Molecular mechanisms of NET formation and degradation revealed by intravital imaging in the liver vasculature
Open accessAbstract
Neutrophil extracellular traps (NETs) composed of DNA decorated with histones and proteases trap and kill bacteria but also injure host tissue. Here we show that during a bloodstream infection with methicillin-resistant Staphylococcus aureus , the majority of bacteria are sequestered immediately by hepatic Kupffer cells, resulting in transient increases in liver enzymes, focal ischaemic areas and a robust neutrophil infiltration into the liver. The neutrophils release NETs into the liver vasculature, which remain anchored to the vascular wall via von Willebrand factor and reveal significant neutrophil elastase (NE) proteolytic activity. Importantly, DNase although very effective at DNA removal, and somewhat effective at inhibiting NE proteolytic activity, fails to remove the majority of histones from the vessel wall and only partly reduces injury. By contrast, inhibition of NET production as modelled by PAD4-deficiency, or prevention of NET formation and proteolytic activity as modelled in NE −/− mice prevent collateral host tissue damage.
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Intravascular NETs can increase local vascular permeability.
“In addition, intravascular NETs can increase local vascular permeability (15), which would permit cancer cells to extravasate more easily.”
From Cancer cells induce metastasis-supporting neutrophil extracellular DNA traps (2016) · cites this paper as [15]
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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
“In patients with COVID-19 injured liver displays patchy necrosis alike in experimental models of the net-damaged liver [128, 129].”
BackgroundSelf-citationThe role of leukocytes in thrombosis
Swystun, L. L., & Liaw, P. C. (2016) · Blood · doi:10.1182/blood-2016-05-718114 · Cited by 301 · see citing works
Neutrophil Extracellular Traps in Arterial and Venous Thrombosis
Laridan, E., Martinod, K., & Meyer, S. F. D. (2019) · Seminars in Thrombosis and Hemostasis · doi:10.1055/s-0038-1677040 · Cited by 293 · see citing works
Primary tumors induce neutrophil extracellular traps with targetable metastasis-promoting effects
Rayes, R. F., Mouhanna, J. G., Nicolau, I. A., Bourdeau, F., Giannias, B., Rousseau, S., Quail, D. F., Walsh, L. A., Sangwan, V., Bertos, N., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.128008 · Cited by 263 · see citing works
Neutrophil Extracellular Traps (NETs) in Cancer Invasion, Evasion and Metastasis
Demkow, U. A. (2021) · Cancers · doi:10.3390/cancers13174495 · Cited by 261 · see citing works
“, who observed the adherence of circulating NETs to blood, resulting in increased cancer extravasation efficiency, which would enable cancer cells to cross the endothelial barrier [61].”
BackgroundIdentification and treatment of the Staphylococcus aureus reservoir in vivo
Surewaard, B. G. J., Deniset, J., Zemp, F. J., Amrein, M., Otto, M. J., Conly, J. M., Omri, A., Yates, R. M., & Kubes, P. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20160334 · Cited by 257 · see citing works
Self-citationNeutrophil Extracellular Traps Drive Endothelial-to-Mesenchymal Transition
Pieterse, E., Rother, N., Garsen, M., Hofstra, J. M., Satchell, S. C., Hoffmann, M. H., Loeven, M. A., Knaapen, H. K. A., van der Heijden, O. W. H., Berden, J. H. M., et al. (2017) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.117.309002 · Cited by 256 · see citing works
Priming of neutrophils toward NETosis promotes tumor growth
Demers, M., Wong, S. L., Martinod, K., Gallant, M., Cabral, J. E., Wang, Y., & Wagner, D. D. (2016) · OncoImmunology · doi:10.1080/2162402x.2015.1134073 · Cited by 252 · see citing works
Nie, M., Yang, L., Bi, X., Wang, Y., Sun, P., Yang, H., Liu, P., Li, Z., Xia, Y., & Jiang, W. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-18-1226 · Cited by 251 · see citing works
“Unlike previous studies, in which NETs lead to metastases via sequestering circulating tumor cells or increasing the permeability of vascular structures (23, 42), we proved that the binding of TLR9 led to the activation of multiple pathways including NFkB, MAPK, and STAT3 pathway in tumor cells.”
ResultPotey, P. M., Rossi, A. G., Lucas, C. D., & Dorward, D. A. (2018) · The Journal of Pathology · doi:10.1002/path.5221 · 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
Chromatin swelling drives neutrophil extracellular trap release
Neubert, E., Meyer, D., Rocca, F., Günay, G., Kwaczala-Tessmann, A., Grandke, J., Senger-Sander, S. N., Geisler, C., Egner, A., Schön, M. P., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06263-5 · Cited by 242 · see citing works
The role of neutrophil extracellular traps in rheumatic diseases
Apel, F., Zychlinsky, A., & Kenny, E. F. (2018) · Nature Reviews Rheumatology · doi:10.1038/s41584-018-0039-z · Cited by 233 · see citing works
Blood coagulation in immunothrombosis—At the frontline of intravascular immunity
Gaertner, F. C., & Maßberg, S. (2016) · Seminars in Immunology · doi:10.1016/j.smim.2016.10.010 · Cited by 233 · see citing works
Splenic Ly6Ghigh mature and Ly6Gint immature neutrophils contribute to eradication of S. pneumoniae
Deniset, J., Surewaard, B. G. J., Lee, W., & Kubes, P. (2017) · The Journal of Experimental Medicine · doi:10.1084/jem.20161621 · Cited by 232 · see citing works
“This splenic tropism is unique to S. pneumoniae infection, as our previous work has shown tremendous preferential sequestration of circulating Staphylococcus aureus, Escherichia coli, and Pseudo- monas aeruginosa by the liver (Kolaczkowska et al., 2015 and unpublished data).”
Self-citationNeutrophils 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
Self-citationNeutrophil 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
Immune determinants of the pre-metastatic niche
Pătraș, L., Shaashua, L., Matei, I. R., & Lyden, D. C. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.02.018 · 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
“Similar findings are also present in work by Kolaczkowska and colleagues where, in a model of b loods t r eam in f e c t i on wi th meth i c i l l in - r e s i s t an t Staphylococcus aureus (MRSA), they demonstrate that significant amount of active histones and NE remained attached to the vasculature wall after DNase…”
ResultSchönrich, G., Raftery, M. J., & Samstag, Y. (2020) · Advances in Biological Regulation · doi:10.1016/j.jbior.2020.100741 · Cited by 221 · see citing works
Peptidylarginine deiminase 4 promotes age-related organ fibrosis
Martinod, K., Witsch, T., Erpenbeck, L., Savchenko, A., Hayashi, H., Cherpokova, D., Gallant, M., Mauler, M., Cifuni, S. M., & Wagner, D. D. (2017) · Journal of Experimental Medicine · doi:10.1084/jem.20160530 · Cited by 218 · see citing works
“Furthermore, neutrophil elastase, a protease that is released along with NETs with its activity maintained (Kolaczkowska et al., 2015), has been shown to directly contribute to lung fibrosis after bleomycin-induced lung injury (Chua et al., 2007).”
BackgroundNeutrophil intrinsic and extrinsic regulation of NETosis in health and disease
Poli, V., & Zanoni, I. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2022.10.002 · Cited by 217 · 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
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
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
Neutrophils in acute inflammation: current concepts and translational implications
Margraf, A., Lowell, C. A., & Zarbock, A. (2021) · Blood · doi:10.1182/blood.2021012295 · Cited by 203 · see citing works
Raup‐Konsavage, W. M., Wang, Y., Wang, W. W., Féliers, D., Ruan, H., & Reeves, W. B. (2017) · Kidney International · doi:10.1016/j.kint.2017.08.014 · Cited by 202 · 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
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
Martinod, K., Witsch, T., Farley, K., Gallant, M., Remold‐O'Donnell, E., & Wagner, D. D. (2016) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.13239 · Cited by 188 · see citing works
Extracellular DNA traps in inflammation, injury and healing
Daniel, C., Leppkes, M., Munoz, L. E., Schley, G., Schett, G. A., & i, M. H. (2019) · Nature Reviews Nephrology · doi:10.1038/s41581-019-0163-2 · Cited by 189 · see citing works
The emerging roles of neutrophil extracellular traps in wound healing
Zhu, S.-N., Yu, Y., Ren, Y., Xu, L.-Y., Wang, H., Ling, X.-M., Jin, L., Hu, Y., Zhang, H., Miao, C., et al. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-04294-3 · Cited by 174 · see citing works
Reactive Oxygen Species Localization Programs Inflammation to Clear Microbes of Different Size
Warnatsch, A., Tsourouktsoglou, T.-D., Branzk, N., Wang, Q., Reincke, S., Herbst, S., Gutierrez, M. G., & Papayannopoulos, V. (2017) · Immunity · doi:10.1016/j.immuni.2017.02.013 · Cited by 183 · see citing works
“To test this hypothesis, we employed mice deficient in the ROS-producing enzyme myeloperoxidase (MPO) that is required for NET formation (Branzk et al., 2014; Kolaczkowska et al., 2015; Metzler et al., 2011, 2014; Papayannopoulos et al., 2010).”
MethodMunir, H., Jones, J. O., Janowitz, T., Hoffmann, M. H., Euler, M., Martins, C. P., Welsh, S. J., & Shields, J. D. (2021) · Nature Communications · doi:10.1038/s41467-021-20982-2 · Cited by 181 · see citing works
Staphylococcus aureus Manipulates Innate Immunity through Own and Host-Expressed Proteases
Pietrocola, G., Nobile, G., Rindi, S., & Speziale, P. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00166 · Cited by 178 · see citing works
“Lastly, some S. aureus secreted molecules can bind and inhibit neutrophil serine proteases which are important for several functions including the regulation of extracellular trap formation (Hu, 2012; Kolaczkowska et al., 2015).”
BackgroundProgrammed Necrosis and Disease:We interrupt your regular programming to bring you necroinflammation
Kim, E. H., Wong, S., & Martinez, J. (2018) · Cell Death and Differentiation · doi:10.1038/s41418-018-0179-3 · Cited by 176 · see citing works
Neutrophil extracellular traps drive inflammatory pathogenesis in malaria
Knackstedt, S. L., Georgiadou, A., Apel, F., Abed, U. A., Moxon, C. A., Cunnington, A. J., Raupach, B., Cunningham, D., Langhorne, J., Krüger, R., et al. (2019) · Science Immunology · doi:10.1126/sciimmunol.aaw0336 · Cited by 171 · see citing works
The gut-liver axis in sepsis: interaction mechanisms and therapeutic potential
Zhang, X., Liu, H., Hashimoto, K., Yuan, S., & Zhang, J. (2022) · Critical Care · doi:10.1186/s13054-022-04090-1 · Cited by 200 · see citing works
Tatsiy, O., & McDonald, P. P. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02036 · Cited by 167 · see citing works
Neutrophil and remnant clearance in immunity and inflammation
Singhal, A., & Kumar, S. (2021) · Immunology · doi:10.1111/imm.13423 · Cited by 156 · see citing works
The role of neutrophil extracellular traps in cancer progression and metastasis
Meo, M. L. D., & Spicer, J. D. (2021) · Seminars in Immunology · doi:10.1016/j.smim.2022.101595 · Cited by 158 · see citing works
The Pathophysiological Role of Neutrophil Extracellular Traps in Inflammatory Diseases
Bonaventura, A., Liberale, L., Carbone, F., Vecchié, A., Díaz-Cañestro, C., Camici, G. G., Montecucco, F., & Dallegri, F. (2018) · Thrombosis and Haemostasis · doi:10.1160/th17-09-0630 · Cited by 154 · see citing works
“192 Since IL-8 has been demonstrated to play a role in NET generation and angiogenesis, a clear clinical relevance for IL-8 in tumour progression has been shown for many tumours, too.”
BackgroundMacrophage inflammatory protein-2 as mediator of inflammation in acute liver injury
Qin, C.-C., Liu, Y.-N., Hu, Y., Yang, Y., & Chen, Z. J. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i17.3043 · Cited by 148 · see citing works
Neonatal NET-inhibitory factor and related peptides inhibit neutrophil extracellular trap formation
Yost, C. C., Schwertz, H., Cody, M. J., Wallace, J. A., Campbell, R. A., Vieira‐de‐Abreu, A., de Araujo, C. V., Schubert, S., Harris, E. S., Rowley, J. W., et al. (2016) · Journal of Clinical Investigation · doi:10.1172/jci83873 · Cited by 151 · see citing works
α-Toxin Induces Platelet Aggregation and Liver Injury during Staphylococcus aureus Sepsis
Surewaard, B. G. J., Thanabalasuriar, A., Zeng, Z., Tkaczyk, C., Cohen, T. S., Bardoel, B. W., Jorch, S. K., Deppermann, C., Wardenburg, J. B., Davis, R. P., et al. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.06.017 · Cited by 147 · see citing works
“Importantly, non-perfused liver areas will ultimately lead to tissue damage, focal necrotic lesions and organ failure (Kolaczkowska et al., 2015).”
Self-citationLazzaretto, B., & Fadeel, B. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1800159 · Cited by 146 · see citing works
Wong, S. L., & Wagner, D. D. (2018) · The FASEB Journal · doi:10.1096/fj.201800691r · Cited by 145 · see citing works
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 142 · see citing works
“…x H u m a n G o u t y J o i n t , c y t o s p i n s y n o v i a l fl u i d I mm u n o fl u o r e s c e n c e m i c r o s c o p y [ 1 4 ] x M u r i n e M S U i n d u c e d a gg N E T s I n t r a p e r i t o n e a l a gg r e g a t e s I mm u n o h i s t o c h e m i c a l m i c r o s c o p y [ 77 ] x”
Imaging the dynamic platelet‐neutrophil response in sterile liver injury and repair in mice
Slaba, I., Wang, J., Kołaczkowska, E., McDonald, B., Lee, W., & Kubes, P. (2015) · Hepatology · doi:10.1002/hep.28003 · Cited by 135 · see citing works
Self-citationNeutrophil Recruitment: From Model Systems to Tissue-Specific Patterns
Margraf, A., Ley, K. F., & Zarbock, A. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.04.010 · Cited by 135 · see citing works
“In mouse models of systemic bacterial infection -- such as via intravenously injected MRSA -- CD44-dependent neutrophil recruitment within the liver has been noted, where NETs can promote liver damage [76].”
BackgroundAdrover, J. M., Carrau, L., Daßler‐Plenker, J., Bram, Y., Chandar, V., Houghton, S., Redmond, D., Merrill, J. R., Shevik, M. E., tenOever, B. R., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.157342 · Cited by 128 · see citing works
“DNase I degradation of the DNA backbone of NETs has been reported to leave several other components of NETs in situ, including proteases and histones (70), and these may be detrimental in certain contexts (71).”
BackgroundYang, J., Wu, Z., Long, Q., Huang, J., Hong, T., Liu, W., & Lin, J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.610696 · Cited by 121 · see citing works
“Blocking VWF by antibody or cleaving VWF by ADAMTS13 did not affect neutrophil recruitment, but markedly prevented the accumulation of DNA fibers, decreased the amount of histone and elastase, and attenuated the tissue damage in liver sinusoid, supporting that the reduction of hepatic damage was due to the disruption…”
BackgroundMicrovascular thrombosis: experimental and clinical implications
Bray, M. A., Sartain, S. E., Gollamudi, J., & Rumbaut, R. E. (2020) · Translational research · doi:10.1016/j.trsl.2020.05.006 · Cited by 119 · see citing works
“Two examples include defining the role of platelets in bacterial clearance in the liver during blood-borne infection and characterizing formation of neutrophil extracellular traps in vivo during infection.(100,101) Biochemical stimulation.”
BackgroundSuperoxide induces Neutrophil Extracellular Trap Formation in a TLR-4 and NOX-Dependent Mechanism
Al‐Khafaji, A. B., Tohme, S. T., Yazdani, H. O., Miller, D., Huang, H., & Tsung, A. (2016) · Molecular Medicine · doi:10.2119/molmed.2016.00054 · Cited by 115 · see citing works
Mohanty, T., Fisher, J., Bakochi, A., Neumann, A., Cardoso, J. F. P., Karlsson, C. A. Q., Pavan, C., Lundgaard, I., Nilson, B., Reinstrup, P., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09040-0 · Cited by 111 · see citing works
Candida albicans-Induced NETosis Is Independent of Peptidylarginine Deiminase 4
Guiducci, E., Lemberg, C., Küng, N., Schraner, E. M., Theocharides, A. P. A., & LeibundGut‐Landmann, S. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01573 · Cited by 107 · see citing works
“To overcome these tissue-specific limitations, most in vivo studies on NETs focused on the lung or the vasculature (13, 15, 75).”
Claushuis, T. A. M., van der Donk, L. E. H., Luitse, A. L., van Veen, H. A., van der Wel, N. N., van Vught, L. A., Roelofs, J. J. T. H., de Boer, O. J., Lankelma, J. M., Boon, L., et al. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1800314 · Cited by 110 · see citing works
In vivo evidence for extracellular DNA trap formation
Yousefi, S., Simon, D., Stojkov, D., Васильевна, К. А., Karaulov, A. V., & Simon, H. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-2497-x · Cited by 111 · see citing works
“Intravenous infection with multi-resistant Staphylococcus aureus led to a rapid sequestration of the bacteria to the liver, neutrophil recruitment and NET formation within the liver sinusoids, and subsequent liver damage 14 .”
BackgroundVascular Endothelial Damage in the Pathogenesis of Organ Injury in Severe COVID-19
Dupont, A., Rauch, A., Staessens, S., Moussa, M. D., Rosa, M., Corseaux, D., Jeanpierre, E., Goutay, J., Caplan, M., Varlet, P., et al. (2021) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.120.315595 · Cited by 106 · see citing works
“Chronic pulmonary disease 21 (26) 1 (10) 15 (25) 14 (35) 8 (26) 5 (22) 16 (32) 7 (32)”
van der Linden, M., Westerlaken, G. H. A., van der Vlist, M., van Montfrans, J. M., & Meyaard, L. (2017) · Scientific Reports · doi:10.1038/s41598-017-06901-w · Cited by 105 · see citing works
NETs-Induced Thrombosis Impacts on Cardiovascular and Chronic Kidney Disease
Thakur, M., Junho, C. V. C., Bernhard, S., Schindewolf, M., Noels, H., & Döring, Y. (2023) · Circulation Research · doi:10.1161/circresaha.123.321750 · Cited by 106 · see citing works
Role of platelets in neutrophil extracellular trap (NET) production and tissue injury
Kim, S., & Jenne, C. N. (2016) · Seminars in Immunology · doi:10.1016/j.smim.2016.10.013 · Cited by 104 · see citing works
Self-citationNeutrophil Extracellular Traps Impair Intestinal Barrier Function during Experimental Colitis
Lin, E. Y.-H., Lai, H.-J., Cheng, Y.-K., Leong, K.-Q., Cheng, L.-C., Chou, Y., Peng, Y.-C., Hsu, Y.-H., & Chiang, H.-S. (2020) · Biomedicines · doi:10.3390/biomedicines8080275 · Cited by 104 · see citing works
“It is also worth mentioning that an intravital imaging-based study has shown although DNase I completely degrades DNA, it fails to remove NET-associated proteins, including histones from the endothelial wall and thus is less protective against systematic inflammation [49].”
BackgroundNeutrophil Extracellular Traps in Colorectal Cancer Progression and Metastasis
Khan, U., Chowdhury, S., Billah, M. M., Islam, K. M. D., Thorlacius, H., & Rahman, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147260 · Cited by 108 · see citing works
“In contrast, one recent study has reported the failure of DNase to eliminate NET associated harmful proteases or histones [108], which are known to cause tissue damage [111].”
BackgroundMurthy, P., Singhi, A. D., Ross, M. A., Loughran, P., Paragomi, P., Papachristou, G. I., Whitcomb, D. C., Zureikat, A. H., Lotze, M. T., Zeh, H. J., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00028 · Cited by 105 · see citing works
“As a “late” inhibitor of NET formation, DNase treatment does not prevent NET formation and does little to counter-act the effects of the release of other NET components, including histones, HMGB1, elastase and other factors (40).”
BackgroundActivated αIIbβ3 on platelets mediates flow-dependent NETosis via SLC44A2
Constantinescu-Bercu, A., Grassi, L., Frontini, M., Salles-Crawley, I. I., Woollard, K., & Crawley, J. T. (2018) · bioRxiv · doi:10.7554/elife.53353 · Cited by 84 · see citing works
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“Murine PMNs isolated from bone marrow are capable of releasing NETs both in vitro [58] and in vivo [59].”
BackgroundSurendran, V., Rutledge, D., Colmon, R., & Chandrasekaran, A. (2021) · Biofabrication · doi:10.1088/1758-5090/abe1cf · Cited by 99 · see citing works
“that intravascular NETs can increase local vascular permeability [87, 88], which would permit cancer cells to extravasate more easily.”
BackgroundResolvin D4 attenuates the severity of pathological thrombosis in mice
Cherpokova, D., Jouvene, C. C., Libreros, S., DeRoo, E., Chu, L., de la Rosa, X., Norris, P. C., Wagner, D. D., & Serhan, C. N. (2019) · Blood · doi:10.1182/blood.2018886317 · Cited by 97 · see citing works
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Lupus and proliferative nephritis are PAD4 independent in murine models
Gordon, R. A., Herter, J. M., Rosetti, F., Campbell, A. M., Nishi, H., Kashgarian, M. J., Bastacky, S., Marinov, A. D., Nickerson, K. M., Mayadas, T. N., et al. (2017) · JCI Insight · doi:10.1172/jci.insight.92926 · Cited by 94 · see citing works
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- Authors
- Kolaczkowska, E., Jenne, C. N., Surewaard, B. G. J., Thanabalasuriar, A., Lee, W.-Y., Sanz, M.-J., Mowen, K., Opdenakker, G., & Kubes, P.
- Affiliations
- University of Calgary (CA)
- Scripps Research Institute (US)
- Rega Institute for Medical Research (BE)
- Corresponding author
- Kubes, Paul
- ORCID
- Venue
- Nature Communications
- Published
- 2015-03-26
- Volume
- 6
- Issue
- 1
- Pages
- 6673-6673
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC4389265
- OpenAlex
- W2034808365
- Cited by
- 584
- References
- 63
- Citations by year
- 2026: 38 · 2025: 53 · 2024: 55 · 2023: 57 · 2022: 61 · 2021: 67 · 2020: 63 · 2019: 58 · 2018: 50 · 2017: 39 · 2016: 38 · 2015: 5
- FWCI
- 21.70
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Homo Politicus (Academy of Humanities and Economics in Lodz) (submittedVersion, cc-by-nc-nd)
- Lirias (KU Leuven) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Alberta Innovates - Health Solutions
- European Commission (273340, 627575)
- Canada Research Chairs
- Alberta Innovates
- Canadian Institutes of Health Research
- FP7 People: Marie-Curie Actions (FP7-PEOPLE-2013, FP7-PEOPLE-2013-IOF)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Inflammation biomarkers and pathways
- Life Sciences › Immunology and Microbiology › Microbiology › Antimicrobial Peptides and Activities
- Keywords
- neutrophil extracellular traps, NET degradation, methicillin-resistant Staphylococcus aureus, bloodstream infection, Kupffer cells, liver vasculature, neutrophil elastase, DNase, histone removal, von Willebrand factor, PAD4, neutrophil infiltration, hepatic ischemia, host tissue damage, intravital imaging
- MeSH terms
- Protein-Arginine Deiminase Type 4, Animals, Deoxyribonucleases, Hepatic Artery, Hepatic Veins, Histones, Hydrolases, Kupffer Cells, Liver, Male, Staphylococcal Infections, von Willebrand Factor, Bacteremia, Mice, Knockout, Leukocyte Elastase, Neutrophil Infiltration, Mice, Methicillin-Resistant Staphylococcus aureus, Extracellular Traps
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 ›
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