD. Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscler Thromb Vasc Biol. 2012;32:1777-1783.

Hakkim A, Furnrohr BG, Amann K, et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci U S A. 2010;107:9813-9818.

Mitroulis I, Kambas K, Chrysanthopoulou A, et al. Neutrophil extracellular trap formation is associated with IL-1beta and autophagy-related signaling in gout. PloS ONE. 2011;6:e29318.

Van Avondt K, Fritsch-Stork R, Derksen RH, Meyaard L. Ligation of signal inhibitory receptor on leukocytes-1 suppresses the release of neutrophil extracellular traps in systemic lupus erythematosus. PloS ONE. 2013;8:e78459.

Brinkmann V, Goosmann C, Kuhn LI, Zychlinsky A. Automatic quantification of in vitro NET formation. Front Immunol. 2012;3:413.

Coelho LP, Pato C, Friaes A, et al. Automatic determination of NET (neutrophil extracellular traps) coverage in fluorescent microscopy images. Bioinformatics. 2015;31:2364-2370.

Fujie K, Shinguh Y, Inamura N, Yasumitsu R, Okamoto M, Okuhara M. Release of neutrophil elastase and its role in tissue injury in acute inflammation: effect of the elastase inhibitor. Eur J Pharmacol. 1999;374:117-125.

Libby LJ, Gelbman BD, Altorki NK, Christos PJ, Libby DM. Surgical lung biopsy in adult respiratory distress syndrome: a meta-analysis. Ann Thorac Surg. 2014;98:1254-1260.

Havemann K, Gramse M. Physiology and pathophysiology of neutral proteinases of human granulocytes. Adv Exp Med Biol. 1984;167:1-20.

Carp H, Miller F, Hoidal JR, Janoff A. Potential mechanism of emphysema: alpha 1-proteinase inhibitor recovered from lungs of cigarette smokers contains oxidized methionine and has decreased elastase inhibitory capacity. Proc Natl Acad Sci U S A. 1982;79:2041-2045.

Janoff A. Elastases and emphysema. Current assessment of the protease-antiprotease hypothesis. Am Rev Respir Dis. 1985;132:417-433.

Cox DW, Levison H. Emphysema of early onset associated with a complete deficiency of alpha-1-antitrypsin (null homozygotes). Am Rev Respir Dis. 1988;137:371-375.

Lee CT, Fein AM, Lippmann M, Holtzman H, Kimbel P, Weinbaum G. Elastolytic activity in pulmonary lavage fluid from patients with adult respiratory-distress syndrome. N Engl J Med. 1981;304:192-196.

McGuire WW, Spragg RG, Cohen AB, Cochrane CG. Studies on the pathogenesis of the adult respiratory distress syndrome. J Clin Invest. 1982;69:543-553.

O'Connor CM, Gaffney K, Keane J, et al. alpha 1-Proteinase inhibitor, elastase activity, and lung disease severity in cystic fibrosis. Am Rev Respir Dis. 1993;148:1665-1670.

Hansen G, Schuster A, Zubrod C, Wahn V. Alpha 1-proteinase inhibitor abrogates proteolytic and secretagogue activity of cystic fibrosis sputum. Respiration. 1995;62:117-124.

Munoz LE, Bilyy R, Biermann MH, et al. Nanoparticles size-dependently initiate self-limiting NETosis-driven inflammation. Proc Natl Acad Sci U S A. 2016;113:E5856-E5865.

Biermann MH, Podolska MJ, Knopf J, et al. Oxidative burst-dependent NETosis is implicated in the resolution of necrosis-associated sterile inflammation. Front Immunol. 2016;7:557.

Bilyy R, Fedorov V, Vovk V, et al. Neutrophil extracellular traps form a barrier between necrotic and viable areas in acute abdominal inflammation. Front Immunol. 2016;7:424.

Kummarapurugu AB, Afosah DK, Sankaranarayanan NV, et al. Molecular principles for heparin oligosaccharide-based inhibition of neutrophil elastase in cystic fibrosis. J Biol Chem. 2018;293:12480-12490.

Papayannopoulos V, Staab D, Zychlinsky A. Neutrophil elastase enhances sputum solubilization in cystic fibrosis patients receiving DNase therapy. PloS ONE. 2011;6:e28526.

Maueroder C, Mahajan A, Paulus S, et al. Menage-a-trois: the ratio of bicarbonate to CO2 and the pH regulate the capacity of neutrophils to form NETs. Front Immunol. 2016;7:583.

Mahajan A, Gruneboom A, Petru L, et al. Frontline Science: aggregated neutrophil extracellular traps prevent inflammation on the neutrophil-rich ocular surface. J Leukoc Biol. 2019;105:1087-1098.

Munoz LE, Boeltz S, Billyy R, et al. Neutrophil extracellular traps initiate gallstone formation. Immunity. 2019. https://doi.org/10.1016/j.immuni.2019.07.002

Brantly ML, Wittes JT, Vogelmeier CF, Hubbard RC, Fells GA, Crystal RG. Use of a highly purified alpha 1-antitrypsin standard to establish ranges for the common normal and deficient alpha 1-antitrypsin phenotypes. Chest. 1991;100:703-708.

Wilson G, O'Leary DJ, Holden BA. Cell content of tears following overnight wear of a contact lens. Curr Eye Res. 1989;8:329-335.

Lay JC, Peden DB, Alexis NE. Flow cytometry of sputum: assessing inflammation and immune response elements in the bronchial airways. Inhal Toxicol. 2011;23:392-406.

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