Neutrophil extracellular traps: structure and biological role

Abstract

Neutrophilic granulocytes make up the majority of blood leukocytes and realize their functions in tissues. Highly differentiated cells of neutrophilic granulocytic differon are characterized by the ability to form neutrophilic extracellular traps (NEТs) — network-like structures formed mainly from the intracellular components of the neutrophil. NEТs are an important factor in the body's defense against infectious pathogens, aimed at the destruction of viruses, bacteria, fungi and protozoa. Analyzed the composition of NEТs, methods of detection, mechanisms and main stages of their formation: 1) the effect of the inductor on the neutrophilic granulocyte and the activation of the respiratory burst with the release of reactive oxygen species (oxygen superoxide); 2) loss of the characteristic segmentation of the nucleus, decondensation of chromatin; 3) the disintegration of the karyolemma into many small vesicles, the movement of chromatin strands (DNA with histone proteins) into the cytoplasm; 4) the formation of NEТs due to the connection of chromatin with numerous biologically active substances of the cytoplasm (mainly from lysed granules); 5) destruction of the plasmolemma and the release of NEТs into the intercellular environment. Data on the participation of NEТs in protective reactions and pathological processes are presented.

Keywords

neutrophil granulocytes / neutrophil extracellular traps / leukocytes / netosis / phagocytosis / degranulation

References

[1] Pigarevskij VE, Mazing JuA. Lizosomal'no-kationnyj test (metodicheskoe pis'mo). Leningrad: NIIJeM; 1987.

[2] Пигаревский В.Е., Мазинг Ю.А. Лизосомально-катионный тест (методическое письмо). Ленинград : НИИЭМ, 1987.

[3] Majanskij AN. Patogeneticheskaja mikrobiologija. Nizhny Novgorod: Izdatel'stvo NGMA; 2006.

[4] Маянский А.Н. Патогенетическая микробиология. Нижний Новгород : Издательство НГМА, 2006.

[5] Akmaev IG, Afanas'ev JuI, Bobova LP, i dr. Rukovodstvo po gistologii. V 2 t. Danilov RK, Bykov VL, editors. Saint Petersburg: SpecLit, 2011. 495 p.

[6] Акмаев И.Г., Афанасьев Ю.И., Бобова Л.П., и др. Руководство по гистологии. В 2 т. / под ред. Р.К. Данилова, В.Л. Быкова. Санкт-Петербург : СпецЛит, 2011. 495 с.

[7] Nesterova IV, Kolesnikova NV, Chudilova GA, et al. The new look at neutrophilic granulocytes: rethinking old dogmas. Part 1. Russian Journal of Infection and Immunity (Infektsiya i immunitet). 2017;7(3):219–230. doi: 10.15789/2220-7619-2017-3-219-230

[8] Нестерова И.В., Колесникова Н.В., Чудилова Г.А., и др. Гранулоциты: переосмысление старых догм. Часть 1 // Инфекция и иммунитет. 2017. Т. 3, № 3. С. 219–230. doi: 10.15789/2220-7619-2017-3-219-230

[9] Simbircev AS, Totoljan AA. Citokiny v laboratornoj diagnostike. In: Dolgov VV, Menshikov VV. Klinicheskaja laboratornaja diagnostika: nacional'noe rukovodstvo v 2 t. Moscow: GJeOTAR-Media; 2013. Vol. 2. P. 193–217.

[10] Симбирцев А.С., Тотолян А.А. Цитокины в лабораторной диагностике. В кн.: Долгов В.В., Меншиков В.В. Клиническая лабораторная диагностика: национальное руководство в 2 т. Москва : ГЭОТАР-Медиа, 2013. Т. 2. С. 193–217.

[11] Korotina OL, Generalov II. Neutrophil extracellular traps: mechanisms of formation, functions. Immunopathology, Allergology, Infectology. 2012;(4):23–32.

[12] Коротина О.Л., Генералов И.И. Нейтрофильные внеклеточные ловушки: механизмы образования, функции // Иммунопатология, аллергология, инфектология. 2012. № 4. С. 23–32.

[13] Brinkmann V, Rechard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532–1535. doi: 10.1126/science.1092385

[14] Brinkmann V., Rechard U., Goosmann C., et al. Neutrophil extracellular traps kill bacteria // Science. 2004. Vol. 303, N 5663. P. 1532–1535. doi: 10.1126/science.1092385

[15] Brinkmann V. Neutrophil extracellular traps in the second decade. J Innate Immun. 2018;10(5-6):414–421. doi: 10.1159/000489829

[16] Brinkmann V. Neutrophil extracellular traps in the second decade // J Innate Immun. 2018. Vol. 10, N 5-6. P. 414–421. doi: 10.1159/000489829

[17] Takei H, Araki A, Watanabe H, et al. Rapid killing of human neutrophils by the potent activator phorbol 12-myristate 13-acetate (PMA) accompanied by changes different from typical apoptosis or necrosis. J Leukoc Biol. 1996;59(2):229–240. doi: 10.1002/jlb.59.2.229

[18] Takei H., Araki A., Watanabe H., et al. Rapid killing of human neutrophils by the potent activator phorbol 12-myristate 13-acetate (PMA) accompanied by changes different from typical apoptosis or necrosis // J Leukoc Biol. 1996. Vol. 9, N 2. 229–240. doi: 10.1002/jlb.59.2.229

[19] Dolgushin II, Shishkova JuS, Kurnosenko IV, et al. Participation of extracellular DNA traps in protective and pathological reactions of the organism. Russian Journal of Immunology. 2015;9(2):164–170.

[20] Долгушин И.И., Савочкина А.Ю., Курносенко И.В., и др. Участие внеклеточных ДНК-ловушек в защитных и патологических реакциях организма // Российский иммунологический журнал. 2015. Т. 9, № 2. С. 164–170.

[21] Vorobjeva NV. Neutrophil extracellular traps: new aspects. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2020;75(4):210–225.

[22] Воробьёва Н.В. Нейтрофильные внеклеточные ловушки: новые аспекты // Вестник Московского университета. Серия 16. Биология. 2020. Т. 75, № 4. С. 210–225.

[23] Wang Y, Li M, Stadler S, et al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol. 2009;184(2):205–213. doi: 10.1083/jcb.200806072

[24] Wang Y., Li M., Stadler S., et al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation // J Cell Biol. 2009. Vol. 184, N 2. P. 205–213. doi: 10.1083/jcb.200806072

[25] Delgado-Rizo V, Martínez-Guzmán MA, Iñiguez-Gutierrez L, et al. Neutrophil extracellular traps and its implications in inflammation. Front Immunol. 2017;8:81. doi: 10.3389/fimmu.2017.00081

[26] Delgado-Rizo V., Martínez-Guzmán M.A., Iñiguez-Gutierrez L., et al. Neutrophil extracellular traps and its implications in inflammation // Front Immunol. 2017. Vol. 8. P. 81. doi: 10.3389/fimmu.2017.00081

[27] Masuda S, Nakazawa D, Shida H, et al. NETosis markers: quest for specific, objective, and quantitative markers. Clin Chim Acta. 2016;459:89–93. doi: 10.1016/j.cca.2016.05.029

[28] Masuda S., Nakazawa D., Shida H., et al. NETosis markers: quest for specific, objective, and quantitative markers // Clin Chim Acta. 2016. Vol. 459. P. 89–93. doi: 10.1016/j.cca.2016.05.029

[29] Nakazawa D, Kudo T. Novel therapeutic strategy based on neutrophil subset and its function in autoimmune disease. Front Pharmacol. 2021;12:6848–6886. doi: 10.3389/fphar.2021.684886

[30] Nakazawa D., Kudo T. Novel therapeutic strategy based on neutrophil subset and its function in autoimmune disease // Front Pharmacol. 2021. Vol. 12. P. 684886. doi: 10.3389/fphar.2021.684886

[31] Vorobjeva NV, Pinegin BV. Neutrophil extracellular traps: mechanisms of formation and role in health and disease. Biochemistry (Moscow). 2014;79(12):1286–1296.

[32] Воробьёва Н.В., Пинегин Б.В. Нейтрофильные внеклеточные ловушки: механизмы образования, роль в норме и при патологии // Биохимия. 2014. Т. 79, № 12. С. 1580–1591.

[33] Alhede M, Qvortrup K, Kragh KN, et al. The origin of extracellular DNA in bacterial bio-film infections in vivo. Pathog Dis. 2020;78(2):ftaa018. doi: 10.1093/femspd/ftaa018

[34] Alhede M., Qvortrup K., Kragh K., et al. The origin of extracellular DNA in bacterial bio-film infections in vivo // Pathogens Dis. 2020. Vol. 78, N 2. P. ftaa018. doi: 10.1093/femspd/ftaa018

[35] Khan MA, Ali ZS, Sweezey N, et al. Progression of cystic fibrosis lung disease from childhood to adulthood: neutrophils, neutrophil extracellular trap (NET) formation, and NET degradation. Genes (Basel). 2019;10(3):183. doi: 10.3390/genes10030183

[36] Khan M.A., Ali Z.S., Sweezey N., et al. Progression of cystic fibrosis lung disease from childhood to adulthood: neutrophils, neutrophil extracellular trap (NET) formation, and NET degradation // Genes (Basel). 2019. Vol. 10, N 3. P. 183. doi: 10.3390/genes10030183

[37] Mayadas TN, Tsokos GC, Tsuboi N. Mechanism sofImmune complex mediated neutrophil recruitmentand tissue injury. Circulation. 2009;120(20):2012–2024. doi: 10.1161/CIRCULATIONAHA.108.771170

[38] Mayadas T.N., Tsokos G.C., Tsuboi N. Mechanism sofImmune complex mediated neutrophil recruitmentand tissue injury // Circulation. 2009. Vol. 120, N 20. P. 2012–2024. doi: 10.1161/CIRCULATIONAHA.108.771170

[39] Ravindran M, Khan MA, Palaniyar N. Neutrophil extracellular trap formation: physiology, pathology, and pharmacology. Biomolecules. 2019;9(8):365. doi: 10.3390/biom9080365

[40] Ravindran M., Khan M.A., Palaniyar N. Neutrophil extracellular trap formation: physiology, pathology, and pharmacology // Biomolecules. 2019. Vol. 9, N 8. P. 365. doi: 10.3390/biom9080365

[41] Sollberger G, Choidas A, Bum GL, et al. Gasdermin D plays a vital role in the generation of neutrophil extracellular traps. Sci Immunol. 2018;3(26):eaar6689. doi: 10.1126/sciimmunol.aar6689

[42] Sollberger G., Choidas A., Bum G.L., et al. Gasdermin D plays a vital role in the generation of neutrophil extracellular traps // Sci Immunol. 2018. Vol. 3, N 26. P. eaar6689. doi: 10.1126/sciimmunol.aar6689

[43] Kravtsov AL. Formation of extracellular traps — the effective mechanism of organism protection from pathogen. Problems of Particularly Dangerous Infections. 2012;(112):69–74.

[44] Кравцов А.Л. Формирование внеклеточных ловушек — эффективный механизм защиты организма от патогена // Проблемы особо опасных инфекций. 2012. № 112. С. 69–74.

[45] Dolgushin II, Mezentseva EA. Neutrophil extracellular traps in the fight against biofilm-forming microorganisms: hunters or prey? Journal of Microbiology, Epidemiology and Immunobiology. 2020;97(5):468–481. doi: 10.36233/0372-9311-2020-97-5-9

[46] Долгушин И.И., Мезенцева Е.А. Нейтрофильные внеклеточные ловушки в борьбе с биопленкообразующими микроорганизмами: охотники или добыча? // Журнал микробиологии, эпидемиологии и иммунобиологии. 2020. Т. 97, № 5. С. 468–481. doi: 10.36233/0372-9311-2020-97-5-9

[47] Urban CF, Reichard U, Brinkmann V, et al. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol. 2006;8(4):668–676. doi: 10.1111/j.1462-5822.2005.00659.x

[48] Urban C.F., Reichard U., Brinkmann V., Zychlinsky A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms // Cell Microbiol. 2006. Vol. 8, N 4. P. 668–676. doi: 10.1111/j.1462-5822.2005.00659.x

[49] Healy LD, Puy C, Fernández JA, et al. Activated protein C inhibits neutrophil extracellular trap formation in vitro and activation in vivo. J Biol Chem. 2017;292(21):8616–8629. doi: 10.1074/jbc.M116.768309

[50] Healy L.D., Puy C., Fernández J.A., et al. Activated protein C inhibits neutrophil extracellular trap formation in vitro and activation in vivo // J Biol Chem. 2017. Vol. 292, N 21. P. 8616–8629. doi: 10.1074/jbc.M116.768309

[51] Díaz-Godínez C, Carrero JC. The state of art of neutrophil extracellular traps in protozoan and helminthic infections. Biosci Rep. 2019;39(1):BSR20180916. doi: 10.1042/BSR20180916

[52] Díaz-Godínez C., Carrero J.C. The state of art of neutrophil extracellular traps in protozoan and helminthic infections // Biosci Rep. 2019. Vol. 39, N 1. P. BSR20180916. doi: 10.1042/BSR20180916

[53] Mehrpouya-Bahrami P, Moriarty AK, De Melo P, et al. STS4 is expressed in neutrophils and promotes antimicrobial immunity. JCI Insight. 2021;6(14):e141326. doi: 10.1172/jci.insight.141326

[54] Mehrpouya-Bahrami P., Moriarty A.K., De Melo P., et al. STS4 is expressed in neutrophils and promotes antimicrobial immunity // JCI Insight. 2021. Vol. 6, N 14. P. e141326. doi: 10.1172/jci.insight.141326

[55] Kubatiev AA, Borovaya TG, Zhukhovitskii VG. Platelets: a modern view on the structure and function. Pathogenesis. 2016;14(1):4–13.

[56] Кубатиев А.А., Боровая Т.Г., Жуховицкий В.Г., и др. Тромбоциты: современный взгляд на структуру и функции // Патогенез. 2016. Т. 14, № 1. С. 4–13.

[57] Kassina DV, Vasilenko IA, Gur’ev AS, et al. Neutrophil extracellular traps: diagnostic and prognostic value in COVID-19. Almanac of Clinical Medicine. 2020;48(S1):43–50.

[58] Кассина Д.В., Василенко И.А., Гурьев А.С., и др. Нейтрофильные внеклеточные ловушки: значение для диагностики и прогноза COVID-19 // Альманах клинической медицины. 2020. Т. 48, № 1. С. S43–S50. doi: 10.18786/2072-0505-2020-48-029

[59] Tomar B, Anders HJ, Desai J, et al. Neutrophils and neutrophil extracellular traps drive necroinflammation in COVID-19. Cells. 2020;9(6):1383. doi: 10.3390/cells9061383

[60] Tomar B., Anders H.J., Desai J., et al. Neutrophils and neutrophil extracellular traps drive necroinflammation in COVID-19 // Cells. 2020. Vol. 9, N 6. P. 1383. doi: 10.3390/cells9061383

[61] Vitkov L, Knopf J, Krunic´ J, et al. Periodontitis-derived dark-NETs in severe Covid-19. Front Immunol. 2022;13:872695. doi: 10.3389/fimmu.2022.872695

[62] Vitkov L., Knopf J., Krunic´ J., et al. Periodontitis-derived dark-NETs in severe Covid-19 // Front Immunol. 2022. Vol. 13. P. 872695. doi: 10.3389/fimmu.2022.872695

[63] Chen T, Li Y, Sun R, et al. Receptor-mediated NETosis on neutrophils. Front Immunol. 2021;12:775267. doi: 10.3389/fimmu.2021.775267

[64] Chen T., Li Y., Sun R., et al. Receptor-mediated NETosis on neutrophils // Front Immunol. 2021. Vol. 12. P. 7752–7767. doi: 10.3389/fimmu.2021.775267

[65] Steinberg BE, Grinstein S. Unconventional roles of the NADPH-oxidase: signaling, ion homeostasis, and cell death. Sci STKE. 2007;2007(379):pe11. doi: 10.1126/stke.3792007pe11

[66] Steinberg B.E., Grinstein S. Unconventional roles of the NADPH-oxidase: signaling, ion homeostasis, and cell death // Sci STKE. 2007. Vol. 2007, N 379. P. 11. doi: 10.1126/stke.3792007pe11

[67] Takishita Y, Yasuda H, Shimizu M, et al. Formation of neutrophil extracellular traps in mitochondrial DNA-deficient cells. J Clin Biochem Nutr. 2020;66(1):15–23. doi: 10.3164/jcbn.19-77

[68] Takishita Y., Yasuda H., Shimizu M., et al. Formation of neutrophil extracellular traps in mitochondrial DNA-deficient cells // J Clin Biochem Nutr. 2020. Vol. 66, N 1. P. 15–23. doi: 10.3164/jcbn.19-77

[69] Vorobyova NV, Kondratenko IV, Vakhlyarskaya SS, et al. The role of the mitochondrial pore in the effector functions of human neutrophils. Immunologiya. 2020;41(1):42–53. doi: 10.33029/0206-4952-2020-41-1-42-53

[70] Воробьева Н.В., Кондратенко И.В., Вахлярская С.С., и др. Роль митохондриальной поры в эффекторных функциях нейтрофилов человека // Иммунология. 2020. Т. 41, № 1. С. 42–53. doi: 10.33029/0206-4952-2020-41-1-42-53

[71] Fadeel B. Babies born without safety NET. Blood. 2009;113(25):6270–6271. doi: 10.1182/blood-2009-03-210328

[72] Fadeel B. Babies born without safety NET // Blood. 2009. Vol. 113, N 25. P. 6270–6271. doi: 10.1182/blood-2009-03-210328

[73] Yipp BG, Kubes P. NETosis: how vital is it? Blood. 2013;122(16):2784–2794. doi: 10.1182/blood-2013-04-457671

[74] Yipp B.G., Kubes P. NETosis: how vital is it? // Blood. 2013. Vol. 122, N 16. P. 2784–2794. doi: 10.1182/blood-2013-04-457671

[75] Neeli I, Dwivedi N, Khan S, et al. Regulation of extracellular chromatin release from neutrophils. J Innate Immun. 2009;1(3):194–201. doi: 10.1159/000206974

[76] Neeli I., Dwivedi N., Khan S., Radic M. Regulation of extracellular chromatin release from neutrophils // J Innate Immun. 2009. Vol. 1, N 3. P. 194–201. doi: 10.1159/000206974

[77] Fuchs TA, Abed U, Goosmann C, et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol. 2007;176(2):231–241. doi: 10.1083/jcb.200606027

[78] Fuchs T.A., Abed U., Goosmann C., et al. Novel cell death program leads to neutrophil extracellular traps // J Cell Biol. 2007. Vol. 176, N 2. P. 231–241. doi: 10.1083/jcb.200606027

[79] Kenny E.F, Herzig A, Kruger R, et al. Diverse stimuli engage different neutrophil extracellular trap pathways. Elife. 2017;6:e24437. doi: 10.7554/eLife.24437

[80] Kenny E.F., Herzig A., Kruger R., et al. Diverse stimuli engage different neutrophil extracellular trap pathways // Elife. 2017. Vol. 6. P. e24437. doi: 10.7554/eLife.24437

[81] Brinkmann V, Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol. 2007;5(8):577–582. doi: 10.1038/nrmicro1710

[82] Brinkmann V., Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs // Nat Rev Microbiol. 2007. Vol. 5, N 8. P. 577–582. doi: 10.1038/nrmicro1710

[83] Pleskova SN, Kryukov RN. Proinflammatory mechanisms of neutrophil granulocyte death. Tsitologiya. 2019;61(5):357–369. doi: 10.1134/S0041377119050031

[84] Плескова С.Н., Крюков Р.Н. Провоспалительные механизмы гибели нейтрофильных гранулоцитов // Цитология. 2019. Т. 61, № 5. С. 357–369. doi: 10.1134/S0041377119050031

[85] Pleskova SN, Gorshkova EN, Boryakov AV, Kriukov RN. Morphological characteristics of rapid and classical netosis. Tsitologiya. 2019;61(9):704–712. doi: 10.1134/S0041377119090098

[86] Плескова С.Н., Горшкова Е.Н., Боряков А.В., Крюков Р.Н. Морфологические особенности быстрого и классического нетоза // Цитология. 2019. Т. 61, № 9. С. 704–712. doi: 10.1134/S0041377119090098

[87] Azzouz D, Palaniyar N. ROS and DNA repair in spontaneous versus agonist-induced NETosis: context matters. Front Immunol. 2022;13:1033815. doi: 10.3389/fimmu.2022.1033815

[88] Azzouz D., Palaniyar N. ROS and DNA repair in spontaneous versus agonist-induced NETosis: context matters // Front Immunol. 2022. Vol. 13. P. 1033815. doi: 10.3389/fimmu.2022.1033815

[89] Farrera C, Fadeel B. Macrophage clearance of neutrophil extracellular traps is a silent process. J Immunol. 2013;191(5):2647–2656. doi: 10.4049/jimmunol.1300436

[90] Farrera C., Fadeel B. Macrophage clearance of neutrophil extracellular traps is a silent process // J Immunol. 2013. Vol. 191, N 5. P. 2647–2656. doi: 10.4049/jimmunol.1300436

[91] von Köckritz-Blickwede M, Goldmann O, Thulin P, et al. Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood. 2008;111(6):3070–3080. doi: 10.1182/blood-2007-07-104018

[92] von Köckritz-Blickwede M., Goldmann O., Thulin P., et al. Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation // Blood. 2008. Vol. 111, N 6. P. 3070–3080. doi: 10.1182/blood-2007-07-104018

[93] Dvorski R, Simon HU, Hoskins A, Yousefi S. Eosinofil and neutrophil extracellular traps in human allergic asthmatic airways. J Allergy Clin Immunol. 2011;127(5):1260–1266. doi: 10.1016/j.jaci.2010.12.1103

[94] Dvorski R., Simon H.U., Hoskins A., Yousefi S. Eosinofil and neutrophil extracellular traps in human allergic asthmatic airways // J Allergy Clin Immunol. 2011. Vol. 127, N 5. P. 1260–1266. doi: 10.1016/j.jaci.2010.12.1103

[95] Möllerherm H, von Köckritz-Blickwede M, Branitzki-Heinemann K. Antimicrobial activity of mast cells: role and relevance of extracellular DNA traps. Front Immunol. 2016;7:265. doi: 10.3389/fimmu.2016.00265

[96] Mollerherm H., von Kockritz-Blickwede M., Branitzki-Heinemann K. Antimicrobial activity of mast cells: role and relevance of extracellular DNA traps // Front Immunol. 2016. Vol. 7. P. 265. doi: 10.3389/fimmu.2016.00265

[97] Granger V, Faille D, Marani V, et al. Human blood monocytes are able to form extracellular traps. J Leukoc Biol. 2017;102(3):775–781. doi: 10.1189/jlb.3MA0916-411R

[98] Granger V., Faille D., Marani V., et al. Human blood monocytes are able to form extracellular traps // J Leukoc Biol. 2017. Vol. 102, N 3. P. 775–781. doi: 10.1189/jlb.3MA0916-411R

[99] Ingelsson B, Söderberg D, Strid T, et al. Lymphocytes eject interferogenic mitochondrial DNA webs in response to CpG and non-CpG oligodeoxynucleotides of class C. Proc Natl Acad Sci U S A. 2018;115(3): E478–E487. doi: 10.1073/pnas.1711950115

[100] Ingelsson B., Söderberg D., Strid T., et al. Lymphocytes eject interferogenic mitochondrial DNA webs in response to CpG and non-CpG oligodeoxynucleotides of class C // Proc Natl Acad Sci U S A. 2018. Vol. 115, N 3. P. E478– E487. doi: 10.1073/pnas.1711950115

[101] Deev RV, Bilyalov AI, Zhampeisov TM. Modern ideas about cell death. Genes & сells. 2018;XIII(1):6–19.

[102] Деев Р.В., Билялов А.И., Жампеисов Т.М. Современные представления о клеточной гибели // Гены и клетки. 2018. Т. XIII, № 1. С. 6–19.

[103] de Buhr N, von Köckritz-Blickwede M. How neutrophil extracellular traps become visible. J Immunol Res. 2016;2016:4604713. doi: 10.1155/2016/4604713

[104] de Buhr N., von Köckritz-Blickwede M. How neutrophil extracellular traps become visible // J Immunol Res. 2016. Vol. 2016. P. 4604713. doi: 10.1155/2016/4604713

[105] Zharkova O, Tay SH, Lee HY, et al. A flow cytometry-based assay for high-throughput detection and quantification of neutrophil extracellular traps in mixed cell populations. Cytometry. 2019;95(3):268–278. doi: 10.1002/cyto.a.23672

[106] Zharkova O., Tay S.H., Lee H.Y., et al. A flow cytometry-based assay for high-throughput detection and quantification of neutrophil extracellular traps in mixed cell populations // Cytometry. 2019. Vol. 95, N 3. P. 268–278. doi: 10.1002/cyto.a.23672

[107] Dolgushin II, Savochkina AJu, Shishkova JuS. Metody obnaruzhenija nejtrofil'nyh vnekletochnyh lovushek i ih primenenie v klinicheskoj laboratornoj diagnostike. Russian Journal of Infection and Immunity (Infektsiya i immunitet). 2012;2(1-2):259–260.

[108] Долгушин И.И., Савочкина А.Ю., Шишкова Ю.С. Методы обнаружения нейтрофильных внеклеточных ловушек и их применение в клинической лабораторной диагностике // Инфекция и иммунитет. 2012. Т. 2, № 1-2. С. 259–260.

[109] Yu X, Tan J, Diamond SL. Hemodynamic force triggers rapid NETosis within sterile thrombotic occlusions. J Thromb Haemost. 2018;16(2):316–329. doi: 10.1111/jth.13907

[110] Yu X., Tan J., Diamond S.L. Hemodynamic force triggers rapid NETosis within sterile thrombotic occlusions // J Thromb Haemost. 2018. Vol. 16, N 2. P. 316–329. doi: 10.1111/jth.13907

[111] Gusakova N, Yarets Yu, Hamaliaka A. NET: the hunt goes on. Science and Innovation. 2017;(4):68–72.

[112] Гусакова Н., Ярец Ю., Гомоляко А. NET: охота продолжается // Наука и инновации. 2017. № 4. С. 68–72.

[113] Shiogama K, Onouchi T, Mizutani Y, et al. Visualization of neutrophil extracellular traps and fibrin meshwork in human fibrinopurulent inflammatory lesions: light microscopic study. Acta Histochem Cytochem. 2016;49(4):109–116. doi: 10.1267/ahc.16015

[114] Shiogama K., Onouchi T., Mizutani Y., et al. Visualization of neutrophil extracellular traps and fibrin meshwork in human fibrinopurulent inflammatory lesions: light microscopic study // Acta Histochem Cytochem. 2016. Vol. 49, N 4. P. 109–116. doi: 10.1267/ahc.16015

[115] Thanabalasuriar A, Scott BNV, Peiseler M, et al. Neutrophil extracellular traps confine Pseudomonas aeruginosa ocular biofilms and restrict brain invasion. Cell Host Microbe. 2019;25(4):526–536. doi: 10.1016/j.chom.2019.02.007

[116] Thanabalasuriar A., Scott B.N.V., Peiseler M., et al. Neutrophil extracellular traps confine Pseudomonas aeruginosa ocular biofilms and restrict brain invasion // Cell Host Microbe. 2019. Vol. 25, N 4. P. 526–536. doi: 10.1016/j.chom.2019.02.007

[117] Seki M. The role of neutrophil extracellular traps in infectious diseases. J Infect Dis. 2017;5:321.

[118] Seki M. The role of neutrophil extracellular traps in infectious diseases // J Infect Dis Ther. 2017. Vol. 5. P. 321.

[119] Twaddell SH, Baines KJ, Grainge C, Gibson PG. The emerging role of neutrophil extracellular traps in respiratory disease. Chest. 2019;156(4):774–782. doi: 10.1016/j.chest.2019.06.012

[120] Twaddell S.H., Baines K.J., Grainge C., Gibson P.G. The emerging role of neutrophil extracellular traps in respiratory disease // Chest. 2019. Vol. 156, N 4. P. 774–782. doi: 10.1016/j.chest.2019.06.012

[121] Sultan AR, Hoppenbrouwers T, Lemmens-den Toom NA, et al. During the early stages of Staphylococcus aureus biofilm formation, induced neutrophil extracellular traps (NETs) are degraded by autologous thermonuclease. Infect Immun. 2019;87(12):e00605–e00619. doi: 10.1128/IAI.00605-19

[122] Sultan A.R., Hoppenbrouwers T., Lemmens-den Toom N.A., et al. During the early stages of Staphylococcus aureus biofilm formation, induced neutrophil extracellular traps (NETs) are degraded by autologous thermonuclease // Infect Immun. 2019. Vol. 87, N 12. P. e00605–e00619. doi: 10.1128/IAI.00605-19

[123] Allen ER, Whitefoot-Keliin KM, Palmatier EM, et al. Extracellular vesicles from A23187-treated neutrophils cause cGASSTING-dependent IL-6 production by macrophages. Front Immunol. 2022;13:949451. doi: 10.3389/fimmu.2022.949451

[124] Allen E.R., Whitefoot-Keliin K.M., Palmatier E.M., et al. Extracellular vesicles from A23187-treated neutrophils cause cGASSTING-dependent IL-6 production by macrophages // Front Immunol. 2022. Vol. 13. P. 949451. doi: 10.3389/fimmu.2022.949451

[125] Jorch SK, Kubes P. An emerging role for neutrophil extracellular traps in noninfectious disease. Nat Med. 2017;23(3):279–287. doi: 10.1038/nm.4294. PMID: 28267716

[126] Jorch S.K., Kubes P. An emerging role for neutrophil extracellular traps in noninfectious disease // Nat Med. 2017. Vol. 23, N 3. P. 279–287. doi: 10.1038/nm.4294. PMID: 28267716

[127] Laridan E, Denorme F, Desender L, et al. Neutrophil extracellular traps in ischemic stroke thrombi. Ann Neurol. 2017;82(2):223–232. doi: 10.1002/ana.24993

[128] Laridan E., Denorme F., Desender L., et al. Neutrophil extracellular traps in ischemic stroke thrombi // Ann Neurol. 2017. Vol. 82, N 2. P. 223–232. doi: 10.1002/ana.24993

[129] Rayes RF, Mouhanna JG, Nicolau I, et al. Primary tumors induce neutrophil extracellular traps with targetable metastasis promoting effects. JCI Insight. 2019;5(16):25. doi: 10.1172/jci.insight.128008

[130] Rayes R.F., Mouhanna J.G., Nicolau I., et al. Primary tumors induce neutrophil extracellular traps with targetable metastasis promoting effects // JCI Insight. 2019. Vol. 5, N 16. P. e128008. doi: 10.1172/jci.insight.128008

[131] Lv D, Xu Y, Cheng H, et al. A novel cell-based assay for dynamically detecting neutrophil extracellular traps-induced lung epithelial injuries. Exp Cell Res. 2020;394(2):112101. doi: 10.1016/j.yexcr.2020.112101

[132] Lv D., Xu Y., Cheng H., et al. A novel cell-based assay for dynamically detecting neutrophil extracellular traps-induced lung epithelial injuries // Exp Cell Res. 2020. Vol. 394, N 2. P. 112101. doi: 10.1016/j.yexcr.2020.112101

[133] Lood C, Blanco LP, Purmalek MM, et al. Neutrophil extracellular trap senrichedin oxidized mitochondrial DNA are inter ferogenicand contribute to lupus-like disease. Nat Med. 2016;22(2):146–153. doi: 10.1038/nm.4027

[134] Lood C., Blanco L., Purmalek M.M., et al. Neutrophil extracellular trap senrichedin oxidized mitochondrial DNA are inter ferogenicand contribute to lupus-like disease // Nat Med. 2016. Vol. 22, N 2. P. 146–153. doi: 10.1038/nm.4027

[135] Martinod K, Wagner DD. Thrombosis: tangled up in NETs. Blood. 2014;123(18):2768–2776. doi: 10.1182/blood-2013-10-463646

[136] Martinod K., Wagner D.D. Thrombosis: tangled up in NETs // Blood. 2014. Vol. 123, N 18. P. 2768–2776. doi: 10.1182/blood-2013-10-463646

[137] Vallés J, Lago A, Santos MT, et al. Neutrophil extracellular traps are increased in patients with acute ischemic stroke: prognostic significance. Thromb Haemost. 2017;117(10):1919–1929. doi: 10.1160/TH17-02-0130

[138] Valles J., Lago A., Santos M.T., et al. Neutrophil extracellular traps are increased in patients with acute ischemic stroke: prognostic significance // Thromb Haemost. 2017. Vol. 117, N 10. P. 1919–1929. doi: 10.1160/TH17-02-0130

[139] Ducroux C, Di Meglio L, Loyau S, еt al. Thrombus neutrophil extracellular traps content impair tPA-induced thrombolysis in acute ischemic stroke. Stroke. 2018;49(3):754–757. doi: 10.1161/STROKEAHA.117.019896

[140] Ducroux C., Di Meglio L., Loyau S., еt al. Thrombus neutrophil extracellular traps content impair tPA-induced thrombolysis in acute ischemic stroke // Stroke. 2018. Vol. 49, N 3. P. 754–757. doi: 10.1161/STROKEAHA.117.019896

[141] Klopf J, Brostjan C, Eilenberg W, Neumayer C. Neutrophil extracellular traps and their implications in cardiovascular and inflammatory disease. Int J Mol Sci. 2021;22(2):559. doi: 10.3390/ijms22020559

[142] Klopf J., Brostjan C., Eilenberg W., et al. Neutrophil extracellular traps and their implications in cardiovascular and inflammatory disease // Int J Mol Sci. 2021. Vol. 22, N 2. P. 559. doi: 10.3390/ijms22020559

[143] Mun Y, Hwang JS, Shin YJ. Role of neutrophils on the ocular surface. Int J Mol Sci. 2021;22(19):10386. doi: 10.3390/ijms221910386

[144] Mun Y., Hwang J.S., Shin Y.J. Role of neutrophils on the ocular surface // Int J Mol Sci. 2021. Vol. 22, N 19. P. 10386. doi: 10.3390/ijms221910386

[145] Yang H, Biermann MH, Brauner JM, et al. New insights into neutrophil extracellular traps: mechanisms of formation and role in inflammation. Front Immunol. 2016;7:302. doi: 10.3389/fimmu.2016.00302

[146] Yang H., Biermann M.H., Brauner J.M., et al. New insights into neutrophil extracellular traps: mechanisms of formation and role in inflammation // Front Immunol. 2016. Vol. 7. P. 302. doi: 10.3389/fimmu.2016.00302

[147] Cedervall J, Zhang Y, Olsson AK. Tumor-induced NETosis as a risk factor for metastasis and organ failure. Cancer Res. 2016;76(15):4311–4315. doi: 10.1158/0008-5472.CAN-15-3051

[148] Cedervall J., Zhang Y., Olsson A.K. Tumor-induced NETosis as a risk factor for metastasis and organ failure // Cancer Res. 2016. Vol. 76, N 15. P. 4311–4315. doi: 10.1158/0008-5472.CAN-15-3051

[149] Thierry AR, Roch B. SARS-CoV2 may evade innate immune response, causing uncontrolled neutrophil extracellular traps formation and multi-organ failure. Clin Sci (Lond). 2020;134(12):1295–1300. doi: 10.1042/CS20200531

[150] Thierry A.R., Roch B. SARS-CoV2 may evade innate immune response, causing uncontrolled neutrophil extracellular traps formation and multi-organ failure // Clin Sci (Lond). 2020. Vol. 134, N 12. P. 1295–1300. doi: 10.1042/CS20200531

[151] Sivanandham R, Brocca-Cofano E, Krampe N, et al. Neutrophil extracellular trap production contributes to pathogenesis in SIV-infected nonhuman primates. J Clin Invest. 2018;128(11):5178–5183. doi: 10.1172/JCI99420

[152] Sivanandham R., Brocca-Cofano E., Krampe N., et al. Neutrophil extracellular trap production contributes to pathogenesis in SIV-infected nonhuman primates // J Clin Invest. 2018. Vol. 128, N 11. P. 5178–5183. doi: 10.1172/JCI99420

[153] Wong SL, Demers M, Martinod M, et al. Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nat Med. 2015;2(7):815–819. doi: 10.1038/nm.3887

[154] Wong S.L., Demers M., Martinod K., et al. Diabetes primes neutrophils to undergo NETosis, which impairs wound healing // Nat Med. 2015. Vol. 21, N 7. P. 815–819. doi: 10.1038/nm.3887

[155] Cools-Lartigue J, Spicer J, McDonald B, et al. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J Clin Invest. 2013;123(8):3446–3458. doi: 10.1172/JCI67484

[156] Cools-Lartigue J., Spicer J., McDonald B., et al. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis // J Clin Invest. 2013. Vol. 123, N 8. P. 3446–3458. doi: 10.1172/JCI67484

[157] Kessenbrock K, Krumbholz M, Schönermarck U, et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med. 2009;15(6):623–625. doi: 10.1038/nm.1959

[158] Kessenbrock K., Krumbholz M., Schönermarck U., et al. Netting neutrophils in autoimmune small-vessel vasculitis // Nat Med. 2009. Vol. 15, N 6. P. 623–625. doi: 10.1038/nm.1959

[159] Carmona-Rivera C, Kapla MJ. Low-density granulocytes: a distinct class of neutrophils in systemic autoimmunity. Semin Immunopathol. 2013;35(4):455–463. doi: 10.1007/s00281-013-0375-7

[160] Carmona-Rivera C., Kapla M.J. Low-density granulocytes: a distinct class of neutrophils in systemic autoimmunity // Semin Immunopathol. 2013. Vol. 35, N 4. P. 455–463. doi: 10.1007/s00281-013-0375-7

[161] van Dam LS, Rabelink TJ, van Kooten C, Teng YKO. Clinical implications of excessive neutrophil extracellular trap formation in renal autoimmune diseases. Kidney Int Rep. 2019;4(2):196–211. doi: 10.1016/j.ekir.2018.11.005

[162] van Dam L.S., Rabelink T.J., van Kooten C., Teng Y.K.O. Clinical implications of excessive neutrophil extracellular trap formation in renal autoimmune diseases // Kidney Int Rep. 2019. Vol. 4, N 2. P. 196–211. doi: 10.1016/j.ekir.2018.11.005

[163] Jariwala MP, Laxer RM. NETosis in rheumatic diseases. Curr Rheumatol Rep. 2021;23(2):9. doi: 10.1007/s11926-020-00977-6

[164] Jariwala M.P., Laxer R.M. NETosis in rheumatic diseases // Curr Rheumatol Rep. 2021. Vol. 23, N 2. P. 9. doi: 10.1007/s11926-020-00977-6

[165] Shida H, Hashimoto N, Kusunoki Y, et al. Anti-neutrophil extracellular trap antibody in a patient with relapse of anti-neutrophil cytoplasmic antibody-associated vasculitis: a case report. BMC Nephrol. 2018; 19(1):145. doi: 10.1186/s12882-018-0953-y

[166] Shida H., Hashimoto N., Kusunoki Y., et al. Anti-neutrophil extracellular trap antibody in a patient with relapse of anti-neutrophil cytoplasmic antibody-associated vasculitis: a case report // BMC Nephreport. 2018. Vol. 19, N 1. P. 145. doi: 10.1186/s12882-018-0953-y

[167] Gupta S, Kaplan MJ. The role of neutrophils and NETosis in autoimmune and renal diseases. Nat Rev Nephrol. 2016;12(7):402–413. doi: 10.1038/nrneph.2016.71

[168] Gupta S., Kaplan M.J. The role of neutrophils and NETosis in autoimmune and renal diseases // Nat Rev Nephrol. 2016. Vol. 12, N 7. P. 402–413. doi: 10.1038/nrneph.2016.71

[169] Khandpur R, Carmona-Rivera C, Vivekanandan-Giri A, et al. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci Transl Med. 2013;5(178):178ra40. doi: 10.1126/scitranslmed.3005580

[170] Khandpur R., Carmona-Rivera C., Vivekanandan-Giri A., et al. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis // Sci Transl Med. 2013. Vol. 5, N 178. P. 178ra40. doi: 10.1126/scitranslmed.3005580

[171] Papayannopoulos V. Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol. 2018;18(2):134–147. doi: 10.1038/nri.2017.105

[172] Papayannopoulos V. Neutrophil extracellular traps in immunity and disease // Nat Rev Immunol. 2018. Vol. 18, N 2. P. 134–147. doi: 10.1038/nri.2017.105

[173] Sabbatini M, Magnelli V, Renò F. NETosis in wound healing: when enough is enough. Cells. 2021;10(3):494. doi: 10.3390/cells10030494

[174] Sabbatini M., Magnelli V., Renò F. NETosis in wound healing: when enough is enough // Cells. 2021. Vol. 10, N 3. P. 494. doi: 10.3390/cells10030494

[175] Barnes BJ, Adrover JM, Baxter-Stoltzfus A, et al. Targeting potential drivers of COVID-19: Neutrophil extracellular traps. J Exp Med. 2020;217(6):e20200652. doi: 10.1084/jem.20200652

[176] Barnes B.J., Adrover J.M., Baxter-Stoltzfus A., et al. Targeting potential drivers of COVID-19: neutrophil extracellular traps // J Exp Med. 2020. Vol. 217, N 6. P. e20200652. doi: 10.1084/jem.20200652

[177] Zuo Y, Yalavarthi S, Shi H, et al. Neutrophil extracellular traps in COVID-19. JCI Insight. 2020;5(11):e138999. doi: 10.1172/jci.insight.138999

[178] Zuo Y., Yalavarthi S., Shi H., et al. Neutrophil extracellular traps in COVID-19 // JCI Insight. 2020. Vol. 5, N 11. P. e138999. doi: 10.1172/jci.insight.138999

RIGHTS & PERMISSIONS

Eco-Vector