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NETs: a new strategy for using old weapons
Abstract
As key players in the host innate immune response, neutrophils are recruited to sites of infection and constitute the first line of defense. They employ three strategies to eliminate invading microbes: microbial uptake, the secretion of antimicrobials, and the recently described release of Neutrophil Extracellular Traps (NETs). Composed of decondensed chromatin and antimicrobial proteins, NETs bind and kill a variety of microbes including bacteria, fungi, and parasites. In addition to using a repertoire of known antimicrobials, NETs incorporate histones into the antimicrobial arsenal. Furthermore, NETs may contribute to microbial containment by forming a physical barrier and a scaffold, to enhance antimicrobial synergy while minimizing damage to host tissues. Their role in innate immunity is only now being uncovered.
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“More recent evidence indicates that neutrophils can also eliminate organisms residing in the extracellular environment through the deployment of neutrophil extracellular traps (NETs).”
From Immunology of Wound Healing (2018) · cites this paper as [41]
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Cites
Proceedings of the National Academy of Sciences of the United States of America
Dowling, J. E., & Wald, G. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.1981.tb06752.x · Cited by 17,937
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
Self-citationAntimicrobial peptides of multicellular organisms
Zasloff, M. (2002) · Nature · doi:10.1038/415389a · Cited by 8,457
Tissue Destruction by Neutrophils
Epstein, F. H., & Weiss, S. J. (1989) · New England Journal of Medicine · doi:10.1056/nejm198902093200606 · Cited by 3,950
Tissue Destruction by Neutrophils
(1989) · New England Journal of Medicine · doi:10.1056/nejm198908033210513 · Cited by 3,634
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
Self-citationNeutrophils and immunity: challenges and opportunities
Nathan, C. (2006) · Nature reviews. Immunology · doi:10.1038/nri1785 · Cited by 2,971
Resolution of inflammation: the beginning programs the end
Serhan, C. N., & Savill, J. (2005) · Nature Immunology · doi:10.1038/ni1276 · Cited by 2,552
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
Jonjić, S., Mutter, W., Weiland, F., Reddehase, M. J., & Koszinowski, U. H. (1989) · The Journal of Experimental Medicine · doi:10.1084/jem.169.4.1199 · Cited by 2,106
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Weber, C., & Noels, H. (2011) · Nature Medicine · doi:10.1038/nm.2538 · Cited by 2,203
“Furthermore, neutrophils activated through TLRs, Fc receptors or cytokine receptors can release nuclear content (DNA fibers, chromatin) that forms a scaffold containing antimicrobial proteins, such as LL-37, termed neutrophil extracellular traps (NETs”
BackgroundNeutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps
Papayannopoulos, V., Metzler, K. D., Hakkim, A., & Zychlinsky, A. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201006052 · Cited by 2,103
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“(“NETosis”) [136], is also believed to contribute to host defense against S.”
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Hakkim, A., Fuchs, T. A., Martinez, N. E., Hess, S., Prinz, H., Zychlinsky, A., & Waldmann, H. (2011) · Nature Chemical Biology · doi:10.1038/nchembio.496 · Cited by 793
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Fournier, B., & Parkos, C. A. (2012) · Mucosal Immunology · doi:10.1038/mi.2012.24 · Cited by 685
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BackgroundEllis, S., Lin, E. J., & Tartar, D. (2018) · Current Dermatology Reports · doi:10.1007/s13671-018-0234-9 · Cited by 625
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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 628
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Solana, R., Tarazona, R., Gayoso, I., Lesur, O., Dupuis, G., & Fulop, T. (2012) · Seminars in Immunology · doi:10.1016/j.smim.2012.04.008 · Cited by 567
“[11] Papayannopoulos V, Zychlinsky A.”
BackgroundInfluentialUnderstanding the mechanisms of faecal microbiota transplantation
Khoruts, A., & Sadowsky, M. J. (2016) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2016.98 · Cited by 579
Gupta, A. K., Joshi, M. B., Philippova, M., Erné, P., Hasler, P., Hahn, S., & Resink, T. J. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.06.006 · Cited by 547
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BackgroundMultiple Roles for Neutrophils in Atherosclerosis
Soehnlein, O. (2012) · Circulation Research · doi:10.1161/circresaha.111.257535 · Cited by 514
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“Although protease dispersal via NETs is implicated in further tissue destruction, the role of proteases is not limited to cleaving bacterial factors, as they are potent antimicrobial agents that can actually end up neutralizing their own effects [25, 58].”
BackgroundInfluentialMacrophage Clearance of Neutrophil Extracellular Traps Is a Silent Process
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“NETs are believed to be an effective defense system against infection, as the entrapment of pathogens in NETs may aid in the local confinement of the infection, whereas the granule-derived enzymes facilitate in the extracellular killing of the “netted” pathogens (4).”
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BackgroundHistones from Dying Renal Cells Aggravate Kidney Injury via TLR2 and TLR4
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“These structures represent a novel method for pathogen killing, independent of both degranulation and phagocytosis, and have been shown to effectively kill a variety of pathogens, including bacteria, fungi, and protozoa (Papayannopoulos and Zychlinsky, 2009; Remijsen et al., 2011a).”
BackgroundMethodNeutrophils in innate host defense against Staphylococcus aureus infections
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BackgroundMitroulis, I., Kambas, K., Chrysanthopoulou, A., Skendros, P., Apostolidou, E., Kourtzelis, I., Drosos, G. I., Boumpas, D. T., & Ritis, K. (2011) · PLoS ONE · doi:10.1371/journal.pone.0029318 · Cited by 387
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Rosales, C. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.4mir0220-574rr · Cited by 372
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Campbell, A. M., Kashgarian, M. J., & Shlomchik, M. J. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3004801 · Cited by 250
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Chen, K., Nishi, H., Travers, R. J., Tsuboi, N., Martinod, K., Wagner, D. D., Stan, R. V., Croce, K., & Mayadas, T. N. (2012) · Blood · doi:10.1182/blood-2011-12-401133 · Cited by 231
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BackgroundTreffers, L. W., Hiemstra, I. H., Kuijpers, T. W., van den Berg, T. K., & Matlung, H. L. (2016) · Immunological Reviews · doi:10.1111/imr.12444 · Cited by 211
Meng, W., Paunel‐Görgülü, A., Flohé, S., Hoffmann, A., Witte, I., MacKenzie, C. R., Baldus, S. E., Windolf, J., & Lögters, T. T. (2012) · Critical Care · doi:10.1186/cc11442 · Cited by 211
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“PMN in WNV Infection • JID 2010:202 (15 December) • 1805 peptides, and produce reactive oxygen species and extracellular traps to combat pathogens [13, 14].”
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“Neutrophils employ three strategies to eliminate invading microbes: (1) microbial uptake followed by intracellular destruction through an array of proteolytic and oxidative enzymes, (2) degranulation and secretion of antimicrobial factors such as myeloperoxidase (MPO) leading to extracellular destruction of microbes,…”
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“lactoferrin, and calprotectin [26,27].”
Aspergillus fumigatus: contours of an opportunistic human pathogen
McCormick, A., Loeffler, J., & Ebel, F. (2010) · Cellular Microbiology · doi:10.1111/j.1462-5822.2010.01517.x · Cited by 185
“NETs represent an anti-microbial effector mechanism that mediates killing of a diverse range of bacterial pathogens as well as C. albicans (Papayannopoulos and Zychlinsky, 2009).”
BackgroundPinegin, B. V., Vorobjeva, N. V., & Pinegin, V. B. (2015) · Autoimmunity Reviews · doi:10.1016/j.autrev.2015.03.002 · Cited by 184
Zhang, J., Hu, K., Di, L., Wang, P., Liu, Z., Zhang, J., Yue, P., Song, W., Zhang, J., Chen, T., et al. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.113964 · Cited by 189
Invertebrate extracellular phagocyte traps show that chromatin is an ancient defence weapon
Robb, C. T., Dyrynda, E. A., Gray, R. D., Rossi, A. G., & Smith, V. J. (2014) · Nature Communications · doi:10.1038/ncomms5627 · Cited by 177
“The discharged chromatin forms complex meshes that ensnare and kill bacteria, fungi, viruses and other parasites 7,9,10 .”
Immune Dysfunction in Uremia 2020
Cohen, G. (2020) · Toxins · doi:10.3390/toxins12070439 · Cited by 178
“NETs also represent a physical barrier and a framework enhancing antimicrobial synergy and reducing harm to host tissues [40].”
BackgroundGray, R. D., Lucas, C. D., Mackellar, A., Li, F., Hiersemenzel, K., Haslett, C., Davidson, D. J., & Rossi, A. G. (2013) · Journal of Inflammation · doi:10.1186/1476-9255-10-12 · Cited by 171
“The beneficial anti-microbial effects of NET formation have been described in several studies [4,20-25].”
BackgroundYuen, J., Pluthero, F. G., Douda, D. N., Riedl, M., Cherry, A., Ulanova, M., Kahr, W. H. A., Palaniyar, N., & Licht, C. P. B. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00137 · Cited by 171
Mycobacterium tuberculosis-Induced Neutrophil Extracellular Traps Activate Human Macrophages
Braian, C., Hogea, V., & Stendahl, O. I. (2013) · Journal of Innate Immunity · doi:10.1159/000348676 · Cited by 174
Innate immunity to intracellular pathogens: macrophage receptors and responses to microbial entry
Plüddemann, A., Mukhopadhyay, S., & Gordon, S. (2011) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00989.x · Cited by 170
“Apart from phagocytosis and degranulation, neutrophils and probably activated macrophages also employ the formation of neutrophil extracellular traps (NETs), which arise from the release of neutrophil nuclear contents into the extracellular space (9, 59).”
BackgroundNeutrophil Extracellular Traps in Sepsis
Camicia, G., Pozner, R. G., & Larrañaga, G. F. D. (2014) · Shock · doi:10.1097/shk.0000000000000221 · Cited by 166
“However, DNases require divalent cations for their activity, providing a potential point of attack by the host (42).”
BackgroundInfluentialHistones trigger sterile inflammation by activating the NLRP 3 inflammasome
Allam, R., Darisipudi, M. N., Tschopp, J., & Anders, H. (2013) · European Journal of Immunology · doi:10.1002/eji.201243224 · Cited by 163
Simplified Human Neutrophil Extracellular Traps (NETs) Isolation and Handling
Najmeh, S., Cools‐Lartigue, J., Giannias, B., Spicer, J. D., & Ferri, L. E. (2015) · Journal of Visualized Experiments · doi:10.3791/52687 · Cited by 165
The Dual Role of Myeloperoxidase in Immune Response
Arnhold, J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218057 · Cited by 172
Pathophysiology of deep vein thrombosis
Navarrete, S., Solar, C., Tapia, R., Pereira, J. I., Eduardo Fuentes, Q., & Palomo, I. F. (2022) · Clinical and Experimental Medicine · doi:10.1007/s10238-022-00829-w · Cited by 164
“Two mechanisms are known by which NET is released: (i) pathogenic microorganisms can directly stimulate their release, and (ii) platelets can stimulate the neutrophil to form NET [85].”
BackgroundNew pathophysiological insights and treatment of ANCA-associated vasculitis
Wilde, B., van Paassen, P., Witzke, O., & Tervaert, J. W. C. (2010) · Kidney International · doi:10.1038/ki.2010.472 · Cited by 151
Aulik, N. A., Hellenbrand, K. M., & Czuprynski, C. J. (2012) · Infection and Immunity · doi:10.1128/iai.06120-11 · Cited by 150
“However, LDH release did increase when macrophages were incubated with a higher dose (5 U) of LKT (Fig.”
BackgroundInfluentialYang, L., Liu, L., Zhang, R., Hong, J., Wang, Y.-P., Wang, J., Zuo, J., Zhang, J., Chen, J., & Hao, H. (2020) · Journal of Cancer · doi:10.7150/jca.44215 · Cited by 157
“Neutrophil extracellular traps (NETs) are large extracellular web-like structures comprised of decondensed chromatin and protease that are released by activated neutrophils under certain stimulus [11-14].”
BackgroundNaegleria fowleri : Sources of infection, pathophysiology, diagnosis, and management; a review
Jahangeer, M., Mahmood, Z., Munir, N., Waraich, U., Tahir, I. M., Akram, M., Shah, S. M. A., Zulfqar, A., & Zainab, R. (2019) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.13192 · Cited by 144
Mohsin, F., Javaid, S., Tariq, M., & Mustafa, M. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.112713 · Cited by 153
How Neutrophil Extracellular Traps Become Visible
de Buhr, N., & von Köckritz‐Blickwede, M. (2016) · Journal of Immunology Research · doi:10.1155/2016/4604713 · Cited by 148
“These antimicrobial components are myeloperoxidase (MPO), neutrophil elastase (NE), cathelicidins like LL-37, histones, proteinase 3, cathepsin, lactoferrin, or gelatinase [3, 16, 17].”
Estradiol-Treated Female Mice as Surrogate Hosts for Neisseria gonorrhoeae Genital Tract Infections
Jerse, A. E., Wu, H., Packiam, M., Vonck, R. A., Begum, A. A., & Garvin, L. E. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00107 · Cited by 141
“PMNs also kill microbes via the release of pre-formed enzymes and antimicrobial peptides and entrapment in neutrophil extracellular traps (NETs) where they are exposed to toxic molecules produced by both pathways (Kobayashi et al., 2005; Papayannopoulos and Zychlinsky, 2009).”
BackgroundNETosis as Source of Autoantigens in Rheumatoid Arthritis
Corsiero, E., Pratesi, F., Prediletto, E., Bombardieri, M., & Migliorini, P. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00485 · Cited by 140
“Arthritis Rheumatol (2014) 66(1):31–9.”
BackgroundVaidya, K., Tucker, B., Kurup, R., Khandkar, C., Pandžić, E., Barraclough, J., Machet, J., Misra, A., Kavurma, M. M., Martínez, G., et al. (2020) · Journal of the American Heart Association · doi:10.1161/jaha.120.018993 · Cited by 139
Eosinophil extracellular DNA traps: molecular mechanisms and potential roles in disease
Yousefi, S., Simon, D., & Simon, H. (2012) · Current Opinion in Immunology · doi:10.1016/j.coi.2012.08.010 · Cited by 143
Vibrio cholerae Evades Neutrophil Extracellular Traps by the Activity of Two Extracellular Nucleases
Seper, A., Hosseinzadeh, A., Gorkiewicz, G., Lichtenegger, S., Roier, S., Leitner, D. R., Röhm, M., Grutsch, A., Reidl, J., Urban, C. F., et al. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003614 · Cited by 140
“Antimicrobial strategies of neutrophils range from phagocytosis of the respective microbes to the formation of NETs, which are able to bind and kill pathogens due to a high concentration of antimicrobial compounds [21,22].”
BackgroundClancy, D. M., Henry, C. M., Sullivan, G. P., & Martin, S. J. (2017) · FEBS Journal · doi:10.1111/febs.14075 · Cited by 140
Achouiti, A., Vogl, T., Urban, C. F., Röhm, M., Hommes, T. J., van Zoelen, M. A. D., Florquin, S., Roth, J., van 't Veer, C., de Vos, A. F., et al. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002987 · Cited by 135
“that MRP8/14 is a major component of neutrophil extracellular traps (NETs) [24], DNA-networks released by neutrophils that trap microorganisms and facilitate interaction with antimicrobial proteins and thereby bacterial killing [25,26].”
BackgroundExtracellular histone release in response to traumatic injury
Kutcher, M., Xu, J., Vilardi, R. F., Ho, C., Esmon, C. T., & Cohen, M. J. M. (2012) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/ta.0b013e318270d595 · Cited by 133
“Second, proteomic analysis of circulating biomarkers in lipopolysaccharide (LPS)-induced septic shock has revealed citrullination of extracellular histones as an element of the early response of neutrophils to inflammatory stimuli(30) and the subsequent incorporation of citrullinated histones into NETs in response to…”
BackgroundJovanović, B., Anastasova, L., Rowe, E., Zhang, Y., Clapp, A. R., & Palić, D. (2010) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2010.10.017 · Cited by 136
“NETs release is closely related to the process of respiratory burst and ROS production appears to be a crucial signal involved in initiating the NETosis cell death program (Papayannopoulos and Zychlinsky, 2009).”
Background
Metadata
- Authors
- Papayannopoulos, V., & Zychlinsky, A.
- Affiliations
- Max Planck Society (DE)
- Corresponding author
- Papayannopoulos, Venizelos
- Venue
- Trends in Immunology
- Publisher
- Elsevier BV
- Published
- 2009-11
- Volume
- 30
- Issue
- 11
- Pages
- 513-521
- ISSN
- 1471-4906 (ISSN-L)
- OpenAlex
- W2101674426
- Cited by
- 634
- References
- 101
- Citations by year
- 2026: 13 · 2025: 15 · 2024: 28 · 2023: 30 · 2022: 34 · 2021: 31 · 2020: 30 · 2019: 39 · 2018: 45 · 2017: 45 · 2016: 50 · 2015: 35 · 2014: 51 · 2013: 46 · 2012: 68
- FWCI
- 3.72
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Trends in Immunology (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Life Sciences › Immunology and Microbiology › Microbiology › Antimicrobial Peptides and Activities
- Health Sciences › Medicine › Hematology › Blood disorders and treatments
- Keywords
- neutrophil extracellular traps, neutrophils, innate immunity, antimicrobial peptides, histones, chromatin, antimicrobial synergy
- MeSH terms
- Animals, Bacterial Infections, Chromatin, Histones, Humans, Immunity, Innate, Inflammation, Neutrophils, Phagocytosis, Cell Degranulation, Autoimmunity, Reactive Oxygen Species
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