Diverse stimuli engage different neutrophil extracellular trap pathways

eLife

Volumn 6, Issue , 2017, Pages

  Kenny, Elaine F ^a   Herzig, Alf ^a   Krüger, Renate ^b   Muth, Aaro ^c   Mondal, Santanu ^c   Thompson, Paul R ^c   Brinkmann, Volker ^a   von Bernuth, Horst ^b   Zychlinsky, Arturo ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; CALCIMYCIN; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; DACTINOMYCIN; DNA; HISTONE H3; LACTATE DEHYDROGENASE; LEUKOCYTE ELASTASE; LEUKOCYTE ELASTASE INHIBITOR; MYELOPEROXIDASE; MYELOPEROXIDASE INHIBITOR; NIGERICIN; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; PROTEINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; PHORBOLOL MYRISTATE ACETATE;

ADULT; APOPTOSIS; ARTICLE; BACTERICIDAL ACTIVITY; CANDIDA ALBICANS; CELL DEATH; CELL ISOLATION; CHRONIC GRANULOMATOUS DISEASE; CLINICAL ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR TRAP; GENE MUTATION; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNITY; INFECTION; NECROPTOSIS; NEUTROPHIL; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAINING; STREPTOCOCCUS AGALACTIAE; WESTERN BLOTTING; YOUNG ADULT; ANALOGS AND DERIVATIVES; IMMUNOLOGY; METABOLISM; NORMAL HUMAN; PATHOLOGY; STREPTOCOCCUS;

CALCIMYCIN; CANDIDA ALBICANS; EXTRACELLULAR TRAPS; GRANULOMATOUS DISEASE, CHRONIC; HEALTHY VOLUNTEERS; HUMANS; METABOLIC NETWORKS AND PATHWAYS; NEUTROPHILS; NIGERICIN; STREPTOCOCCUS; TETRADECANOYLPHORBOL ACETATE;

EID: 85023643495     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.24437     Document Type: Article

References (51)

1. Amini P, Stojkov D, Wang X, Wicki S, Kaufmann T, Wong WW, Simon HU, Yousefi S. 2016. NET formation can occur independently of RIPK3 and MLKL signaling. European Journal of Immunology 46:178–184. doi: 10.1002/eji.201545615, PMID: 26549703
2. Amulic B, Cazalet C, Hayes GL, Metzler KD, Zychlinsky A. 2012. Neutrophil function: from mechanisms to disease. Annual Review of Immunology 30:459–489. doi: 10.1146/annurev-immunol-020711-074942, PMID: 22224774
3. Bardoel BW, Kenny EF, Sollberger G, Zychlinsky A. 2014. The balancing act of neutrophils. Cell Host & Microbe 15:526–536. doi: 10.1016/j.chom.2014.04.011, PMID: 24832448
4. Barrientos L, Marin-Esteban V, de Chaisemartin L, Le-Moal VL, Sandré C, Bianchini E, Nicolas V, Pallardy M, Chollet-Martin S. 2013. An improved strategy to recover large fragments of functional human neutrophil extracellular traps. Frontiers in Immunology 4:166. doi: 10.3389/fimmu.2013.00166, PMID: 23805143
5. Brinkmann V, Goosmann C, Kühn LI, Zychlinsky A. 2012. Automatic quantification of in vitro NET formation. Frontiers in Immunology 3:413. doi: 10.3389/fimmu.2012.00413, PMID: 23316198
6. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. 2004. Neutrophil extracellular traps kill Bacteria. Science 303:1532–1535. doi: 10.1126/science.1092385, PMID: 15001782
7. Brinkmann V, Zychlinsky A. 2012. Neutrophil extracellular traps: is immunity the second function of chromatin? The Journal of Cell Biology 198:773–783. doi: 10.1083/jcb.201203170, PMID: 22945932
8. Causey CP, Thompson PR. 2008. An improved synthesis of haloaceteamidine-based inactivators of protein arginine deiminase 4 (PAD4). Tetrahedron Letters 49:4383–4385. doi: 10.1016/j.tetlet.2008.05.021, PMID: 195 87776
9. den Dunnen JT, Antonarakis SE. 2001. Nomenclature for the description of human sequence variations. Human Genetics 109:121–124. doi: 10.1007/s004390100505, PMID: 11479744
10. Desai J, Kumar SV, Mulay SR, Konrad L, Romoli S, Schauer C, Herrmann M, Bilyy R, Müller S, Popper B, Nakazawa D, Weidenbusch M, Thomasova D, Krautwald S, Linkermann A, Anders HJ. 2016. PMA and crystal-induced neutrophil extracellular trap formation involves RIPK1-RIPK3-MLKL signaling. European Journal of Immunology 46:223–229. doi: 10.1002/eji.201545605, PMID: 26531064
11. DeSouza-Vieira T, Guimarães-Costa A, Rochael NC, Lira MN, Nascimento MT, Lima-Gomez PS, Mariante RM, Persechini PM, Saraiva EM. 2016. Neutrophil extracellular traps release induced by Leishmania: role of PI3Kγ, ERK, PI3Ks, PKC, and [Ca2+]. Journal of Leukocyte Biology 100:801–810. doi: 10.1189/jlb.4A0615-261RR, PMID: 27154356
12. Douda DN, Khan MA, Grasemann H, Palaniyar N. 2015. SK3 channel and mitochondrial ROS mediate NADPH oxidase-independent NETosis induced by calcium influx. PNAS 112:2817–2822. doi: 10.1073/pnas. 1414055112, PMID: 25730848
13. Ermert D, Zychlinsky A, Urban C. 2009. Fungal and bacterial killing by neutrophils. Methods in Molecular Biology 470:293–312. doi: 10.1007/978-1-59745-204-5_21, PMID: 19089391
14. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A. 2007. Novel cell death program leads to neutrophil extracellular traps. The Journal of Cell Biology 176:231–241. doi: 10.1083/jcb.200606027, PMID: 17210947
15. Fuchs TA, Brill A, Wagner DD. 2012. Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arteriosclerosis, Thrombosis, and Vascular Biology 32:1777–1783. doi: 10.1161/ATVBAHA.111.242859, PMID: 22652600
16. Fuhrmann J, Clancy KW, Thompson PR. 2015. Chemical biology of protein arginine modifications in epigenetic regulation. Chemical Reviews 115:5413–5461. doi: 10.1021/acs.chemrev.5b00003, PMID: 25970731
17. Gazendam RP, van Hamme JL, Tool AT, Hoogenboezem M, van den Berg JM, Prins JM, Vitkov L, van de Veerdonk FL, van den Berg TK, Roos D, Kuijpers TW. 2016. Human neutrophils use different mechanisms to kill Aspergillus fumigatus conidia and hyphae: evidence from phagocyte defects. The Journal of Immunology 196: 1272–1283. doi: 10.4049/jimmunol.1501811, PMID: 26718340
18. Gennaro R, Pozzan T, Romeo D. 1984. Monitoring of cytosolic free Ca2+ in C5a-stimulated neutrophils: loss of receptor-modulated Ca2+ stores and Ca2+ uptake in granule-free cytoplasts. PNAS 81:1416–1420. doi: 10. 1073/pnas.81.5.1416, PMID: 6324190
19. Ghari F, Quirke AM, Munro S, Kawalkowska J, Picaud S, McGouran J, Subramanian V, Muth A, Williams R, Kessler B, Thompson PR, Fillipakopoulos P, Knapp S, Venables PJ, La Thangue NB. 2016. Citrullination-acetylation interplay guides E2F-1 activity during the inflammatory response. Science Advances 2:e1501257. doi: 10.1126/sciadv.1501257, PMID: 26989780
20. Gray RD, Lucas CD, Mackellar A, Li F, Hiersemenzel K, Haslett C, Davidson DJ, Rossi AG. 2013. Activation of conventional protein kinase C (PKC) is critical in the generation of human neutrophil extracellular traps. Journal of Inflammation 10:12. doi: 10.1186/1476-9255-10-12, PMID: 23514610
21. Gupta AK, Giaglis S, Hasler P, Hahn S. 2014. Efficient neutrophil extracellular trap induction requires mobilization of both intracellular and extracellular calcium pools and is modulated by cyclosporine A. PLoS One 9:e97088. doi: 10.1371/journal.pone.0097088, PMID: 24819773
22. Hakkim A, Fuchs TA, Martinez NE, Hess S, Prinz H, Zychlinsky A, Waldmann H. 2011. Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nature Chemical Biology 7:75–77. doi: 10. 1038/nchembio.496, PMID: 21170021
23. Hakkim A, Fürnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, Herrmann M, Voll RE, Zychlinsky A. 2010. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. PNAS 107:9813– 9818. doi: 10.1073/pnas.0909927107, PMID: 20439745
24. Henriet SS, Verweij PE, Warris A. 2012. Aspergillus nidulans and chronic granulomatous disease: a unique host-pathogen interaction. The Journal of Infectious Diseases 206:1128–1137. doi: 10.1093/infdis/jis473, PMID: 2282 9648
25. Heyworth PG, Cross AR, Curnutte JT. 2003. Chronic granulomatous disease. Current Opinion in Immunology 15: 578–584. doi: 10.1016/S0952-7915(03)00109-2, PMID: 14499268
26. Hosseinzadeh A, Thompson PR, Segal BH, Urban CF. 2016. Nicotine induces neutrophil extracellular traps. Journal of Leukocyte Biology 100:1105–1112. doi: 10.1189/jlb.3AB0815-379RR, PMID: 27312847
27. Jones JE, Slack JL, Fang P, Zhang X, Subramanian V, Causey CP, Coonrod SA, Guo M, Thompson PR. 2012. Synthesis and screening of a haloacetamidine containing library to identify PAD4 selective inhibitors. ACS Chemical Biology 7:160–165. doi: 10.1021/cb200258q, PMID: 22004374
28. Kaplan MJ, Radic M. 2012. Neutrophil extracellular traps: double-edged swords of innate immunity. The Journal of Immunology 189:2689–2695. doi: 10.4049/jimmunol.1201719, PMID: 22956760
29. Kawalkowska J, Quirke AM, Ghari F, Davis S, Subramanian V, Thompson PR, Williams RO, Fischer R, La Thangue NB, Venables PJ. 2016. Abrogation of collagen-induced arthritis by a peptidyl arginine deiminase inhibitor is associated with modulation of T cell-mediated immune responses. Scientific Reports 6:26430. doi: 10.1038/srep26430, PMID: 27210478
30. Kessenbrock K, Krumbholz M, Schönermarck U, Back W, Gross WL, Werb Z, Gröne HJ, Brinkmann V, Jenne DE. 2009. Netting neutrophils in autoimmune small-vessel vasculitis. Nature Medicine 15:623–625. doi: 10.1038/nm.1959, PMID: 19448636
31. Knight JS, Subramanian V, O’Dell AA, Yalavarthi S, Zhao W, Smith CK, Hodgin JB, Thompson PR, Kaplan MJ. 2015. Peptidylarginine deiminase inhibition disrupts NET formation and protects against kidney, skin and vascular disease in lupus-prone MRL/lpr mice. Annals of the Rheumatic Diseases 74:2199–2206. doi: 10.1136/annrheumdis-2014-205365, PMID: 25104775
32. Kolaczkowska E, Kubes P. 2013. Neutrophil recruitment and function in health and inflammation. Nature Reviews Immunology 13:159–175. doi: 10.1038/nri3399, PMID: 23435331
33. Konig MF, Andrade F. 2016. A critical reappraisal of neutrophil extracellular traps and NETosis mimics based on differential requirements for protein citrullination. Frontiers in Immunology 7:461. doi: 10.3389/fimmu.2016. 00461, PMID: 27867381
34. Lewis HD, Liddle J, Coote JE, Atkinson SJ, Barker MD, Bax BD, Bicker KL, Bingham RP, Campbell M, Chen YH, Chung CW, Craggs PD, Davis RP, Eberhard D, Joberty G, Lind KE, Locke K, Maller C, Martinod K, Patten C, et al. 2015. Inhibition of PAD4 activity is sufficient to disrupt mouse and human NET formation. Nature Chemical Biology 11:189–191. doi: 10.1038/nchembio.1735, PMID: 25622091
35. Lood C, Blanco LP, Purmalek MM, Carmona-Rivera C, De Ravin SS, Smith CK, Malech HL, Ledbetter JA, Elkon KB, Kaplan MJ. 2016. Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nature Medicine 22:146–153. doi: 10.1038/nm.4027, PMID: 26779811
36. Losman MJ, Fasy TM, Novick KE, Monestier M. 1992. Monoclonal autoantibodies to subnucleosomes from a MRL/Mp(-)+/+ mouse. Oligoclonality of the antibody response and recognition of a determinant composed of histones H2A, H2B, and DNA. Journal of Immunology 148:1561–1569. PMID: 1371530
37. Macdonald SJ, Dowle MD, Harrison LA, Shah P, Johnson MR, Inglis GG, Clarke GD, Smith RA, Humphreys D, Molloy CR, Amour A, Dixon M, Murkitt G, Godward RE, Padfield T, Skarzynski T, Singh OM, Kumar KA, Fleetwood G, Hodgson ST, et al. 2001. The discovery of a potent, intracellular, orally bioavailable, long duration inhibitor of human neutrophil elastase–GW311616A a development candidate. Bioorganic & Medicinal Chemistry Letters 11:895–898. doi: 10.1016/S0960-894X(01)00078-6, PMID: 11294386
38. Manzenreiter R, Kienberger F, Marcos V, Schilcher K, Krautgartner WD, Obermayer A, Huml M, Stoiber W, Hector A, Griese M, Hannig M, Studnicka M, Vitkov L, Hartl D. 2012. Ultrastructural characterization of cystic fibrosis sputum using atomic force and scanning electron microscopy. Journal of Cystic Fibrosis 11:84–92. doi: 10.1016/j.jcf.2011.09.008, PMID: 21996135
39. Martinod K, Demers M, Fuchs TA, Wong SL, Brill A, Gallant M, Hu J, Wang Y, Wagner DD. 2013. Neutrophil histone modification by peptidylarginine deiminase 4 is critical for deep vein thrombosis in mice. PNAS 110: 8674–8679. doi: 10.1073/pnas.1301059110, PMID: 23650392
40. Metzler KD, Goosmann C, Lubojemska A, Zychlinsky A, Papayannopoulos V. 2014. A myeloperoxidase-containing complex regulates neutrophil elastase release and actin dynamics during NETosis. Cell Reports 8: 883–896. doi: 10.1016/j.celrep.2014.06.044, PMID: 25066128
41. Neeli I, Radic M. 2013. Opposition between PKC isoforms regulates histone deimination and neutrophil extracellular chromatin release. Frontiers in Immunology 4:38. doi: 10.3389/fimmu.2013.00038, PMID: 23430 963
42. Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. 2010. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. The Journal of Cell Biology 191:677–691. doi: 10.1083/jcb.201006052, PMID: 20974816
43. Remijsen Q, Kuijpers TW, Wirawan E, Lippens S, Vandenabeele P, Vanden Berghe T. 2011a. Dying for a cause: netosis, mechanisms behind an antimicrobial cell death modality. Cell Death and Differentiation 18:581–588. doi: 10.1038/cdd.2011.1, PMID: 21293492
44. Remijsen Q, Vanden Berghe T, Wirawan E, Asselbergh B, Parthoens E, De Rycke R, Noppen S, Delforge M, Willems J, Vandenabeele P. 2011b. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Research 21:290–304. doi: 10.1038/cr.2010.150, PMID: 21060338
45. Rochael NC, Guimarães-Costa AB, Nascimento MT, DeSouza-Vieira TS, Oliveira MP, Garcia e Souza LF, Oliveira MF, Saraiva EM. 2015. Classical ROS-dependent and early/rapid ROS-independent release of neutrophil extracellular traps triggered by Leishmania parasites. Scientific Reports 5:18302. doi: 10.1038/srep18302, PMID: 26673780
46. Scapini P, Cassatella MA. 2014. Social networking of human neutrophils within the immune system. Blood 124: 710–719. doi: 10.1182/blood-2014-03-453217, PMID: 24923297
47. Sollberger G, Amulic B, Zychlinsky A. 2016. Neutrophil extracellular trap formation is Independent of De Novo Gene expression. PLoS One 11:e0157454. doi: 10.1371/journal.pone.0157454, PMID: 27310721
48. Tran TM, MacIntyre A, Hawes M, Allen C. 2016. Escaping underground nets: extracellular DNases degrade plant extracellular traps and contribute to virulence of the plant pathogenic bacterium Ralstonia solanacearum. PLOS Pathogens 12:e1005686. doi: 10.1371/journal.ppat.1005686, PMID: 27336156
49. van Venrooij WJ, Vossenaar ER, Zendman AJ. 2004. Anti-CCP antibodies: the new rheumatoid factor in the serology of rheumatoid arthritis. Autoimmunity Reviews 3 Suppl 1:S17–19. PMID: 15309772
50. Virreira Winter S, Zychlinsky A, Bardoel BW. 2016. Genome-wide CRISPR screen reveals novel host factors required for Staphylococcus aureus α-hemolysin-mediated toxicity. Scientific Reports 6:24242. doi: 10.1038/srep24242, PMID: 27066838
51. Yaron JR, Gangaraju S, Rao MY, Kong X, Zhang L, Su F, Tian Y, Glenn HL, Meldrum DR. 2015. K(+) regulates ca(2 +) to drive inflammasome signaling: dynamic visualization of ion flux in live cells. Cell Death and Disease 6: e1954. doi: 10.1038/cddis.2015.277, PMID: 26512962