NETosing neutrophils activate complement both on their own NETs and bacteria via alternative and non-alternative pathways

Frontiers in Immunology

Volumn 7, Issue APR, 2016, Pages

  Yuen, Joshua ^a,b   Pluthero, Fred G ^a,c   Douda, David N ^a,b   Riedl, Magdalena ^a   Cherry, Ahmed ^a   Ulanova, Marina ^d   Kahr, Walter H A ^a,b,c,d,e   Palaniyar, Nades ^a,b   Licht, Christoph ^a,b,c,e  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d LAKEHEAD UNIVERSITY   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Alternative pathway; Complement system; NETosis; Neutrophil extracellular traps; Properdin; Pseudomonas aeruginosa

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5B; COMPLEMENT FACTOR; COMPLEMENT MEMBRANE ATTACK COMPLEX; DNA; FORMYLMETHIONYLLEUCYLPHENYLALANINE; NEPHRITIC FACTOR; PHORBOL 13 ACETATE 12 MYRISTATE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; BACTERIUM; BACTERIUM CULTURE; CELL ISOLATION; CELL LYSATE; COLOCALIZATION ANALYSIS; COMPLEMENT ALTERNATIVE PATHWAY; CONFOCAL MICROSCOPY; EXTRACELLULAR TRAP; HUMAN; HUMAN CELL; LEUKOCYTE ACTIVATION; MICROPLATE READER; NEUTROPHIL; NONHUMAN; NORMAL HUMAN; PSEUDOMONAS AERUGINOSA; RESPIRATORY BURST; SPINNING DISK CONFOCAL MICROSCOPY; SYTOX GREEN PLATE READER ASSAY; WESTERN BLOTTING;

EID: 84966709074     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00137     Document Type: Article

References (42)

1. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol (2013) 13:159-75. doi: 10.1038/nri3399
2. Nauseef WM, Borregaard N. Neutrophils at work. Nat Immunol (2014) 15:602-11. doi:10.1038/ni.2921
3. 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. doi:10.1371/journal.ppat.1000639
4. Cheng OZ, Palaniyar N. NET balancing: a problem in inflammatory lung diseases. Front Immunol (2013) 4:1. doi:10.3389/fimmu.2013.00001
5. Zawrotniak M, Rapala-Kozik M. Neutrophil extracellular traps (NETs)-formation and implications. Acta Biochim Pol (2013) 60:277-84
6. 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) 176:231-41. doi:10.1083/jcb.200606027
7. Douda DN, Yip L, Khan MA, Grasemann H, Palaniyar N. Akt is essential to induce NADPH-dependent NETosis and to switch the neutrophil death to apoptosis. Blood (2014) 123:597-600. doi:10.1182/blood-2013-09-526707
8. Douda DN, Grasemann H, Pace-Asciak C, Palaniyar N. A lipid mediator hepoxilin A3 is a natural inducer of neutrophil extracellular traps in human neutrophils. Mediators Inflamm (2015) 2015:520871. doi:10.1155/2015/520871
9. Douda DN, Khan MA, Grasemann H, Palaniyar N. SK3 channel and mitochondrial ROS mediate NADPH oxidase-independent NETosis induced by calcium influx. Proc Natl Acad Sci U S A (2015) 112:2817-22. doi:10.1073/pnas.1414055112
10. Yousefi S, Mihalache C, Kozlowski E, Schmid I, Simon HU. Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ (2009) 16:1438-44. doi:10.1038/cdd.2009.96
11. Papayannopoulos V, Zychlinsky A. NETs: a new strategy for using old weapons. Trends Immunol (2009) 30:513-21. doi:10.1016/j.it.2009.07.011
12. 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) 13:463-9. doi:10.1038/nm1565
13. Kessenbrock K, Krumbholz M, Schonermarck U, Back W, Gross WL, Werb Z, et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med (2009) 15:623-5. doi:10.1038/nm.1959
14. 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 U S A (2010) 107:9813-8. doi:10.1073/pnas.0909927107
15. Douda DN, Jackson R, Grasemann H, Palaniyar N. Innate immune collectin surfactant protein D simultaneously binds both neutrophil extracellular traps and carbohydrate ligands and promotes bacterial trapping. J Immunol (2011) 187:1856-65. doi:10.4049/jimmunol.1004201
16. Villanueva E, Yalavarthi S, Berthier CC, Hodgin JB, Khandpur R, Lin AM, et al. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol (2011) 187:538-52. doi:10.4049/jimmunol.1100450
17. Kaplan MJ, Radic M. Neutrophil extracellular traps: double-edged swords of innate immunity. J Immunol (2012) 189:2689-95. doi:10.4049/jimmunol.1201719
18. Bellac CL, Dufour A, Krisinger MJ, Loonchanta A, Starr AE, Auf Dem Keller U, et al. Macrophage matrix metalloproteinase-12 dampens inflammation and neutrophil influx in arthritis. Cell Rep (2014) 9:618-32. doi:10.1016/j.celrep.2014.09.006
19. Jin L, Batra S, Douda DN, Palaniyar N, Jeyaseelan S. CXCL1 contributes to host defense in polymicrobial sepsis via modulating T cell and neutrophil functions. J Immunol (2014) 193:3549-58. doi:10.4049/jimmunol.1401138
20. Muller S, Radic M. Citrullinated autoantigens: from diagnostic markers to pathogenetic mechanisms. Clin Rev Allergy Immunol (2014) 49:232-9. doi:10.1007/s12016-014-8459-2
21. Riedl M, Fakhouri F, Le Quintrec M, Noone DG, Jungraithmayr TC, Fremeaux-Bacchi V, et al. Spectrum of complement-mediated thrombotic microangiopathies: pathogenetic insights identifying novel treatment approaches. Semin Thromb Hemost (2014) 40:444-64. doi:10.1055/s-0034-1376153
22. Grayson PC, Kaplan MJ. At the bench: neutrophil extracellular traps (NETs) highlight novel aspects of innate immune system involvement in autoimmune diseases. J Leukoc Biol (2015) 99(2):253-64. doi:10.1189/jlb.5BT0615-247R
23. Palaniyar N, Mall MA, Taube C, Worgall S, Grasemann H. New developments in cystic fibrosis airway inflammation. Mediators Inflamm (2015) 2015:769425. doi:10.1155/2015/769425
24. Yildiz C, Palaniyar N, Otulakowski G, Khan MA, Post M, Kuebler WM, et al. Mechanical ventilation induces neutrophil extracellular trap formation. Anesthesiology (2015) 122:864-75. doi:10.1097/ALN.0000000000000605
25. Wang H, Wang C, Zhao MH, Chen M. Neutrophil extracellular traps can activate alternative complement pathways. Clin Exp Immunol (2015) 181:518-27. doi:10.1111/cei.12654
26. Noris M, Remuzzi G. Overview of complement activation and regulation. Semin Nephrol (2013) 33:479-92. doi:10.1016/j.semnephrol.2013.08.001
27. Cortes C, Ohtola JA, Saggu G, Ferreira VP. Local release of properdin in the cellular microenvironment: role in pattern recognition and amplification of the alternative pathway of complement. Front Immunol (2012) 3:412. doi:10.3389/fimmu.2012.00412
28. Young RL, Malcolm KC, Kret JE, Caceres SM, Poch KR, Nichols DP, et al. Neutrophil extracellular trap (NET)-mediated killing of Pseudomonas aeruginosa: evidence of acquired resistance within the CF airway, independent of CFTR. PLoS One (2011) 6:e23637. doi:10.1371/journal.pone.0023637
29. Khatua B, Bhattacharya K, Mandal C. Sialoglycoproteins adsorbed by Pseudomonas aeruginosa facilitate their survival by impeding neutrophil extracellular trap through siglec-9. J Leukoc Biol (2012) 91:641-55. doi:10.1189/jlb.0511260
30. Shan Q, Dwyer M, Rahman S, Gadjeva M. Distinct susceptibilities of corneal Pseudomonas aeruginosa clinical isolates to neutrophil extracellular trap-mediated immunity. Infect Immun (2014) 82:4135-43. doi:10.1128/IAI.02169-14
31. Cote O, Clark ME, Viel L, Labbe G, Seah SY, Khan MA, et al. Secretoglobin 1A1 and 1A1A differentially regulate neutrophil reactive oxygen species production, phagocytosis and extracellular trap formation. PLoS One (2014) 9:e96217. doi:10.1371/journal.pone.0096217
32. Heinen S, Pluthero FG, Van Eimeren VF, Quaggin SE, Licht C. Monitoring and modeling treatment of atypical hemolytic uremic syndrome. Mol Immunol (2013) 54:84-8. doi:10.1016/j.molimm.2012.10.044
33. Fuchs TA, Kremer Hovinga JA, Schatzberg D, Wagner DD, Lammle B. Circulating DNA and myeloperoxidase indicate disease activity in patients with thrombotic microangiopathies. Blood (2012) 120:1157-64. doi:10.1182/blood-2012-02-412197
34. Schwaeble WJ, Reid KB. Does properdin crosslink the cellular and the humoral immune response? Immunol Today (1999) 20:17-21. doi:10.1016/S0167-5699(98)01376-0
35. Kemper C, Hourcade DE. Properdin: new roles in pattern recognition and target clearance. Mol Immunol (2008) 45:4048-56. doi:10.1016/j.molimm.2008.06.034
36. Camous L, Roumenina L, Bigot S, Brachemi S, Fremeaux-Bacchi V, Lesavre P, et al. Complement alternative pathway acts as a positive feedback amplification of neutrophil activation. Blood (2010) 117:1340-9. doi:10.1182/blood-2010-05-283564
37. O'Flynn J, Dixon KO, Faber Krol MC, Daha MR, Van Kooten C. Myeloperoxidase directs properdin-mediated complement activation. J Innate Immun (2013) 6:417-25. doi:10.1159/000356980
38. Gupta-Bansal R, Parent JB, Brunden KR. Inhibition of complement alternative pathway function with anti-properdin monoclonal antibodies. Mol Immunol (2000) 37:191-201. doi:10.1016/S0161-5890(00)00047-X
39. Leffler J, Martin M, Gullstrand B, Tyden H, Lood C, Truedsson L, et al. Neutrophil extracellular traps that are not degraded in systemic lupus erythematosus activate complement exacerbating the disease. J Immunol (2012) 188:3522-31. doi:10.4049/jimmunol.1102404
40. Farrera C, Fadeel B. Macrophage clearance of neutrophil extracellular traps is a silent process. J Immunol (2013) 191:2647-56. doi:10.4049/jimmunol.1300436
41. Rother RP, Rollins SA, Mojcik CF, Brodsky RA, Bell L. Discovery and development of the complement inhibitor eculizumab for the treatment of paroxysmal nocturnal hemoglobinuria. Nat Biotechnol (2007) 25:1256-64. doi:10.1038/nbt1207-1488c
42. Legendre CM, Licht C, Muus P, Greenbaum LA, Babu S, Bedrosian C, et al. Terminal complement inhibitor eculizumab in atypical hemolytic-uremic syndrome. N Engl J Med (2013) 368:2169-81. doi:10.1056/NEJMoa1208981