Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps
Abstract
Neutrophil extracellular traps (NETs) represent extracellular structures able to bind and kill microorganisms. It is believed that they are generated by neutrophils undergoing cell death, allowing these dying or dead cells to kill microbes. We show that, following priming with granulocyte/macrophage colony-stimulating factor (GM-CSF) and subsequent short-term toll-like receptor 4 (TLR4) or complement factor 5a (C5a) receptor stimulation, viable neutrophils are able to generate NETs. Strikingly, NETs formed by living cells contain mitochondrial, but no nuclear, DNA. Pharmacological or genetic approaches to block reactive oxygen species (ROS) production suggested that NET formation is ROS dependent. Moreover, neutrophil populations stimulated with GM-CSF and C5a showed increased survival compared with resting neutrophils, which did not generate NETs. In conclusion, mitochondrial DNA release by neutrophils and NET formation do not require neutrophil death and do also not limit the lifespan of these cells.
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Different cellular lineages may extrude their mitochondria upon activation.
“Different cellular lineages (10–18) may extrude their mitochondria upon activation.”
From Autoantibodies in Systemic Lupus Erythematosus Target Mitochondrial RNA (2019) · cites this paper as [10]
Various activated cells and damaged tissues release extracellular mitochondria.
“Various cellular lineages are capable of extruding their mitochondria. Activated mast cells10, T-cells11, eosinophils12, hepatocytes13, neutrophils14–16 and platelets17,18, in addition to damaged organs or tissues7,13,19,20, release extracellular mitochondria.”
From Anti-mitochondrial autoantibodies in systemic lupus erythematosus and their association with disease manifestations (2019) · cites this paper as [14]
During immune response, neutrophils utilize mtDNA as a structural molecule to bind cytotoxic proteins into neutrophil extracellular traps (NETs), which are then released onto advancing plaque biofilms.
“during immune response, neutrophils utilize mtDNA as a structural molecule to bind cytotoxic proteins into neutrophil extracellular traps (NETs), which are then released onto advancing plaque biofilms (Yousefi et al., 2009)”
From Successful enrichment and recovery of whole mitochondrial genomes from ancient human dental calculus (2016) · cites this paper as Yousefi et al., 2009
A considerable fraction of nucleic acids contained in NETs is of mitochondrial rather than nuclear origin.
“Several reports demonstrate that a considerable fraction of the nucleic acids contained in NETs is of mitochondrial, rather than nuclear, origin [724–728].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [724]
Both NETotic cell death and NET extrusion in the absence of RCD rely on activity of NADPH oxidases.
“both NETotic cell death and NET extrusion in the absence of RCD appears to rely on the activity of NADPH oxidases [724, 736, 737].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [724]
NET extrusion per se does not necessarily result in cellular lysis.
“NET extrusion per se does not necessarily result in cellular lysis [722, 724, 735].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [724]
Cites
Neutrophil Extracellular Traps Kill Bacteria
Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y., & Zychlinsky, A. (2004) · Science · doi:10.1126/science.1092385 · Cited by 10,268 · see citing works
Novel cell death program leads to neutrophil extracellular traps
Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., Weinrauch, Y., Brinkmann, V., & Zychlinsky, A. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200606027 · Cited by 3,197 · see citing works
Neutrophils and immunity: challenges and opportunities
Nathan, C. (2006) · Nature reviews. Immunology · doi:10.1038/nri1785 · Cited by 2,971 · see citing works
Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood
Clark, S. R., Ma, A. C., Tavener, S. A., McDonald, B., Goodarzi, Z., Kelly, M. M., Patel, K. D., Chakrabarti, S., McAvoy, E., Sinclair, G. D., et al. (2007) · Nature Medicine · doi:10.1038/nm1565 · Cited by 2,309 · see citing works
Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis
Yousefi, S., Perozzo, R., Schmid, I., Ziemiecki, A., Schaffner, T. J., Scapozza, L., Brunner, T., & Simon, H. (2006) · Nature Cell Biology · doi:10.1038/ncb1482 · Cited by 1,300 · see citing works
Self-citationCatapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense
Yousefi, S., Gold, J. A., Andina, N., Lee, J. J., Kelly, A. M., Kozlowski, E., Schmid, I., Straumann, A., Reichenbach, J., Gleich, G. J., et al. (2008) · Nature Medicine · doi:10.1038/nm.1855 · Cited by 967 · see citing works
Self-citationBeneficial suicide: why neutrophils die to make NETs
Brinkmann, V., & Zychlinsky, A. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1710 · Cited by 937 · see citing works
Selective fluorescent imaging of superoxide <i>in vivo</i> using ethidium-based probes
Robinson, K. M., Janes, M. S., Pehar, M., Monette, J. S., Ross, M. F., Hagen, T. M., Murphy, M. P., & Beckman, J. S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601945103 · Cited by 777 · see citing works
von Köckritz‐Blickwede, M., Goldmann, O., Thulin, P., Heinemann, K., Norrby‐Teglund, A., Rohde, M., & Medina, E. (2008) · Blood · doi:10.1182/blood-2007-07-104018 · Cited by 553 · see citing works
Gupta, A. K., Hasler, P., Holzgreve, W., Gebhardt, G., & Hahn, S. (2005) · Human Immunology · doi:10.1016/j.humimm.2005.11.003 · Cited by 403 · see citing works
Neutrophil apoptosis pathways and their modifications in inflammation
Simon, H. (2003) · Immunological Reviews · doi:10.1034/j.1600-065x.2003.00038.x · Cited by 350 · see citing works
Self-citationMartinelli, S., Urosevic, M., Daryadel, A., Oberholzer, P. A., Baumann, C. K., Fey, M. F., Dummer, R., Simon, H., & Yousefi, S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405883200 · Cited by 294 · see citing works
Self-citationConus, S., Perozzo, R., Reinheckel, T., Peters, C., Scapozza, L., Yousefi, S., & Simon, H. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20072152 · Cited by 262 · see citing works
Self-citationvon Gunten, S., Yousefi, S., Seitz, M., Jakob, S. M., Schaffner, T. J., Seger, R. A., Takala, J. A., Villiger, P. M., & Simon, H. (2005) · Blood · doi:10.1182/blood-2004-10-4112 · Cited by 217 · see citing works
Self-citationvon Gunten, S., Schaub, A., Vogel, M., Stadler, B. M., Miescher, S., & Simon, H. (2006) · Blood · doi:10.1182/blood-2006-05-021568 · Cited by 135 · see citing works
Self-citationNeutrophil apoptosis mediated by nicotinic acid receptors (GPR109A)
Kostylina, G., Simon, D., Fey, M. F., Yousefi, S., & Simon, H. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402238 · Cited by 119 · see citing works
Self-citationFungal and Bacterial Killing by Neutrophils
Ermert, D., Zychlinsky, A., & Urban, C. F. (2008) · Methods in molecular biology · doi:10.1007/978-1-59745-204-5_21 · Cited by 83 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Galluzzi, L., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Agostinis, P., Alnemri, E. S., Altucci, L., Amelio, I., Andrews, D. W., et al. (2018) · Cell Death & Differentiation · doi:10.1038/s41418-017-0012-4 · Cited by 6,680 · see citing works
Neutrophils in the activation and regulation of innate and adaptive immunity
Mantovani, A., Cassatella, M. A., Costantini, C., & Jaillon, S. (2011) · Nature reviews. Immunology · doi:10.1038/nri3024 · Cited by 3,044 · see citing works
Extracellular DNA traps promote thrombosis
Fuchs, T. A., Brill, A. G., Duerschmied, D., Schatzberg, D., Monestier, M., Myers, D. D., Wrobleski, S. K., Wakefield, T. W., Hartwig, J. H., & Wagner, D. D. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005743107 · Cited by 2,517 · see citing works
Galluzzi, L., Vitale, I., Abrams, J. M., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., Dawson, T. M., Dawson, V. L., El-Deiry, W. S., Fulda, S., et al. (2012) · Cell Death & Differentiation · doi:10.1038/cdd.2011.96 · Cited by 2,421 · see citing works
Self-citationNeutrophils, from marrow to microbes.
Borregaard, N. (2010) · Immunity · doi:10.1016/j.immuni.2010.11.011 · Cited by 1,550 · see citing works
Khandpur, R., Carmona‐Rivera, C., Vivekanandan‐Giri, A., Gizinski, A. M., Yalavarthi, S., Knight, J. S., Friday, S. C., Li, S., Patel, R. M., Subramanian, V., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005580 · Cited by 1,342 · see citing works
An emerging role for neutrophil extracellular traps in noninfectious disease
Jorch, S. K., & Kubes, P. (2017) · Nature Medicine · doi:10.1038/nm.4294 · Cited by 1,244 · see citing works
The Neutrophil's Role During Health and Disease.
Liew, P., & Kubes, P. (2019) · Physiological Reviews · doi:10.1152/physrev.00012.2018 · Cited by 1,032 · see citing works
Neutrophil Extracellular Traps: Double-Edged Swords of Innate Immunity
Kaplan, M. J., & Radic, M. Z. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1201719 · Cited by 1,168 · see citing works
Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo
Yipp, B. G., Petri, B., Salina, D., Jenne, C. N., Scott, B. N. V., Zbytnuik, L. D., Pittman, K., Asaduzzaman, M., Wu, K., Meijndert, H. C., et al. (2012) · Nature Medicine · doi:10.1038/nm.2847 · Cited by 1,169 · see citing works
Pilsczek, F. H., Salina, D., Poon, K. K. H., Fahey, C., Yipp, B. G., Sibley, C. D., Robbins, S. M., Green, F. H. Y., Surette, M. G., Sugai, M., et al. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1000675 · Cited by 1,114 · see citing works
Neutrophil extracellular traps: Is immunity the second function of chromatin?
Brinkmann, V., & Zychlinsky, A. (2012) · Journal of Cell Biology · doi:10.1083/jcb.201203170 · Cited by 1,021 · see citing works
Yipp, B. G., & Kubes, P. (2013) · Blood · doi:10.1182/blood-2013-04-457671 · Cited by 998 · see citing works
Demers, M., Krause, D. S., Schatzberg, D., Martinod, K., Voorhees, J. R., Fuchs, T. A., Scadden, D. T., & Wagner, D. D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200419109 · Cited by 883 · see citing works
Mitochondrial DNA in inflammation and immunity
Riley, J. S., & Tait, S. W. G. (2020) · EMBO Reports · doi:10.15252/embr.201949799 · Cited by 876 · see citing works
Neutrophil extracellular trap cell death requires both autophagy and superoxide generation
Remijsen, Q., Berghe, T. V., Wirawan, E., Asselbergh, B., Parthoens, E., De Rycke, R., Noppen, S., Delforge, M., Willems, J., & Vandenabeele, P. (2011) · Cell Research · doi:10.1038/cr.2010.150 · Cited by 818 · see citing works
Teijeira, Á., Garasa, S., Gato, M., Alfaro, C., Miguéliz, I., Cirella, A., de Andrea, C., Ochoa, M. C., Otano, I., Etxeberría, I., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.03.001 · Cited by 799 · see citing works
Neutrophils and NETS in modulating acute and chronic inflammation
Castanheira, F. V. S., & Kubes, P. (2019) · Blood · doi:10.1182/blood-2018-11-844530 · Cited by 792 · see citing works
The neutrophil in vascular inflammation
Phillipson, M., & Kubes, P. (2011) · Nature Medicine · doi:10.1038/nm.2514 · Cited by 766 · see citing works
Neutrophil Extracellular Traps Mediate a Host Defense Response to Human Immunodeficiency Virus-1
Saitoh, T., Komano, J. A., Saitoh, Y., Misawa, T., Takahama, M., Kozaki, T., Uehata, T., Iwasaki, H., Omori, H., Yamaoka, S., et al. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.05.015 · Cited by 731 · see citing works
Neutrophil Extracellular Traps and Its Implications in Inflammation: An Overview
Delgado‐Rizo, V., Martinez-Guzman, M. A., Íñiguez-Gutiérrez, L., García-Orozco, A., Alvarado‐Navarro, A., & Fafutis‐Morris, M. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00081 · Cited by 688 · see citing works
Neutrophils: Between Host Defence, Immune Modulation, and Tissue Injury
Krüger, P., Saffarzadeh, M., Weber, A. N. R., Rieber, N. P., Radsak, M. P., von Bernuth, H., Benarafa, C., Roos, D., Skokowa, J., & Hartl, D. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004651 · Cited by 663 · see citing works
Denning, N., Aziz, M., Gurien, S. D., & Wang, P. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02536 · Cited by 632 · see citing works
Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality
Remijsen, Q., Kuijpers, T. W., Wirawan, E., Lippens, S., Vandenabeele, P., & Berghe, T. V. (2011) · Cell Death and Differentiation · doi:10.1038/cdd.2011.1 · Cited by 612 · see citing works
The multifactorial role of neutrophils in rheumatoid arthritis
Wright, H. L., Moots, R. J., & Edwards, S. W. (2014) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2014.80 · Cited by 591 · see citing works
Neutrophil Extracellular Trap (NET) Impact on Deep Vein Thrombosis
Fuchs, T. A., Brill, A. G., & Wagner, D. D. (2012) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.111.242859 · Cited by 587 · see citing works
Neutrophil Extracellular Traps in Atherosclerosis and Atherothrombosis
Döring, Y., Soehnlein, O., & Weber, C. (2017) · Circulation Research · doi:10.1161/circresaha.116.309692 · Cited by 579 · see citing works
Are Reactive Oxygen Species Always Detrimental to Pathogens?
Paiva, C. N., & Bozza, M. T. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5447 · Cited by 559 · see citing works
NETosis: Molecular Mechanisms, Role in Physiology and Pathology
Vorobjeva, N. V., & Chernyak, B. V. (2020) · Biochemistry (Moscow) · doi:10.1134/s0006297920100065 · Cited by 559 · see citing works
Iba, T., & Levy, J. H. (2017) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.13911 · Cited by 556 · see citing works
Selders, G. S., Fetz, A. E., Radic, M. Z., & Bowlin, G. L. (2017) · Regenerative Biomaterials · doi:10.1093/rb/rbw041 · Cited by 538 · see citing works
Neutrophil extracellular traps — the dark side of neutrophils
Sørensen, O. E., & Borregaard, N. (2016) · Journal of Clinical Investigation · doi:10.1172/jci84538 · Cited by 532 · see citing works
Caielli, S., Athale, S., Domic, B., Murat, E., Chandra, M., Banchereau, R., Baisch, J., Phelps, K., Clayton, S., Gong, M., et al. (2016) · Journal of Experimental Medicine · doi:10.1084/jem.20151876 · Cited by 501 · see citing works
NET balancing: a problem in inflammatory lung diseases
Cheng, O. Z., & Palaniyar, N. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00001 · Cited by 453 · see citing works
Neutrophil Apoptosis: Relevance to the Innate Immune Response and Inflammatory Disease
Fox, S., Leitch, A. E., Duffin, R., Haslett, C., & Rossi, A. G. (2010) · Journal of Innate Immunity · doi:10.1159/000284367 · Cited by 441 · see citing works
Boeltz, S., Amini, P., Anders, H., Andrade, F., Bilyy, R. O., Chatfield, S. M., Cichoń, I., Clancy, D. M., Desai, J., Dumych, T. I., et al. (2019) · Cell Death and Differentiation · doi:10.1038/s41418-018-0261-x · Cited by 439 · see citing works
Self-citationThe role of neutrophils and NETosis in autoimmune and renal diseases
Gupta, S., & Kaplan, M. J. (2016) · Nature Reviews Nephrology · doi:10.1038/nrneph.2016.71 · Cited by 433 · see citing works
Parker, H., Dragunow, M., Hampton, M. B., Kettle, A. J., & Winterbourn, C. C. (2012) · Journal of Leukocyte Biology · doi:10.1189/jlb.1211601 · Cited by 430 · see citing works
Neutrophil, neutrophil extracellular traps and endothelial cell dysfunction in sepsis
Zhang, H., Wang, Y., Qu, M., Li, W., Wu, D., Cata, J. P., & Miao, C. (2023) · Clinical and Translational Medicine · doi:10.1002/ctm2.1170 · Cited by 429 · see citing works
Neutrophil Extracellular Traps
Thålin, C., Hisada, Y., Lundström, S., Mackman, N., & Wallén, H. (2019) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.119.312463 · Cited by 408 · see citing works
Todkar, K., Chikhi, L., Desjardins, V., El-Mortada, F., Pépin, G., & Germain, M. (2021) · Nature Communications · doi:10.1038/s41467-021-21984-w · Cited by 382 · see citing works
The Roles of Mitochondrial Damage-Associated Molecular Patterns in Diseases
Nakahira, K., Hisata, S., & Choi, A. M. K. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2015.6407 · Cited by 363 · see citing works
Heme-induced neutrophil extracellular traps contribute to the pathogenesis of sickle cell disease
Chen, G., Zhang, D., Fuchs, T. A., Manwani, D., Wagner, D. D., & Frenette, P. S. (2014) · Blood · doi:10.1182/blood-2013-10-529982 · Cited by 354 · see citing works
Neutrophil clearance: when the party is over, clean-up begins
Bratton, D. L., & Henson, P. M. (2011) · Trends in Immunology · doi:10.1016/j.it.2011.04.009 · Cited by 350 · see citing works
The Role of Macrophages in Staphylococcus aureus Infection
Pidwill, G. R., Gibson, J. F., Cole, J., Renshaw, S. A., & Foster, S. J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.620339 · Cited by 341 · see citing works
Parker, H. A., Albrett, A. M., Kettle, A. J., & Winterbourn, C. C. (2011) · Journal of Leukocyte Biology · doi:10.1189/jlb.0711387 · Cited by 342 · see citing works
Neutrophil phenotypes and functions in cancer: A consensus statement
Quail, D. F., Amulic, B., Aziz, M., Barnes, B. J., Eruslanov, E. B., Fridlender, Z. G., Goodridge, H. S., Granot, Z., Hidalgo, A., Huttenlocher, A., et al. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20220011 · Cited by 336 · see citing works
Tumor-Associated Neutrophils in Cancer: Going Pro
Wu, L., Saxena, S., Awaji, M. I., & Singh, R. K. (2019) · Cancers · doi:10.3390/cancers11040564 · Cited by 338 · see citing works
Neutrophil Extracellular Trap Formation: Physiology, Pathology, and Pharmacology
Ravindran, M., Khan, M. A., & Palaniyar, N. (2019) · Biomolecules · doi:10.3390/biom9080365 · Cited by 328 · see citing works
Wang, H., Li, T., Chen, S., Gu, Y., & Ye, S. (2015) · Arthritis & Rheumatology · doi:10.1002/art.39296 · Cited by 325 · see citing works
Neutrophil Extracellular Traps in the Second Decade
Brinkmann, V. (2018) · Journal of Innate Immunity · doi:10.1159/000489829 · Cited by 315 · see citing works
Hamilton, J. A. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20190945 · Cited by 310 · see citing works
Patients with COVID-19: in the dark-NETs of neutrophils
Ackermann, M., Anders, H., Bilyy, R. O., Bowlin, G. L., Daniel, C., LORENZO, R. D., Egeblad, M., Henneck, T., Hidalgo, A., Hoffmann, M. H., et al. (2021) · Cell Death and Differentiation · doi:10.1038/s41418-021-00805-z · Cited by 307 · see citing works
Self-citationPeculiarities of cell death mechanisms in neutrophils
Geering, B., & Simon, H.-U. (2011) · Cell Death and Differentiation · doi:10.1038/cdd.2011.75 · Cited by 301 · see citing works
Self-citationHydrogen sulfide: An endogenous regulator of the immune system
Dilek, N., Papapetropoulos, A., Toliver-Kinsky, T. E., & Szabó, C. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.105119 · Cited by 293 · see citing works
Neutrophils in innate and adaptive immunity
Jaillon, S., Galdiero, M. R., Prete, D. D., Cassatella, M. A., Garlanda, C., & Mantovani, A. (2013) · Seminars in Immunopathology · doi:10.1007/s00281-013-0374-8 · Cited by 284 · see citing works
Keshari, R. S., Verma, A. R., Barthwal, M. K., & Dikshit, M. (2012) · Journal of Cellular Biochemistry · doi:10.1002/jcb.24391 · Cited by 283 · see citing works
Mitochondria as central hub of the immune system
Breda, C. N. D. S., Davanzo, G. G., Basso, P. J., Câmara, N. O. S., & Moraes‐Vieira, P. M. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101255 · Cited by 280 · see citing works
Neutrophil Extracellular Traps Go Viral
Schönrich, G., & Raftery, M. J. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00366 · Cited by 277 · see citing works
The role of platelets in mediating a response to human influenza infection
Koupenova, M., Corkrey, H. A., Vitseva, O. I., Manni, G., Pang, C. J., Clancy, L., Yao, C., Rade, J. J., Levy, D. A., Wang, J. P., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09607-x · Cited by 277 · see citing works
Extracellular DNA, Neutrophil Extracellular Traps, and Inflammasome Activation in Severe Asthma
Lachowicz-Scroggins, M. E., Dunican, E. M., Charbit, A. R., Raymond, W. W., Looney, M. R., Peters, M. C., Gordon, E. D., Woodruff, P. G., Lefrançais, E., Phillips, B. R., et al. (2019) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201810-1869oc · Cited by 275 · see citing works
Eosinophil and neutrophil extracellular DNA traps in human allergic asthmatic airways
Dworski, R., Simon, H., Hoskins, A., & Yousefi, S. (2011) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2010.12.1103 · Cited by 266 · see citing works
Self-citationKey mechanisms governing resolution of lung inflammation
Robb, C. T., Regan, K., Dorward, D. A., & Rossi, A. G. (2016) · Seminars in Immunopathology · doi:10.1007/s00281-016-0560-6 · Cited by 263 · see citing works
Targeting GM-CSF in inflammatory diseases
Wicks, I. P., & Roberts, A. W. (2015) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2015.161 · Cited by 261 · see citing works
Living and dying for inflammation: neutrophils, eosinophils, basophils
Geering, B., Stoeckle, C., Conus, S., & Simon, H. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.04.002 · Cited by 257 · see citing works
Self-citationMacrophage Extracellular Traps: A Scoping Review
Doster, R. S., Rogers, L. M., Gaddy, J. A., & Aronoff, D. M. (2017) · Journal of Innate Immunity · doi:10.1159/000480373 · Cited by 254 · see citing works
The Role of Reactive Oxygen Species (ROS) in the Formation of Extracellular Traps (ETs) in Humans
Stoiber, W., Obermayer, A., Steinbacher, P., & Krautgartner, W.-D. (2015) · Biomolecules · doi:10.3390/biom5020702 · Cited by 250 · see citing works
Neeli, I., & Radic, M. Z. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00038 · Cited by 248 · see citing works
Neutrophil extracellular traps in cancer
Cristinziano, L., Modestino, L., Antonelli, A., Marone, G., Simon, H., Varricchi, G., & Galdiero, M. R. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.07.011 · Cited by 247 · see citing works
Self-citationAllen, C., Thornton, P., Dénes, Á., McColl, B. W., Pierozynski, A., Monestier, M., Pinteaux, E., Rothwell, N. J., & Allan, S. M. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200409 · Cited by 245 · see citing works
Wu, M., Zhang, H., Tie, C., Yan, C., Deng, Z., Wan, Q., Liu, X., Yan, F., & Zheng, H. (2018) · Nature Communications · doi:10.1038/s41467-018-07250-6 · Cited by 245 · see citing works
Konig, M. F., & Andrade, F. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00461 · Cited by 240 · see citing works
Neutrophil Extracellular Traps and Their Implications in Cardiovascular and Inflammatory Disease
Klopf, J., Brostjan, C., Eilenberg, W. H., & Neumayer, C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22020559 · Cited by 237 · see citing works
Myeloperoxidase: A new player in autoimmunity
Strzępa, A., Pritchard, K. A., & Dittel, B. N. (2017) · Cellular Immunology · doi:10.1016/j.cellimm.2017.05.002 · Cited by 236 · see citing works
Platelets and Infections – Complex Interactions with Bacteria
Hamzeh‐Cognasse, H., Damien, P., Chabert, A., Pozzetto, B., Cognasse, F., & Garraud, O. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00082 · Cited by 234 · see citing works
Molecular mechanisms and therapeutic target of NETosis in diseases
Huang, J., Hong, W., Wan, M., & Zheng, L. (2022) · MedComm · doi:10.1002/mco2.162 · Cited by 234 · see citing works
Molecular Mechanisms of mtDNA-Mediated Inflammation
Gaetano, A. D., Solodka, K., Zanini, G., Selleri, V., Mattioli, A. V., Nasi, M., & Pinti, M. (2021) · Cells · doi:10.3390/cells10112898 · Cited by 235 · see citing works
Grayson, P. C., & Kaplan, M. J. (2015) · Journal of Leukocyte Biology · doi:10.1189/jlb.5bt0615-247r · Cited by 228 · see citing works
Cedervall, J., Zhang, Y., Huang, H., Zhang, L., Femel, J., Dimberg, A., & Olsson, A. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-3299 · Cited by 229 · see citing works
Neutrophils and neutrophil extracellular traps in the liver and gastrointestinal system
Honda, M., & Kubes, P. (2018) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2017.183 · Cited by 227 · see citing works
Neutrophil extracellular traps in the pathology of cancer and other inflammatory diseases
Herre, M., Cedervall, J., Mackman, N., & Olsson, A. (2022) · Physiological Reviews · doi:10.1152/physrev.00062.2021 · Cited by 232 · see citing works
Systemic Lupus Erythematosus Pathogenesis: Interferon and Beyond
Caielli, S., Wan, Z., & Pascual, V. (2023) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101921-042422 · Cited by 221 · see citing works
Young, R. L., Malcolm, K. C., Kret, J. E., Caceres, S. M., Poch, K. R., Nichols, D. P., Taylor‐Cousar, J. L., Saavedra, M. T., Randell, S. H., Vasil, M. L., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023637 · Cited by 226 · see citing works
Drury, B., Hardisty, G. R., Gray, R. D., & Ho, G. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.03.002 · Cited by 222 · see citing works
The role of neutrophil extracellular traps in acute lung injury
Scozzi, D., Liao, F., Krupnick, A. S., Kreisel, D., & Gelman, A. E. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.953195 · Cited by 220 · see citing works
Resolution of inflammation: Mechanisms and opportunity for drug development
Alessandri, A. L., Sousa, L. P., Lucas, C. D., Rossi, A. G., Pinho, V., & Teixeira, M. M. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.04.006 · Cited by 217 · see citing works
Pieterse, E., Rother, N., Yanginlar, C., Hilbrands, L. B., & van der Vlag, J. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00484 · Cited by 217 · see citing works
Figueroa, G., Álvarez-Carrasco, P., Ortega, E., & Maldonado‐Bernal, C. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.631821 · Cited by 218 · see citing works
The expanding world of extracellular traps: not only neutrophils but much more
Goldmann, O., & Medina, E. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00420 · Cited by 215 · see citing works
Damage-associated molecular patterns in trauma
Relja, B., & Land, W. G. (2019) · European Journal of Trauma and Emergency Surgery · doi:10.1007/s00068-019-01235-w · Cited by 218 · see citing works
The role of neutrophils in host defense and disease
Lehman, H. K., & Segal, B. H. (2020) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2020.02.038 · Cited by 218 · see citing works
Marcos, V., Zhou, Z., Yildirim, A. Ö., Bohla, A., Hector, A., Vitkov, L., Wiedenbauer, E.-M., Krautgartner, W. D., Stoiber, W., Belohradsky, B. H., et al. (2010) · Nature Medicine · doi:10.1038/nm.2209 · Cited by 212 · see citing works
RetractedIn vitro induction of NETosis: Comprehensive live imaging comparison and systematic review
Hoppenbrouwers, T., Autar, A. S. A., Sultan, A. R., Abraham, T. E., van Cappellen, W. A., Houtsmuller, A. B., van Wamel, W. J. B., van Beusekom, H. M. M., van Neck, J. W., & de Maat, M. P. M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0176472 · Cited by 206 · see citing works
Neutrophil Extracellular Traps in ANCA-Associated Vasculitis
Appelgren, D., & Segelmark, M. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00256 · Cited by 211 · see citing works
Role of neutrophil extracellular traps in radiation resistance of invasive bladder cancer
Shinde-Jadhav, S., Mansure, J. J., Rayes, R. F., Marcq, G., Ayoub, M., Skowronski, R., Kool, R., Bourdeau, F., Brimo, F., Spicer, J. D., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23086-z · Cited by 213 · see citing works
Tan, C., Aziz, M., & Wang, P. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.3ru0620-375r · Cited by 211 · see citing works
Neutrophil extracellular traps: protagonists of cancer progression?
Erpenbeck, L., & Schön, M. P. (2017) · Oncogene · doi:10.1038/onc.2016.406 · Cited by 199 · see citing works
Okeke, E. B., Louttit, C., Fry, C., Najafabadi, A. H., Han, K., Nemzek, J. A., & Moon, J. J. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.119836 · Cited by 196 · see citing works
ETosis: A Microbicidal Mechanism beyond Cell Death
Guimarães-Costa, A. B., Nascimento, M. T. C., Wardini, A. B., Pinto-da-Silva, L. H., & Saraiva, E. M. (2012) · Journal of Parasitology Research · doi:10.1155/2012/929743 · Cited by 195 · see citing works
Extracellular DNA NET-Works With Dire Consequences for Health
Sorvillo, N., Cherpokova, D., Martinod, K., & Wagner, D. D. (2019) · Circulation Research · doi:10.1161/circresaha.119.314581 · Cited by 196 · see citing works
- Authors
- Yousefi, S., Mihalache, C., Kozlowski, E., Schmid, I., & Simon, H. U.
- Affiliations
- University of Bern (CH)
- Corresponding author
- Yousefi, S
- ORCID
- Venue
- Cell Death & Differentiation
- Published
- 2009-07-17
- Volume
- 16
- Issue
- 11
- Pages
- 1438-1444
- ISSN
- 1350-9047 (ISSN-L)
- 1476-5403
- OpenAlex
- W2056112680
- Cited by
- 1,036
- References
- 17
- Citations by year
- 2026: 84 · 2025: 82 · 2024: 67 · 2023: 89 · 2022: 92 · 2021: 93 · 2020: 84 · 2019: 79 · 2018: 66 · 2017: 57 · 2016: 66 · 2015: 43 · 2014: 28 · 2013: 36 · 2012: 36
- FWCI
- 9.90
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Cell Death and Differentiation (publishedVersion)
- PubMed (publishedVersion)
- Bern Open Repository and Information System (University of Bern) (submittedVersion)
- Funders
- National Science Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (107526, 112078)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Life Sciences › Immunology and Microbiology › Microbiology › Antimicrobial Peptides and Activities
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- neutrophil extracellular traps, mitochondrial DNA release, neutrophil survival, reactive oxygen species, GM-CSF, TLR4, C5a receptor, innate immunity, antimicrobial defense
- MeSH terms
- DNA, Mitochondrial, Humans, Neutrophils, Complement C5a, Granulocyte-Macrophage Colony-Stimulating Factor, Apoptosis, Reactive Oxygen Species, Neutrophil Activation, Toll-Like Receptor 4
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