Cited by 634Neutrophil, Myeloperoxidase and Oxidative MechanismsAntimicrobial Peptides and ActivitiesBlood disorders and treatments

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NETs: a new strategy for using old weapons

Papayannopoulos, Venizelos, Zychlinsky, Arturo·2009·Trends in Immunology

DOI 10.1016/j.it.2009.07.011

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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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Background
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Background
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Background
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Background
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Background
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BackgroundSelf-citation
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Background
Bovine macrophage-derived extracellular traps act as early effectors against the abortive parasite Neospora caninum
Wei, Z., Wang, Y., Zhang, X., Wang, X., Gong, P., Li, J., Taubert, A., Hermosilla, C. R., Zhang, X., & Yang, Z. (2018) · Veterinary Parasitology · doi:10.1016/j.vetpar.2018.06.002 · Cited by 36
Streptococcus thermophilus alters the expression of genes associated with innate and adaptive immunity in human peripheral blood mononuclear cells
Dargahi, N., Johnson, J., & Apostolopoulos, V. (2020) · PLoS ONE · doi:10.1371/journal.pone.0228531 · Cited by 37
“In addition, myeloperoxidase (MPO), an enzyme abundantly expressed by neutrophils and promotes inflammation, is also involved in autoimmune disorders (multiple sclerosis, rheumatoid arthritis) [79, 80].”
Background
Immune Response to the Enteric ParasiteEntamoeba histolytica
Uribe‐Querol, E., & Rosales, C. (2020) · Physiology · doi:10.1152/physiol.00038.2019 · Cited by 37
Fine-tuning neutrophil activation: Strategies and consequences
van der Linden, M., & Meyaard, L. (2016) · Immunology Letters · doi:10.1016/j.imlet.2016.05.015 · Cited by 36
Role for Streptococcal Collagen-Like Protein 1 in M1T1 Group A Streptococcus Resistance to Neutrophil Extracellular Traps
Döhrmann, S., Anik, S., Olson, J., Anderson, E. L., Etesami, N. S., No, H., Snipper, J., Nizet, V., & Okumura, C. Y. M. (2014) · Infection and Immunity · doi:10.1128/iai.01921-14 · Cited by 36
“The production of reactive oxygen species (ROS) through the oxidative burst is a critical stimulatory pathway promoting the generation of NETs (3).”
BackgroundInfluential
Acinetobacter baumannii escape from neutrophil extracellular traps (NETs)
Kamoshida, G., Kikuchi‐Ueda, T., Tansho‐Nagakawa, S., Nakano, R., Nakano, A., Kikuchi, H., Ubagai, T., & Ono, Y. (2014) · Journal of Infection and Chemotherapy · doi:10.1016/j.jiac.2014.08.032 · Cited by 36
Extracellular trap formation in kuruma shrimp (Marsupenaeus japonicus) hemocytes is coupled with c-type lysozyme
Koiwai, K., Alenton, R. R. R., Kondo, H., & Hırono, I. (2016) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2016.03.039 · Cited by 36
Immunothrombosis in Acute Ischemic Stroke
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“43 First, neutrophils kill micro-organisms via phagocytosis through a reactive oxygen species–dependent mechanism.”
Tobacco exposure and susceptibility to tuberculosis: Is there a smoking gun?
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“Formation of NETs is dependent on intrinsic oxidative burst produced by neutrophils [46].”
Background
Regulation of in vivo delivery of nanomedicines by herbal medicines
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Neutrophil Extracellular Trap in Human Diseases
Araźna, M., Pruchniak, M. P., Życińska, K., & Demkow, U. A. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-4549-0_1 · Cited by 32
Interactions of Staphylococci with Osteoblasts and Phagocytes in the Pathogenesis of Implant-Associated Osteomyelitis
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Relevance of α-defensins (HNP1-3) and defensin β-1 in diabetes.
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Neutrophil extracellular traps involvement in corneal fungal infection.
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Peptidylarginine deiminase and deiminated proteins are detected throughout early halibut ontogeny - Complement components C3 and C4 are post-translationally deiminated in halibut (Hippoglossus hippoglossus L.)
Magnadóttir, B., Bragason, B. Þ., Bricknell, I. R., Bowden, T. J., Nicholas, A. P., Hristova, M., Guðmundsdóttir, S., Dodds, A. W., & Lange, S. (2018) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2018.10.016 · Cited by 34
Computational Methodologies for the in vitro and in situ Quantification of Neutrophil Extracellular Traps
van Breda, S. V., Vokálová, L., Neugebauer, C., Rossi, S. W., Hahn, S., & Hasler, P. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01562 · Cited by 34
Redox Activity and Nano–Bio Interactions Determine the Skin Injury Potential of Co3O4‑Based Metal Oxide Nanoparticles toward Zebrafish
Peng, G., He, Y., Wang, X., Cheng, Y., Zhang, H., Savolainen, K., Mädler, L., Pokhrel, S., & Lin, S. (2020) · ACS Nano · doi:10.1021/acsnano.9b08938 · Cited by 34
Characteristics and Role of Neutrophil Extracellular Traps in Asthma
Chen, F., Yu, M. H., Zhong, Y., Wang, L., & Huang, H. (2021) · Inflammation · doi:10.1007/s10753-021-01526-8 · Cited by 36
“NE degrades virulence factors of Gram-negative bacteria [4], and serine protease can penetrate and destroy bacterial membranes [47].”
Background
Pathophysiology, staging and therapy of severe sepsis in baboon models
Taylor, F. B., Kinasewitz, G. T., & Lupu, F. (2011) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2011.01454.x · Cited by 34
“In direct response to the invading bacteria, neutrophils and other inflammatory cells release extracellular traps (ETs) made of DNA and core histones, as well as anti-microbial components (defensins, myeloperoxidase, elastase) that bind, disarm an kill microbes extracellularly, independent of phagocytic uptake [11].”
Background
Comparison of the virulence of exopolysaccharide-producing Prevotella intermedia to exopolysaccharide non-producing periodontopathic organisms
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“In such a situation, PMNLs are known to produce a harmful effect to the surrounding tissue by elaborating a variety of degradative enzymes and oxygen radicals in an attempt to clear the invaded pathogens [46,47].”
Autophagy mediates neutrophil responses to bacterial infection
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Host Defense Against Implant Infection: The Ambivalent Role of Phagocytosis
Arciola, C. R. (2010) · The International Journal of Artificial Organs · doi:10.1177/039139881003300901 · Cited by 34
The relationship between autophagy, increased neutrophil extracellular traps formation and endothelial dysfunction in chronic kidney disease
Kim, J.-K., Park, M. J., Lee, H. W., Lee, H., Choi, S. R., Song, Y. R., Kim, H. J., Park, H. C., & Kim, S. G. (2018) · Clinical Immunology · doi:10.1016/j.clim.2018.10.003 · Cited by 33
Inflammation and Repair
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Neutrophil Extracellular Vesicles: A Delicate Balance between Pro-Inflammatory Responses and Anti-Inflammatory Therapies
Zhou, Y., & Bréchard, S. (2022) · Cells · doi:10.3390/cells11203318 · Cited by 33
Targeting Neutrophil Extracellular Traps in Gouty Arthritis: Insights into Pathogenesis and Therapeutic Potential
Li, C., Wu, C., Li, F., Xu, W., Zhang, X., Huang, Y., & Xia, D. (2024) · Journal of Inflammation Research · doi:10.2147/jir.s460333 · Cited by 34
Th17 cells and neutrophils: Close collaborators in chronic Leishmania mexicana infections leading to disease severity
Zamora, C., Delgado-Domínguez, J., Zamora‐Chimal, J., & Becker, I. (2017) · Parasite Immunology · doi:10.1111/pim.12420 · Cited by 32
Spontaneous formation of neutrophil extracellular traps in serum‐free culture conditions
Kamoshida, G., Kikuchi‐Ueda, T., Nishida, S., Tansho‐Nagakawa, S., Kikuchi, H., Ubagai, T., & Ono, Y. (2017) · FEBS Open Bio · doi:10.1002/2211-5463.12222 · Cited by 34
Control of the inflammatory response during pregnancy: potential role of VIP as a regulatory peptide
Ramhorst, R., Calo, G., Paparini, D., Vota, D., Hauk, V. C., Gallino, L., Merech, F., Grasso, E., & Leirós, C. P. (2018) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13632 · Cited by 32
Interleukin-33 Induces Neutrophil Extracellular Trap (NET) Formation and Macrophage Necroptosis via Enhancing Oxidative Stress and Secretion of Proatherogenic Factors in Advanced Atherosclerosis
Tembhre, M. K., Sriwastva, M. K., Hote, M. P., Srivastava, S., Solanki, P., Imran, S., Lakshmy, R., Sharma, A., Jaiswal, K. P., & Upadhyay, A. D. (2022) · Antioxidants · doi:10.3390/antiox11122343 · Cited by 33
“The neutrophil extracellular traps (NETs) or NETosis is a recently identified cell death mechanism (distinct from apoptosis and necrosis), and NETs are formed in response to pathogens and under the influence of myriad of inflammatory factors [6,7].”
Background
Opa+ N eisseria gonorrhoeae exhibits reduced survival in human neutrophils via Src family kinase-mediated bacterial trafficking into mature phagolysosomes
Johnson, M. B., Ball, L. M., Daily, K. P., Martin, J. N., Columbus, L. M., & Criss, A. K. (2014) · Cellular Microbiology · doi:10.1111/cmi.12389 · Cited by 32
“Polymorphonuclear leukocyte antimicrobial mechanisms include generation of reactive oxygen species (ROS) via NADPH oxidase, release of antimicrobial enzymes and peptides, and production of neutrophil extracellular traps (Borregaard et al., 2007; Papayannopoulos and Zychlinsky, 2009; Borregaard, 2010).”
Background
Battle and balance at mucosal surfaces – The story of Shigella and antimicrobial peptides
Gudmundsson, G. H., Bergman, P., Andersson, J., Raqib, R., & Agerberth, B. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.03.081 · Cited by 32
The battle with the host over microbial size
Weiser, J. N. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.01.001 · Cited by 31
“For example, secreted DNA/chromatin from neutrophils (NETs, neutrophil extracellular traps) forms a scaffold that ensnares microbes [22,23].”
Background
Biological Activity of CXCL8 Forms Generated by Alternative Cleavage of the Signal Peptide or by Aminopeptidase-Mediated Truncation
Mortier, A., Berghmans, N., Ronsse, I., Grauwen, K., Stegen, S., Damme, J. V., & Proost, P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023913 · Cited by 32
“formation of neutrophil extracellular traps (NETs), a mechanism that allows neutrophils to retain antimicrobial activity after death, has been identified as an additional mechanism and alternative for death by necrosis or apoptosis [8,9].”
Background
Tetrahydroisoquinolines: New Inhibitors of Neutrophil Extracellular Trap (NET) Formation
Martinez, N. E., Zimmermann, T. J., Goosmann, C., Alexander, T., Hedberg, C., Ziegler, S., Zychlinsky, A., & Waldmann, H. (2017) · ChemBioChem · doi:10.1002/cbic.201600650 · Cited by 31
Self-citation
Bovine Neutrophils Release Extracellular Traps and Cooperate With Macrophages in Mycobacterium avium subsp. paratuberculosis clearance In Vitro
Ladero-Auñon, I., Molina, E., Holder, A. L., Kolakowski, J., Harris, H., Urkitza, A., Anguíta, J., Werling, D., & Elguezábal, N. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.645304 · Cited by 31
Perioperative Elevation in Cell-Free DNA Levels in Patients Undergoing Cardiac Surgery: Possible Contribution of Neutrophil Extracellular Traps to Perioperative Renal Dysfunction
Qi, Y., Uchida, T., Yamamoto, M., Yamamoto, Y., Kido, K., Ito, H., Ohno, N., Asahara, M., Yamada, Y., Yamaguchi, O., et al. (2016) · Anesthesiology Research and Practice · doi:10.1155/2016/2794364 · Cited by 31
Vps13F links bacterial recognition and intracellular killing inDictyostelium
Leiba, J., Sabra, A., Bodinier, R., Marchetti, A., de Lima, W. C., Melotti, A., Perrin, J., Burdet, F., Pagni, M., Soldati, T., et al. (2017) · Cellular Microbiology · doi:10.1111/cmi.12722 · Cited by 31
“Other mechanisms such as the generation of DNA and lytic enzymes that complex by dying neutrophils (NETs: Neutrophil Extracellular Traps) may in addition account for extracellular killing of bacteria (Papayannopoulos & Zychlinsky, 2009).”
Background
Effective NET formation in neutrophils from individuals with G6PD Taiwan-Hakka is associated with enhanced NADP+biosynthesis
Cheng, M. L., Ho, H., Lin, H.-Y., Lai, Y., & Chiu, D. T. Y. (2013) · Free Radical Research · doi:10.3109/10715762.2013.816420 · Cited by 31

Authors: Papayannopoulos, V., & Zychlinsky, A.
Affiliations: Max Planck Society (DE)
Corresponding author: Papayannopoulos, Venizelos
ORCID: Papayannopoulos, Venizelos
Zychlinsky, Arturo
Venue: Trends in Immunology
Publisher: Elsevier BV
Published: 2009-11
Volume: 30
Issue: 11
Pages: 513-521
ISSN: 1471-4906 (ISSN-L)
DOI: 10.1016/j.it.2009.07.011
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
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
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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NETs: a new strategy for using old weapons

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