Cited by 818Neutrophil, Myeloperoxidase and Oxidative MechanismsCell death mechanisms and regulationAntimicrobial Peptides and Activities

The DOI matches its Crossref record; 51 of the 51 references it cites were found in a registry or an index.

Neutrophil extracellular trap cell death requires both autophagy and superoxide generation

Open access

Remijsen, Quinten, Berghe, Tom Vanden, Wirawan, Ellen, Asselbergh, Bob, Parthoens, Eef, De Rycke, Riet, Noppen, Sam, Delforge, Michel, Willems, Jean, Vandenabeele, Peter·2011·Cell Research

DOI 10.1038/cr.2010.150PMC PMC3193439

Open this paper in CoChat — free account Open PDF

Abstract

Neutrophil extracellular traps (NETs) are extracellular chromatin structures that can trap and degrade microbes. They arise from neutrophils that have activated a cell death program called NET cell death, or NETosis. Activation of NETosis has been shown to involve NADPH oxidase activity, disintegration of the nuclear envelope and most granule membranes, decondensation of nuclear chromatin and formation of NETs. We report that in phorbol myristate acetate (PMA)-stimulated neutrophils, intracellular chromatin decondensation and NET formation follow autophagy and superoxide production, both of which are required to mediate PMA-induced NETosis and occur independently of each other. Neutrophils from patients with chronic granulomatous disease, which lack NADPH oxidase activity, still exhibit PMA-induced autophagy. Conversely, PMA-induced NADPH oxidase activity is not affected by pharmacological inhibition of autophagy. Interestingly, inhibition of either autophagy or NADPH oxidase prevents intracellular chromatin decondensation, which is essential for NETosis and NET formation, and results in cell death characterized by hallmarks of apoptosis. These results indicate that apoptosis might function as a backup program for NETosis when autophagy or NADPH oxidase activity is prevented.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1038/cr.2010.150

Cites

51 of 51 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

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
Autophagy in the Pathogenesis of Disease
Levine, B., & Kroemer, G. (2008) · Cell · doi:10.1016/j.cell.2007.12.018 · Cited by 7,069
Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009
Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., El-Deiry, W. S., Golstein, P., Green, D. R., et al. (2009) · Cell Death & Differentiation · doi:10.1038/cdd.2008.150 · Cited by 3,399
Self-citation
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
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
NADPH Oxidase: An Update
BABIOR, B. M. (1999) · Blood · doi:10.1182/blood.v93.5.1464 · Cited by 2,147
Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4
Scherz‐Shouval, R., Shvets, E., Fass, E., Shorer, H., Gil, L., & Elazar, Z. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601623 · Cited by 2,101
Identification of RIP1 kinase as a specific cellular target of necrostatins
Degterev, A., Hitomi, J., Germscheid, M., Ch'en, I. L., Korkina, O., Teng, X., Abbott, D., Cuny, G. D., Yuan, C., Wagner, G., et al. (2008) · Nature Chemical Biology · doi:10.1038/nchembio.83 · Cited by 2,059
Netting neutrophils in autoimmune small-vessel vasculitis
Kessenbrock, K., Krumbholz, M., Schönermarck, U., Back, W. E., Gross, W. L., Werb, Z., Gröne, H., Brinkmann, V., & Jenne, D. E. (2009) · Nature Medicine · doi:10.1038/nm.1959 · Cited by 1,687
Inhibition of Macroautophagy Triggers Apoptosis
Boya, P., González‐Polo, R. A., Casares, N., Perfettini, J., Dessen, P., Larochette, N., Métivier, D., Meley, D., Souquère, S., Yoshimori, T., et al. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.3.1025-1040.2005 · Cited by 1,669

Show all 51 references

Sorted by citations

Items 501–600 of 818

Cell death classification: A new insight based on molecular mechanisms
Dehghan, S., Kheshtchin, N., Hassannezhad, S., & Soleimani, M. (2023) · Experimental Cell Research · doi:10.1016/j.yexcr.2023.113860 · Cited by 21
An emerging role for neutrophils in the pathogenesis of endometriosis
Wilson, T. R., Kasper, S., & Burns, K. A. (2025) · npj Women s Health · doi:10.1038/s44294-025-00059-x · Cited by 21
IFN-γ Induces Mimic Extracellular Trap Cell Death in Lung Epithelial Cells Through Autophagy-Regulated DNA Damage
Lin, C., Chien, S.-Y., Chen, C., Hsieh, C.-Y., Tseng, P., & Wang, Y. (2015) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2015.0011 · Cited by 18
Ovine vital neutrophil extracellular traps bind and impair Haemonchus contortus L3 in a breed‐dependent manner
Garza, J. J., Greiner, S. P., & Bowdridge, S. A. A. (2018) · Parasite Immunology · doi:10.1111/pim.12572 · Cited by 18
Short-Term Fever-Range Hyperthermia Accelerates NETosis and Reduces Pro-inflammatory Cytokine Secretion by Human Neutrophils
Keitelman, I. A., Sabbione, F., Shiromizu, C. M., Giai, C., Fuentes, F., Rosso, D. A., Ledo, C., Miglio, M. S., Guzmán, M., Geffner, J. R., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02374 · Cited by 18
Alum triggers infiltration of human neutrophils ex vivo and causes lysosomal destabilization and mitochondrial membrane potential‐dependent NET‐formation
Reithofer, M., Karacs, J., Strobl, J., Kitzmüller, C., Polak, D., Seif, K., Kamalov, M., Becker, C. F. W., Greiner, G., Schmetterer, K. G., et al. (2020) · The FASEB Journal · doi:10.1096/fj.202001413r · Cited by 18
NETosis in myocardial ischemia‑reperfusion injury: From mechanisms to therapies (Review)
Zhang, Z., Wang, Y., Li, T., & Wang, H. (2025) · Biomedical Reports · doi:10.3892/br.2025.1991 · Cited by 18
Neutrophil extracellular traps, damage‐associated molecular patterns, and cell death during sepsis
Iba, T., Murai, M., Nagaoka, I., & Tabe, Y. (2013) · Acute Medicine & Surgery · doi:10.1002/ams2.10 · Cited by 17
Systemic and Cardiac Alterations After Long Bone Fracture
Weber, B., Lackner, I., Knecht, D., Braun, C., Gebhard, F. T., Huber-Lang, M. S., Hildebrand, F., Horst, K., Pape, H., Ignatius, A. A., et al. (2020) · Shock · doi:10.1097/shk.0000000000001536 · Cited by 17
Crosstalk Between Autophagy and Hypoxia-Inducible Factor-1α in Antifungal Immunity
Quäschling, T., Friedrich, D., Deepe, G. S., & Rupp, J. (2020) · Cells · doi:10.3390/cells9102150 · Cited by 17
NADPH oxidase in B cells and macrophages protects against murine lupus by regulation of TLR7
Gordon, R. A., Cosgrove, H. A., Marinov, A. D., Gingras, S., Tilstra, J. S., Campbell, A. M., Bastacky, S., Kashgarian, M. J., Perl, A., Nickerson, K. M., et al. (2024) · JCI Insight · doi:10.1172/jci.insight.178563 · Cited by 17
Neutrophil NET Formation with Microbial Stimuli Requires Late Stage NADPH Oxidase Activity
Parker, H. A., Jones, H. L., Kaldor, C. D., Hampton, M. B., & Winterbourn, C. C. (2021) · Antioxidants · doi:10.3390/antiox10111791 · Cited by 18
Neutrophils delay repair process in Wallerian degeneration by releasing NETs outside the parenchyma
Yamamoto, Y., Kadoya, K., Terkawi, M. A., Endo, T., Konno, K., Watanabe, M., Ichihara, S., Hara, A., Kaneko, K., Iwasaki, N., et al. (2022) · Life Science Alliance · doi:10.26508/lsa.202201399 · Cited by 16
Worsening Thrombotic Complication of Atherosclerotic Plaques Due to Neutrophils Extracellular Traps: A Systematic Review
Nappi, F., Bellomo, F., & Singh, S. S. A. (2023) · Biomedicines · doi:10.3390/biomedicines11010113 · Cited by 17
Autophagy in Inflammatory Response against SARS-CoV-2
Resnik, R., Mingorance, F. L., Rivera, F., Mitchell, F., González, C. D., & Vaccaro, M. I. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054928 · Cited by 17
New insights into autophagy in inflammatory subtypes of asthma
Dong, H., Yang, W. Z., Li, W., Zhu, S., Zhu, L., Gao, P., & Hao, Y. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1156086 · Cited by 16
Tamm-Horsfall protein augments neutrophil NETosis during urinary tract infection
Mercado-Evans, V., Branthoover, H., Chew, C., Serchejian, C., Saltzman, A. B., Mejia, M. E., Zulk, J. J., Cornax, I., Nizet, V., & Patras, K. A. (2024) · JCI Insight · doi:10.1172/jci.insight.180024 · Cited by 18
A Label-Free Quantitative Proteomic Analysis of Mouse Neutrophil Extracellular Trap Formation Induced by Streptococcus suis or Phorbol Myristate Acetate (PMA)
Wang, X., Zhao, J., Cai, C., Tang, X., Fu, L., Zhang, A., & Li, H. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02615 · Cited by 16
PRAK Is Required for the Formation of Neutrophil Extracellular Traps
Wang, Y., Wang, Y., Wu, J., Liu, C., Zhou, Y. J., Mi, L., Zhang, Y., & Wang, W. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01252 · Cited by 16
Glycolysis, monocarboxylate transport, and purinergic signaling are key events in Eimeria bovis-induced NETosis
Conejeros, I., López-Osorio, S., Zhou, E., Velásquez, Z. D., Río, M. C. D., Burgos, R. A., Alarcón, P., Chaparro-Gutiérrez, J. J., Hermosilla, C. R., & Taubert, A. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.842482 · Cited by 16
A variety of death modes of neutrophils and their role in the etiology of autoimmune diseases
Li, Y., Wu, Y., Huang, J., Cao, X., An, Q., Peng, Y., Zhao, Y., & Luo, Y. (2023) · Immunological Reviews · doi:10.1111/imr.13284 · Cited by 16
Neutrophil Extracellular Traps: A Crucial Factor in Post-Surgical Abdominal Adhesion Formation
Lu, Y., Elrod, J., i, M. H., Knopf, J., & Boettcher, M. (2024) · Cells · doi:10.3390/cells13110991 · Cited by 15
Neutrophil and neutrophil extracellular trap involvement in neutrophilic asthma: A review
Li, Y., Yang, T., & Jiang, B. (2024) · Medicine · doi:10.1097/md.0000000000039342 · Cited by 17
Direct and indirect methods of evaluating the NETosis process
Kasprzycka, W., Homa‐Mlak, I., Mlak, R., & Malecka-Massalska, T. J. (2019) · Journal of Pre-Clinical and Clinical Research · doi:10.26444/jpccr/105563 · Cited by 15
Site-specific inhibition of neutrophilic inflammation by low-dose nanotherapy for immunoregulatory treatment of asthma
Ma, Y., Li, L., Hu, Y., Han, S., Yang, Q., Pu, W., Zhang, J., & Zhang, J. (2023) · Nano Today · doi:10.1016/j.nantod.2023.101957 · Cited by 15
Nitric Oxide: Regulation and Function in Neutrophil Immune Responses
Kumar, S., & Dikshit, M. (2024) · Antioxidants and Redox Signaling · doi:10.1089/ars.2022.0220 · Cited by 17
Fundamental mechanisms of cell death for polycystic ovary syndrome
Li, Y., Peng, Y., Yang, Y., Xu, N., Shi, T., Liu, R., Luan, Y., & Yin, C.-H. (2025) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2025.102043 · Cited by 14
Boosting of post‐exposure human T‐cell and B‐cell recall responses in vivo by Burkholderia pseudomallei‐related proteins
Nithichanon, A., Gourlay, L. J., Bancroft, G. J., Ato, M., Takahashi, Y., & Lertmemongkolchai, G. (2017) · Immunology · doi:10.1111/imm.12709 · Cited by 14
Common and Rare Variants Genetic Association Analysis of Circulating Neutrophil Extracellular Traps
Donkel, S. J., Portilla-Fernández, E., Ahmad, S., Rivadeneira, F., van Rooij, F. J. A., Ikram, M. A., Leebeek, F. W. G., de Maat, M. P. M., & Ghanbari, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.615527 · Cited by 14
Defective nuclear entry of hydrolases prevents neutrophil extracellular trap formation in patients with chronic granulomatous disease
Romão, S., Puente, E. T., Nytko, K. J., Siler, U., Münz, C., & Reichenbach, J. (2015) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2015.09.007 · Cited by 14
The Expanding Role of Extracellular Traps in Inflammation and Autoimmunity: The New Players in Casting Dark Webs
Huang, S. U.-S., & O’Sullivan, K. M. (2022) · doi:10.20944/preprints202203.0021.v1 · Cited by 65
Neutrophil Extracellular Traps in Cardiovascular Diseases: Pathological Roles and Therapeutic Implications
Ma, Y., Zhang, J., Qi, Y., Lu, Y., Dong, Y., & Hu, D. (2025) · Biomolecules · doi:10.3390/biom15091263 · Cited by 15
Circadian Control of Neutrophils Drives Collateral Perfusion and Stroke Outcome
Vázquez‐Reyes, S., García‐Culebras, A., Di, G., Castro-Millán, F. J., Díaz-Benito, B., Nieto‐Vaquero, C., Ruíz-Sánchez, A., Merino-Casamayor, E., Parra-Pérez, C., Moraga, A., et al. (2025) · Circulation Research · doi:10.1161/circresaha.125.326438 · Cited by 17
IgD enhances the release of neutrophil extracellular traps (NETs) via FcδR in rheumatoid arthritis patients
Pan, W., Xin, Q., Xu, J., He, J., Chen, Z., Hu, X., Li, T., Zhu, Y., Wei, W., & Wu, Y. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.109484 · Cited by 13
The central role of neutrophil extracellular traps (NETs) and by‐products in COVID‐19 related pulmonary thrombosis
Li, S., Wang, H., & Shao, Q. (2023) · Immunity Inflammation and Disease · doi:10.1002/iid3.949 · Cited by 14
Neutrophil extracellular traps in adult diseases and neonatal bacterial infectious diseases: A review
Li, Z., & Yuan, T. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e23559 · Cited by 13
Characteristics and Regulation of Human Eosinophil ETosis In Vitro
Tomizawa, H., Arima, M., Miyabe, Y., Furutani, C., Kodama, S., Ito, K., Watanabe, K., Hasegawa, R., Nishiyama, S., Hizuka, K., et al. (2024) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2023-0438oc · Cited by 14
A disulfidptosis-related lncRNA signature for analyzing tumor microenvironment and clinical prognosis in hepatocellular carcinoma
Zheng, H., Cheng, J., Zhuang, Z., Li, D., Yang, J., Yuan, F., Fan, X., & Liu, X. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1412277 · Cited by 13
Therapeutic Anticoagulation with Argatroban and Heparins Reduces Granulocyte Migration: Possible Impact on ECLS-Therapy?
Bredthauer, A., Kopfmueller, M., Gruber, M. A., Pfaehler, S.-M., Lehle, K., Petermichl, W., Seyfried, T., Bitzinger, D., & Redel, A. (2020) · Cardiovascular Therapeutics · doi:10.1155/2020/9783630 · Cited by 13
Searching for combination therapy by clustering methods: Stimulation of PKC in Golgi apparatus combined with hypericin induced PDT
Lenkavská, L., Tomková, S., Horváth, D., & Huntošová, V. (2020) · Photodiagnosis and Photodynamic Therapy · doi:10.1016/j.pdpdt.2020.101813 · Cited by 13
The Small GTPase Cdc42 Negatively Regulates the Formation of Neutrophil Extracellular Traps by Engaging Mitochondria
Tackenberg, H., Möller, S., Filippi, M., & Laskay, T. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.564720 · Cited by 13
Modulations in human neutrophil metabolome and S-glutathionylation of glycolytic pathway enzymes during the course of extracellular trap formation
Awasthi, D., Nagarkoti, S., Sadaf, S., Aggarwal, H., Gupta, S. K., Chandra, T., Kumar, Y., Kumar, S., & Dikshit, M. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2022.166581 · Cited by 13
Capability of Neutrophils to Form NETs Is Not Directly Influenced by a CMA-Targeting Peptide
Maueröder, C., Schall, N., Meyer, F., Mahajan, A., Garnier, B., Hahn, J., Kienhöfer, D., Hoffmann, M. H., & Muller, S. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00016 · Cited by 13
Bacteria causing pyometra in bitch and queen induce neutrophil extracellular traps
Rebordão, M. R., Alexandre‐Pires, G., Carreira, M., Adriano, L., Carneiro, C., Nunes, T., Mateus, L. M., & Ferreira-Dias, G. M. (2017) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2017.09.001 · Cited by 14
Irreversible Tissue Thermal Alterations: Skin Burns, Thermal Damage and Cell Death
Pearce, J. A. (2018) · doi:10.1002/9781119127420.ch26 · Cited by 13
Ambient NO2 hinders neutrophil extracellular trap formation in rats: Assessment of the role of neutrophil autophagy
Ye, S., Ma, Y., Li, S., Luo, S., Wei, L. J., Hu, D., & Xiao, F. (2023) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2023.131755 · Cited by 12
FTY720 induces neutrophil extracellular traps via a NADPH oxidase-independent pathway
Zhang, L., Gao, H., Yang, L., Liu, T., Zhang, Q., Xun, J., Li, C., Cui, L., & Wang, X. (2021) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2021.109015 · Cited by 12
Sodium butyrate attenuates bovine mammary epithelial cell injury by inhibiting the formation of neutrophil extracellular traps
Li, Y., Liu, J., Cui, Y., Cao, Y., Xu, P., Kan, X., Guo, W., & Fu, S. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.109009 · Cited by 11
The effect of different atmosphere absolute hyperbaric oxygen on the expression of extracellular histones after traumatic brain injury in rats
Liang, F., Sun, L., Yang, J., Liu, X., Zhang, J., Zhu, W., Yang, L., & Ding, N. (2020) · Cell Stress and Chaperones · doi:10.1007/s12192-020-01137-6 · Cited by 12
Dunye Guanxinning Improves Acute Myocardial Ischemia-Reperfusion Injury by Inhibiting Neutrophil Infiltration and Caspase-1 Activity
Zhang, Q. G., Wang, S., Chen, X., Guo, H., Ling, S., & Xu, J. W. (2018) · Mediators of Inflammation · doi:10.1155/2018/4608017 · Cited by 12
Sperm induce macrophage extracellular trap formation via phagocytosis-dependent mechanism
Lu, C., Wu, Z., Gao, H., Li, H., Deng, R., Luo, N., Fan, S., Li, X., He, D., & Zhao, H. (2023) · Biology of Reproduction · doi:10.1093/biolre/ioad068 · Cited by 11
Increased formation of neutrophil extracellular traps induced by autophagy and identification of autophagy‐related biomarkers in systemic lupus erythematosus
Li, M., Weng, L., Yu, D., Yang, G., & Jin, H. (2023) · Experimental Dermatology · doi:10.1111/exd.14881 · Cited by 11
Pseudomonas plecoglossicida infection induces neutrophil autophagy-driven NETosis in large yellow croaker Larimichthys crocea
Cao, J.-F., & Chen, J. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1521080 · Cited by 11
Neutrophils: a new target for postoperative cognitive dysfunction
Cheng, J., Gao, J., Li, J., & Tian, H. M. (2025) · APOPTOSIS · doi:10.1007/s10495-025-02098-w · Cited by 13
Extracellular Traps in Inflammation: Pathways and Therapeutic Targets
Tonello, S., Vercellino, N., D’Onghia, D., Fracchia, A., Caria, G., Sola, D., Tillio, P. A., Sainaghi, P. P., & Colangelo, D. (2025) · Life · doi:10.3390/life15040627 · Cited by 11
Cigarette smoke condensate attenuates phorbol ester-mediated neutrophil extracellular trap formation
Bokaba, R. P., Anderson, R., Theron, A. J., & Tintinger, G. R. (2017) · African Health Sciences · doi:10.4314/ahs.v17i3.33 · Cited by 11
Neutrophils generated in vitro from hematopoietic stem cells isolated from apheresis samples and umbilical cord blood form neutrophil extracellular traps
Kuhikar, R., Khan, N., Khare, S., Fulzele, A., Melinkeri, S. R., Kale, V. P., & Limaye, L. S. (2020) · Stem Cell Research · doi:10.1016/j.scr.2020.102150 · Cited by 11
Autophagy Modulators From Chinese Herbal Medicines: Mechanisms and Therapeutic Potentials for Asthma
Zhang, Y., Wang, X., Zhang, H., Tang, H., Hu, H., Wang, S., Wong, V. K. W., Li, Y., & Deng, J. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.710679 · Cited by 11
Citrulline is not a major determinant of autoantibody reactivity to neutrophil extracellular traps
de Bont, C. M., & Pruijn, G. J. M. (2023) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2022.0249 · Cited by 11
Neutrophil/lymphocyte ratio elevation in renal dysfunction is caused by distortion of leukocyte hematopoiesis in bone marrow
Ito, S., Ohno, Y., Tanaka, T. T., Kobuchi, S., Ayajiki, K., Manabe, E., Masuyama, T., Sakamoto, J.-I., & Tsujino, T. (2019) · Renal Failure · doi:10.1080/0886022x.2019.1597736 · Cited by 11
In vitro Modulatory Effects of Quercetin on Bovine Neutrophil Effector Functions
Chuammitri, P., Amphaiphan, C., & Nojit, P. (2015) · The Thai Journal of Veterinary Medicine · doi:10.56808/2985-1130.2628 · Cited by 11
NETosis-specific cell death: a novel mechanism in the pathogenesis of gouty arthritis
Liu, K., Ma, S., Li, D., Wang, M., Zhao, H., Song, Z., Su, M., Meng, Q., & Zhou, Z. (2025) · European journal of medical research · doi:10.1186/s40001-025-03408-3 · Cited by 11
Rethinking neutrophil extracellular traps
Liu, Y., Ma, Y.-H., Yang, J.-W., Man, J.-W., Wang, H.-B., Li, Y., Liang, C., Cao, J., Chen, S., Li, K.-P., et al. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.110834 · Cited by 12
Grass carp Il-2 promotes neutrophil extracellular traps formation via inducing ROS production and autophagy in vitro
Lv, M., Wang, Y., Yu, J., Kong, Y., Zhou, H. Y., Zhang, A., & Wang, X. (2023) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2023.109261 · Cited by 10
Influence of iron- and zinc-chelating agents on neutrophil extracellular trap formation
Kuźmicka, W., Moskalik, A., Manda‐Handzlik, A., Demkow, U. A., Wachowska, M., & Ciepiela, O. (2021) · Central European Journal of Immunology · doi:10.5114/ceji.2021.106985 · Cited by 10
Endocrine-disrupting chemical exposure augments neutrophilic inflammation in severe asthma through the autophagy pathway
Quoc, Q. L., Cao, T. B. T., Kim, S., Choi, Y., Ryu, M. S., Choi, Y., Park, H., & Shin, Y. S. (2023) · Food and Chemical Toxicology · doi:10.1016/j.fct.2023.113699 · Cited by 10
Dengue virus infection in mice induces bone marrow myeloid cell differentiation and generates Ly6Glow immature neutrophils with modulated functions
Duggal, S., Rawat, S., Siddqui, G., Vishwakarma, P., Samal, S., Banerjee, A. K., & Vrati, S. (2023) · Journal of Leukocyte Biology · doi:10.1093/jleuko/qiad099 · Cited by 11
When Our Best Friend Becomes Our Worst Enemy: The Mitochondrion in Trauma, Surgery, and Critical Illness
Torp, M., Stensløkken, K., & Vaage, J. (2024) · Journal of Intensive Care Medicine · doi:10.1177/08850666241237715 · Cited by 10
Neutrophil Extracellular Traps in Infectious Human Diseases
Zawrotniak, M., Kozik, A., & Rąpała‐Kozik, M. (2017) · InTech eBooks · doi:10.5772/intechopen.68443 · Cited by 12
Charged polyhedral oligomeric silsesquioxanes trigger in vitro METosis via both oxidative stress and autophagy
Tonello, S., Carniato, F., Rizzi, M., Migliario, M., Rocchetti, V., Marchese, L., & Renò, F. (2017) · Life Sciences · doi:10.1016/j.lfs.2017.09.040 · Cited by 10
A1 and A2A adenosine receptors play a protective role to reduce prevalence of autoimmunity following tissue damage
Riff, R., Naamani, O., Mazar, J., Haviv, Y. S., Chaimovitz, C., & Douvdevani, A. (2021) · Clinical & Experimental Immunology · doi:10.1111/cei.13607 · Cited by 10
Tanshinone IIA Improves Acute Gouty Arthritis in Rats through Regulating Neutrophil Activation and the NLRP3 Inflammasome
Xu, L., Liu, X., Zhang, Y., Jia, T., Li, L., Du, Y., Chen, W., & Zhang, S. (2022) · Disease Markers · doi:10.1155/2022/5851412 · Cited by 10
Deficient Neutrophil Extracellular Trap Formation in Patients Undergoing Bone Marrow Transplantation
Glenn, J. W., Cody, M. J., McManus, M. P., Pulsipher, M. A., Schiffman, J. D., & Yost, C. C. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00250 · Cited by 10
Cationic Liposomes Cause ROS Generation and Release of Neutrophil Extracellular Traps
Lotosh, N. Y., Alyaseva, S. O., Малашенкова, И. К., Sorokoumova, G. M., Vasilov, R. G., & Selischeva, A. A. (2019) · Biochemistry (Moscow) Supplement Series A Membrane and Cell Biology · doi:10.1134/s1990747818040074 · Cited by 10
The role of novel programmed cell death in head and neck squamous cell carcinoma: from mechanisms to potential therapies
Xi, Y., Gao, L., Li, S.-M., Sun, K., Chen, P., Cai, Z., Ren, W., & Zhi, K. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1228985 · Cited by 9
Unveiling the nexus: Decoding interactions between regulated cell death and systemic lupus erythematosus pathogenesis for innovative therapeutic avenues
Tan, Q., Huang, W., Zheng, Y., Li, M., Yi, T., & Yu, S. (2024) · Rheumatology & autoimmunity · doi:10.1002/rai2.12104 · Cited by 9
Candida albicans aspartyl protease (Sap6) inhibits neutrophil function via a “Trojan horse” mechanism
Zawrotniak, M., Satała, D., Juszczak, M., Braś, G., & Rąpała‐Kozik, M. (2025) · Scientific Reports · doi:10.1038/s41598-025-91425-x · Cited by 9
Autophagy inhibitors block pathogenic NET release in immune-mediated inflammatory disease without impairing host defence
Nolan, A., Foulkes, D. M., Fairweather, E. E., Alarcon, M. F., Linford, C., Sellin, A., McLaren, Z., Eyers, P. A., & Wright, H. L. (2025) · Rheumatology · doi:10.1093/rheumatology/keaf437 · Cited by 10
Comprehensive analysis of regulated cell death pathways: intrinsic disorder, protein–protein interactions, and cross-pathway communication
Sorokin, O., Hause, F., Wedler, A., Alakhras, T., Bauchspiess, T., Dietrich, A., Günther, W. F., Guha, C., Obika, K. B., Kraft, J., et al. (2025) · APOPTOSIS · doi:10.1007/s10495-025-02161-6 · Cited by 14
Biophysical Changes of Leukocyte Activation (and NETosis) in the Cellular Host Response to Sepsis
Sorrells, M. G., Seo, Y., Magnen, M., Broussard, B. N., Sheybani, R., Shah, A. M., O’Neal, H. R., Tse, H. T. K., Looney, M. R., & Carlo, D. D. (2023) · Diagnostics · doi:10.3390/diagnostics13081435 · Cited by 9
Ultrasound and Redox-Triggered Morphology Transitions of Supramolecular Self-assemblies with pH Responsiveness for Triple-Controlled Release
Yao, H., Yang, T., He, J. W., Du, G., Song, X., Zhang, Y., & Tian, W. J. (2019) · Langmuir · doi:10.1021/acs.langmuir.9b01153 · Cited by 9
Overexpression of ATG5 Gene Makes Granulocyte-Like HL-60 Susceptible to Release Reactive Oxygen Species
Mroczek, A., Cieloch, A., Manda‐Handzlik, A., Kuźmicka, W., Muchowicz, A., & Wachowska, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21155194 · Cited by 9
Bio-impedance measurement allows displaying the early stages of neutrophil extracellular traps
Linnemann, C., Venturelli, S., Konrad, F. M., Nussler, A. K., & Ehnert, S. (2020) · EXCLI journal · doi:10.17179/excli2020-2868 · Cited by 10
Neutrophil extracellular traps (NETs) in a randomized controlled trial of a combination of antiviral and nonsteroidal anti-inflammatory treatment in a bovine model of respiratory syncytial virus infection
Mutua, V. N., Cavallo, F., & Gershwin, L. J. (2021) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2021.110323 · Cited by 9
Autophagy Induced by Palmitic Acid Regulates Neutrophil Adhesion Through the Granule-Dependent Degradation of αMβ2 Integrin in Dairy Cows With Fatty Liver
Peng, Z.-C., Zhao, C.-X., Du, X., Yang, Y., Li, Y., Song, Y.-X., Fang, B., Zhang, Y.-M., Qin, X., Zhang, Y.-Y., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.726829 · Cited by 7
Neutrophil extracellular traps in diseases of the female reproductive organs
Morawiec, M.-L., Kubina, R., Stępień, S., Smycz‐Kubańska, M., Królewska‐Daszczyńska, P., Ratajczak–Wrona, W., & Mielczarek‐Palacz, A. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1589329 · Cited by 9
Shear Stress as a Danger Signal: Inducing Inflammation and Thrombosis via Mechanosensitive NETosis
Baratchi, S., & Peter, K. (2025) · BioEssays · doi:10.1002/bies.70065 · Cited by 8
Autophagy Traps Neutrophils into a Protective Alliance during Sepsis
Laval, J., Singh, A., & Hartl, D. (2017) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201701-0149ed · Cited by 7
Reverse effects of Streptococcus mutans physiological states on neutrophil extracellular traps formation as a strategy to escape neutrophil killing
Huang, L., Lu, W., Yang, N., & Liu, J. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.1023457 · Cited by 8
Deciphering the Genetic Code of Autoimmune Kidney Diseases
Huang, S. U.-S., Kulatunge, O., & O’Sullivan, K. M. (2023) · Genes · doi:10.3390/genes14051028 · Cited by 8
Role of platelets and NETs in arterial thrombosis
Zhang, Y., Ye, J., Sun, S., Li, R., Tang, S., Wang, M., & Sun, G. (2025) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-025-03921-6 · Cited by 8
Oxidative Stress Facilitates IFN-γ-Induced Mimic Extracellular Trap Cell Death in A549 Lung Epithelial Cancer Cells
Lin, C., Chen, C., Chien, S.-Y., Tseng, P., Wang, Y., & Tsai, T.-T. (2016) · PLoS ONE · doi:10.1371/journal.pone.0162157 · Cited by 8
Murine lupus is neutrophil elastase-independent in the MRL.Faslpr model
Gordon, R. A., Tilstra, J. S., Marinov, A. D., Nickerson, K. M., Bastacky, S., & Shlomchik, M. J. (2020) · PLoS ONE · doi:10.1371/journal.pone.0226396 · Cited by 8
Neutrophil extracellular traps: Their role in periodontal disease - (Retracted)
Kolaparthy, L., Sanivarapu, S., Swarna, C., & Devulapalli, N. (2014) · Journal of Indian Society of Periodontology · doi:10.4103/0972-124x.147399 · Cited by 9
Retracted
Emerging paradigms in arterial thrombosis
Wisler, J. W., & Becker, R. C. (2013) · Journal of Thrombosis and Thrombolysis · doi:10.1007/s11239-013-0965-1 · Cited by 8
CD200R1L is a functional evolutionary conserved activating receptor in human neutrophils
Ramos, M. I. P., Keşmir, C., Stok, J. E., Geerdink, R. J., Satravelas, N., Westerlaken, G. H. A., Meyaard, L., & van der Vlist, M. (2021) · Journal of Leukocyte Biology · doi:10.1002/jlb.2a0520-334r · Cited by 6
Multitarget natural compounds taming NETosis: A translational strategy for cancer and inflammatory diseases
Jia, W., Zhang, J., Shang, Y., & Liu, S. (2025) · Cancer Letters · doi:10.1016/j.canlet.2025.218103 · Cited by 7
Techniques for measuring NETosis: A critical literature review and outlook for standardization
Gillot, C., Bouarroudj, H., Decarpentrie, J., Mullier, F., Dogné, J., & Douxfils, J. (2026) · Thrombosis Research · doi:10.1016/j.thromres.2026.109697 · Cited by 7
The Effect of Vitamin D3 on Neutrophil Extracellular Trap Formation in High-Glucose Conditions
Basyreva, L. Y., Shmeleva, E. V., Ivanov, V. A., Vakhrusheva, T. V., Panasenko, O. M., Ostrovsky, E. M., Гусев, С. А., & Сергиенко, В. И. (2023) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-024-05983-7 · Cited by 7
Unveiling the Intricacies of Autophagy in Asthma: Unraveling Novel Therapeutic Avenues
Peng, J., Lu, N., Hua, S., Song, L., & Liu, H. (2024) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2901022 · Cited by 7

Authors: Remijsen, Q., Berghe, T. V., Wirawan, E., Asselbergh, B., Parthoens, E., De Rycke, R., Noppen, S., Delforge, M., Willems, J., & Vandenabeele, P.
Affiliations: KU Leuven (BE)
Ghent University (BE)
Universitair Ziekenhuis Leuven (BE)
Corresponding author: Willems, Jean
Vandenabeele, Peter
ORCID: Berghe, Tom Vanden
Asselbergh, Bob
Noppen, Sam
Delforge, Michel
Vandenabeele, Peter
Venue: Cell Research
Publisher: Springer Science and Business Media LLC
Published: 2010-11-09
Volume: 21
Issue: 2
Pages: 290-304
ISSN: 1001-0602 (ISSN-L)
1748-7838
DOI: 10.1038/cr.2010.150
PMC: PMC3193439
OpenAlex: W2091512988
Cited by: 818
References: 51
Citations by year: 2026: 32 · 2025: 58 · 2024: 50 · 2023: 54 · 2022: 48 · 2021: 68 · 2020: 57 · 2019: 87 · 2018: 56 · 2017: 73 · 2016: 62 · 2015: 49 · 2014: 40 · 2013: 39 · 2012: 31
FWCI: 11.55
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: public-domain
www.springer.com/tdm (tdm)
Locations: Cell Research (publishedVersion, public-domain)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Ghent University Academic Bibliography (Ghent University) (submittedVersion)
Funders: European Commission (200767)
Universiteit Gent (01M00709)
Vlaams Instituut voor Biotechnologie (BOF09/01M00709)
Vlaamse regering (BOF09/01M00709)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Life Sciences › Immunology and Microbiology › Microbiology › Antimicrobial Peptides and Activities
Keywords: neutrophil extracellular traps, NETosis, autophagy, superoxide, NADPH oxidase, chromatin decondensation, neutrophil cell death, apoptosis, chronic granulomatous disease, phorbol myristate acetate, innate immunity
MeSH terms: NADPH Oxidase 2, Autophagy, Granulomatous Disease, Chronic, Humans, Membrane Glycoproteins, NADH, NADPH Oxidoreductases, Neutrophils, Superoxides, Tetradecanoylphorbol Acetate, Apoptosis, NADPH Oxidases, Chromatin Assembly and Disassembly

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Neutrophil extracellular trap cell death requires both autophagy and superoxide generation

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks