Условия реализации феномена запрограммированной гибели нейтрофилов с появлением внеклеточных ДНК-ловушек при тромбообразовании

Обложка

Цитировать

Полный текст

Аннотация

   Формирование внеклеточных ДНК-ловушек нейтрофилов (NET-оз) – механизм запрограммированной клеточной смерти лейкоцитов, имеющий исходно антибактериальную и противогрибковую функции. Способность нейтрофилов активироваться при контакте с активированными тромбоцитами и, в свою очередь, активировать контактный путь свертывания с помощью ДНК-ловушек играет центральную роль в венозных тромбозах и диссеминированном внутрисосудистом свертывании крови при COVID-19. При этом внутриклеточная сигнализация, управляющая NET-озом, является крайне плохо понятной даже для простейших случаев, когда этот процесс вызывается липополисахаридами бактериальной стенки. В настоящем обзоре мы рассматриваем случай NET-оза при тромбозе, для которого вопросов еще больше. Внимание сосредоточено на условиях наблюдения NET-оза и особенностях его протекания при разных сценариях.

Об авторах

А. Н. Свешникова

ФГБУ «Национальный медицинский исследовательский центр детской гематологии, онкологии и иммунологии им. Дмитрия Рогачева» Минздрава России; ФГБОУ ВО «Московский государственный университет им. М.В. Ломоносова»; ФГБУН «Центр теоретических проблем физико-химической фармакологии» РАН

Автор, ответственный за переписку.
Email: a.sveshnikova@physics.msu.ru
ORCID iD: 0000-0003-4720-7319

Анастасия Никитична Свешникова, д-р физ.-мат. наук, заведующая лабораторией

лаборатория клеточной биологии и трансляционной медицины

117997; ул. Саморы Машела, 1; Москва

Россия

Е. А. Адаманская

ФГБУ «Национальный медицинский исследовательский центр детской гематологии, онкологии и иммунологии им. Дмитрия Рогачева» Минздрава России; ФГБУН «Центр теоретических проблем физико-химической фармакологии» РАН

ORCID iD: 0009-0000-4828-4063

Москва

Россия

М. А. Пантелеев

ФГБУ «Национальный медицинский исследовательский центр детской гематологии, онкологии и иммунологии им. Дмитрия Рогачева» Минздрава России; ФГБОУ ВО «Московский государственный университет им. М.В. Ломоносова»; ФГБУН «Центр теоретических проблем физико-химической фармакологии» РАН

ORCID iD: 0000-0002-8128-7757

Москва

Россия

Список литературы

  1. Robb C.T., Dyrynda E.A., Gray R.D., Rossi A.G., Smith V.J. Invertebrate Extracellular Phagocyte Traps Show That Chromatin Is an Ancient Defence Weapon. Nat Commun 2014; 5: 4627. doi: 10.1038/ncomms5627
  2. Daniel C., Leppkes M., Muñoz L.E., Schley G., Schett G., Herrmann M. Extracellular DNA Traps in Inflammation, Injury and Healing. Nat Rev Nephrol 2019; 15: 559–75. doi: 10.1038/s41581-019-0163-2
  3. Palacios-Acedo A.L., Mège D., Crescence L., Dignat-George F., Dubois C., Panicot-Dubois L. Platelets, Thrombo-Inflammation, and Cancer: Collaborating With the Enemy. Front Immunol 2019; 10: 1805. doi: 10.3389/fimmu.2019.01805
  4. Sveshnikova A.N., Ataullakhanov F.I., Panteleev M.A. Compartmentalized Calcium Signaling Triggers Subpopulation Formation upon Platelet Activation through PAR1. Mol BioSyst 2015; 11: 1052–60. doi: 10.1039/c4mb00667d
  5. Caudrillier A., Kessenbrock K., Gilliss B.M., Nguyen J.X., Marques M.B., Monestier M., et al. Platelets Induce Neutrophil Extracellular Traps in Transfusion-Related Acute Lung Injury. J Clin Invest 2012; 122: 2661–71. doi: 10.1172/JCI61303
  6. Golas A., Parhi P., Dimachkie Z.O., Siedlecki C.A., Vogler E.A. Surface-Energy Dependent Contact Activation of Blood Factor XII. Biomaterials 2010; 31: 1068–79. doi: 10.1016/j.biomaterials.2009.10.039
  7. Fuchs T.A., Brill A., Wagner D.D. Neutrophil Extracellular Trap (NET) Impact on Deep Vein Thrombosis. Arterioscler Thromb Vasc Biol 2012; 32: 1777–83. doi: 10.1161/ATVBAHA.111.242859
  8. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., et al. Neutrophil Extracellular Traps Kill Bacteria. Science 2004; 303: 1532–5. doi: 10.1126/science.1092385
  9. Rosales C. Neutrophil: A Cell with Many Roles in Inflammation or Several Cell Types? Front Physiol 2018; 9: 113.
  10. Козлов С.О., Кудрявцев И.В., Грудинина Н.А., Костевич В.А., Панасенко О.М., Соколов А.В., Васильев В.Б. Активированные нейтрофилы, продуцирующие HOCL, выявляющиеся при проточной цитометрии и конфокальной микроскопии с помощью целестинового синего В. Acta Biomedica Scientifica 2016; 1 (3(2)): 86–91. doi: 10.12737/article_590823a4895537.04307905.
  11. Bratton D.L., Henson P.M. Neutrophil Clearance: When the Party Is over, Clean-up Begins. Trends Immunol 2011; 32: 350–7. doi: 10.1016/j.it.2011.04.009
  12. Hoffbrand V., Vyas P., Campo E., Haferlach T., Gomez K. Color Atlas of Clinical Hematology: Molecular and Cellular Basis of Disease. John Wiley & Sons; 2019. ISBN 978-1-119-05701-7.
  13. Borregaard N., Sørensen O.E., Theilgaard-Mönch K. Neutrophil Granules: A Library of Innate Immunity Proteins. Trends Immunol 2007; 28: 340–5. doi: 10.1016/j.it.2007.06.002
  14. Погорелов В., Козинец Г., Дягилева О., Луговская С., Проценко Д., Сарычева Т. Гематологический атлас. Настольное руководство врача-лаборанта. Litres; 2022. ISBN 978-5-04-256439-0.
  15. Murphy K.M., Weaver C. Janeway’s Immunobiology; Garland Science/Taylor & Francis Group, LLC; 2017. ISBN 978-0-8153-4505-3.
  16. Адаманская Е.А., Юшкова E.B., Федорова Д.В., Соколов А.В., Подоплелова Н.А., Свешникова А.Н. Методика наблюдения ДНК-ловушек нейтрофилов в образцах крови педиатрических пациентов. Сборник тезисов XXIV съезда физиологического общества им. И.П. Павлова. СПб.: ООО «Издательство ВВМ»; 2023.
  17. Nathan C. Neutrophils and Immunity: Challenges and Opportunities. Nat Rev Immunol 2006; 6: 173–82. doi: 10.1038/nri1785
  18. Segal A.W. How Neutrophils Kill Microbes. Ann Rev Immunol 2005; 23: 197–223. doi: 10.1146/annurev.immunol.23.021704.115653
  19. Mayadas T.N., Cullere X., Lowell C.A. The Multifaceted Functions of Neutrophils. Annu Rev Pathol 2014; 9: 181–218. doi: 10.1146/annurev-pathol-020712-164023
  20. Witko-Sarsat V., Rieu P., Descamps-Latscha B., Lesavre P., Halbwachs-Mecarelli L. Neutrophils: Molecules, Functions and Pathophysiological Aspects. Lab Invest 2000; 80: 617–53. doi: 10.1038/labinvest.3780067
  21. Smith C.K., Kaplan M.J. The Role of Neutrophils in the Pathogenesis of Systemic Lupus Erythematosus. Curr Opin Rheumatol 2015; 27: 448. doi: 10.1097/BOR.0000000000000197
  22. Yu Y., Su K. Neutrophil Extracellular Traps and Systemic Lupus Erythematosus. J Clin Cell Immunol 2013; 4: 139. doi: 10.4172/2155-9899.1000139
  23. Summers C., Rankin S.M., Condliffe A.M., Singh N., Peters A.M., Chilvers E.R. Neutrophil Kinetics in Health and Disease. Trends Immunol 2010; 31: 318–24. doi: 10.1016/j.it.2010.05.006
  24. Petri B., Sanz M.-J. Neutrophil Chemotaxis. Cell Tissue Res 2018; 371: 425–36. doi: 10.1007/s00441-017-2776-8
  25. Murphy P.M. Neutrophil Receptors for Interleukin-8 and Related CXC Chemokines. Semin Hematol 1997; 34: 311–8.
  26. Schoenwaelder S.M., Ruggeri Z.M., Westein E., Kaplan Z.S., Jackson S.P., Ashworth K.J., et al. The CXCR1/2 Ligand NAP-2 Promotes Directed Intravascular Leukocyte Migration through Platelet Thrombi. Blood 2013; 121: 4555–66. doi: 10.1182/blood-2012-09-459636
  27. Damascena H.L., Silveira W.A.A., Castro M.S., Fontes W. Neutrophil Activated by the Famous and Potent PMA (Phorbol Myristate Acetate). Cells 2022; 11: 2889. doi: 10.3390/cells11182889
  28. Karpurapu M., Lee, Y.G., Qian Z., Wen J., Ballinger M.N., Rusu L., et al. Inhibition of Nuclear Factor of Activated T Cells (NFAT) C3 Activation Attenuates Acute Lung Injury and Pulmonary Edema in Murine Models of Sepsis. Oncotarget 2018; 9: 10606–20. doi: 10.18632/oncotarget.24320
  29. Zanoni I., Ostuni R., Capuano G., Collini M., Caccia M., Ronchi A.E., et al. CD14 Regulates the Dendritic Cell Life Cycle after LPS Exposure through NFAT Activation. Nature 2009; 460 (7252): 264–8. doi: 10.1038/nature08118
  30. Businaro R., Scaccia E., Bordin A., Pagano F., Corsi M., Siciliano C., et al. Platelet Lysate-Derived Neuropeptide y Influences Migration and Angiogenesis of Human Adipose Tissue-Derived Stromal Cells. Sci Rep 2018; 8: 14365. doi: 10.1038/s41598-018-32623-8
  31. Cassatella M.A. The Neutrophil: An Emerging Regulator of Inflammatory and Immune Response. Karger Medical and Scientific Publishers; 2003. ISBN 978-3-8055-7552-2.
  32. Lindbom L., Werr J. Integrin-Dependent Neutrophil Migration in Extravascular Tissue. Semin Immunol 2002; 14: 115–21. doi: 10.1006/smim.2001.0348
  33. Pluskota E., Soloviev D.A., Szpak D., Weber C., Plow E.F. Neutrophil Apoptosis: Selective Regulation by Different Ligands of Integrin aMb2. J Immunol 2008; 181: 3609–19.
  34. Ugarova T.P., Yakubenko V.P. Recognition of Fibrinogen by Leukocyte Integrins. Ann N Y Acad Sci 2001; 936: 368–85. doi: 10.1111/j.1749-6632.2001.tb03523.x
  35. Zarbock A., Ley K. Platelet-Neutrophil-Interactions: Linking Hemostasis and Inflammation. Blood Rev 2007; 21 (2): 99–111. doi: 10.1016/j.blre.2006.06.001
  36. Yago T., Shao B., Miner J.J., Yao L., Klopocki A.G., Maeda K., et al. E-Selectin Engages PSGL-1 and CD44 through a Common Signaling Pathway to Induce Integrin aLb2-Mediated Slow Leukocyte Rolling. Blood 2010; 116: 485–94. doi: 10.1182/blood-2009-12-259556
  37. Zhou F., Zhang F., Zarnitsyna V.I., Doudy L., Yuan Z., Li K., et al. The Kinetics of E-Selectin- and P-Selectin-Induced Intermediate Activation of Integrin aLb2 on Neutrophils. J Cell Sci 2021; 134: jcs258046. doi: 10.1242/jcs.258046
  38. Jenne C.N., Kubes P. Platelets in Inflammation and Infection. Platelets 2015; 26: 286–92. doi: 10.3109/09537104.2015.1010441
  39. Koupenova M., Corkrey H.A., Vitseva O., Manni G., Pang C.J., Clancy L., et al. The Role of Platelets in Mediating a Response to Human Influenza Infection. Nat Commun 2019; 10: 1780. doi: 10.1038/s41467-019-09607-x
  40. Sveshnikova A., Stepanyan M., Panteleev M. Platelet Functional Responses and Signalling: The Molecular Relationship. Part 1: Responses. Systems Biol Physiol Rep 2021; 1: 20. doi: 10.52455/sbpr.01.202101014
  41. Nicolai L., Schiefelbein K., Lipsky S., Leunig A., Hoffknecht M., Pekayvaz K., et al. Vascular Surveillance by Haptotactic Blood Platelets in Inflammation and Infection. Nat Commun 2020; 11: 5778. doi: 10.1038/s41467-020-19515-0
  42. Gros A., Syvannarath V., Lamrani L., Ollivier V., Loyau S., Goerge T., et al. Single Platelets Seal Neutrophil-Induced Vascular Breaches via GPVI during Immune-Complex-Mediated Inflammation in Mice. Blood 2015; 126: 1017–26. doi: 10.1182/blood-2014-12-617159
  43. Knorr D.A., Bachanova V., Verneris M.R., Miller J.S. Clinical Utility of Natural Killer Cells in Cancer Therapy and Transplantation. Semin Immunol 2014; 26: 161–72. doi: 10.1016/j.smim.2014.02.002
  44. Shannon O. The Role of Platelets in Sepsis. Res Pract Thromb Haemost 2021; 5: 27–37. doi: 10.1002/rth2.12465
  45. Schattner M., Jenne C.N., Negrotto S., Ho-Tin-Noe B. Editorial: Platelets and Immune Responses During Thromboinflammation. Front Immunol 2020; 11: 1079. doi: 10.3389/fimmu.2020.01079
  46. Bonaventura A., Vecchié A., Dagna L., Martinod K., Dixon D.L., van Tassell B.W., et al. Endothelial Dysfunction and Immunothrombosis as Key Pathogenic Mechanisms in COVID-19. Nat Rev Immunol 2021; 21: 319–29. doi: 10.1038/s41577-021-00536-9
  47. Zhu Y., Chen X., Liu X. NETosis and Neutrophil Extracellular Traps in COVID-19: Immunothrombosis and Beyond. Front Immunol 2022; 13: 838011. doi: 10.3389/fimmu.2022.838011.
  48. de Bont C.M., Koopman W.J.H., Boelens W.C., Pruijn G.J.M. Stimulus-Dependent Chromatin Dynamics, Citrullination, Calcium Signalling and ROS Production during NET Formation. Biochim Biophys Acta Mol Cell Res 2018; 1865: 1621–9. doi: 10.1016/j.bbamcr.2018.08.014
  49. Khan M.A., Farahvash A., Douda D.N., Licht, J.-C., Grasemann H., Sweezey N., Palaniyar N. JNK Activation Turns on LPS- and Gram-Negative Bacteria-Induced NADPH Oxidase-Dependent Suicidal NETosis. Sci Rep 2017; 7: 3409. doi: 10.1038/s41598-017-03257-z
  50. Agarwal S., Loder S., Cholok D., Li J., Bian G., Yalavarthi S., et al. Disruption of Neutrophil Extracellular Traps (NETs) Links Mechanical Strain to Post-Traumatic Inflammation. Front Immunol 2019; 10: 2148. doi: 10.3389/fimmu.2019.02148
  51. Pai D., Gruber M., Pfaehler S.-M., Bredthauer A., Lehle K., Trabold B. Polymorphonuclear Cell Chemotaxis and Suicidal NETosis: Simultaneous Observation Using fMLP, PMA, H7, and Live Cell Imaging. J Immunol Res 2020; 2020: e1415947. doi: 10.1155/2020/1415947
  52. Arroyo R., Khan M.A., Echaide M., Pérez-Gil J., Palaniyar N. SP-D Attenuates LPS-Induced Formation of Human Neutrophil Extracellular Traps (NETs), Protecting Pulmonary Surfactant Inactivation by NETs. Commun Biol 2019; 2: 1–13. doi: 10.1038/s42003-019-0662-5
  53. Papayannopoulos V. Neutrophil Extracellular Traps in Immunity and Disease. Nat Rev Immunol 2018; 18: 134–47. doi: 10.1038/nri.2017.105
  54. 孝泰野村 NETosis. 日本小児アレル ギー学会誌 2019; 33: 348–9. doi: 10.3388/jspaci.33.348
  55. Remijsen Q., Kuijpers T.W., Wirawan E., Lippens S., Vandenabeele P., Vanden Berghe T. Dying for a Cause: NETosis, Mechanisms behind an Antimicrobial Cell Death Modality. Cell Death Differ 2011; 18: 581–8. doi: 10.1038/cdd.2011.1
  56. Thiam H.R., Wong S.L., Wagner D.D., Waterman C.M. Cellular Mechanisms of NETosis. Annu Rev Cell Dev Biol 2020; 36: 191–218. doi: 10.1146/annurev-cellbio-020520-111016
  57. Stoimenou M., Tzoros G., Skendros P., Chrysanthopoulou A. Methods for the Assessment of NET Formation: From Neutrophil Biology to Translational Research. Int J Mol Sci 2022; 23: 15823. doi: 10.3390/ijms232415823
  58. Andrews R.K., Arthur J.F., Gardiner E.E. Neutrophil Extracellular Traps (NETs) and the Role of Platelets in Infection. Thromb Haemost 2014; 112: 659–65. doi: 10.1160/TH14-05-0455
  59. Balázs A., Mall M.A. Mucus Obstruction and Inflammation in Early Cystic Fibrosis Lung Disease: Emerging Role of the IL-1 Signaling Pathway. Pediatr Pulmonol 2019; 54: S5–12. doi: 10.1002/ppul.24462
  60. Martinod K., Witsch T., Farley K., Gallant M., Remold-O’Donnell E., Wagner D.D. Neutrophil Elastase-Deficient Mice Form Neutrophil Extracellular Traps in an Experimental Model of Deep Vein Thrombosis. J Thromb Haemost 2016; 14 (3): 551–8. doi: 10.1111/jth.13239
  61. Martyanov A.A., Boldova A.E., Stepanyan M.G., An O.I., Gur’ev A.S., Kassina D.V., et al. Longitudinal Multiparametric Characterization of Platelet Dysfunction in COVID-19: Effects of Disease Severity, Anticoagulation Therapy and Inflammatory Status. Thromb Res 2022; 211: 27–37. doi: 10.1016/j.thromres.2022.01.013
  62. Ramacciotti E., Myers D.D., Wrobleski S.K., Deatrick K.B., Londy F.J., Rectenwald J.E., et al. P-Selectin/PSGL-1 Inhibitors versus Enoxaparin in the Resolution of Venous Thrombosis: A Meta-Analysis. Thromb Res 2010; 125: e138–42. doi: 10.1016/j.thromres.2009.10.022
  63. Lee K.H., Kronbichler A., Park D.D.-Y., Park Y., Moon H., Kim H., et al. Neutrophil Extracellular Traps (NETs) in Autoimmune Diseases: A Comprehensive Review. Autoimmun Rev 2017; 16: 1160–73. doi: 10.1016/j.autrev.2017.09.012
  64. Mesa M.A., Vasquez G. NETosis. Autoimmune Diseases 2013; 2013: e651497. doi: 10.1155/2013/651497
  65. Philip F., Kadamur G., Silos R.G., Woodson J., Ross E.M. Synergistic Activation of Phospholipase C-B3 by Gaq and Gbg Describes a Simple Two-State Coincidence Detector. Curr Biol 2010; 20: 1327–35. doi: 10.1016/J.CUB.2010.06.013
  66. Vorobjeva N., Galkin I., Pletjushkina O., Golyshev S., Zinovkin R., Prikhodko A. et al. Mitochondrial Permeability Transition Pore Is Involved in Oxidative Burst and NETosis of Human Neutrophils. Biochim Biophys Acta Mol Basis Dis 2020; 1866: 165664. doi: 10.1016/j.bbadis.2020.165664
  67. Yang C., Wang Z., Li L., Zhang Z., Jin X., Wu P., et al. Aged Neutrophils Form Mitochondria-Dependent Vital NETs to Promote Breast Cancer Lung Metastasis. J Immunother Cancer 2021; 9: e002875. doi: 10.1136/jitc-2021-002875
  68. Luo H.R., Loison F. Constitutive Neutrophil Apoptosis: Mechanisms and Regulation. Am J Hematol 2008; 83: 288–95. doi: 10.1002/ajh.21078
  69. Fuchs T.A., Abed U., Goosmann C., Hurwitz R., Schulze I., Wahn V., et al. Novel Cell Death Program Leads to Neutrophil Extracellular Traps. J Cell Biol 2007; 176: 231–41. doi: 10.1083/jcb.200606027
  70. Bianchi M., Hakkim A., Brinkmann V., Siler U., Seger R.A., Zychlinsky A., et al. Restoration of NET Formation by Gene Therapy in CGD Controls Aspergillosis. Blood 2009; 114: 2619–22. doi: 10.1182/blood-2009-05-221606
  71. Saffarzadeh M., Juenemann C., Queisser M.A., Lochnit G., Barreto G., Galuska S.P., et al. Neutrophil Extracellular Traps Directly Induce Epithelial and Endothelial Cell Death: A Predominant Role of Histones. PLoS One 2012; 7: e32366. doi: 10.1371/journal.pone.0032366
  72. Thiam H.R., Wong S.L., Qiu R., Kittisopikul M., Vahabikashi A., Goldman A.E., et al. NETosis Proceeds by Cytoskeleton and Endomembrane Disassembly and PAD4-Mediated Chromatin Decondensation and Nuclear Envelope Rupture. Proc Natl Acad Sci U S A 2020; 117: 7326–37. doi: 10.1073/pnas.1909546117
  73. Metzler K.D., Goosmann C., Lubojemska A., Zychlinsky A., Papayannopoulos V. A Myeloperoxidase-Containing Complex Regulates Neutrophil Elastase Release and Actin Dynamics during NETosis. Cell Rep 2014; 8: 883–96. doi: 10.1016/j.celrep.2014.06.044
  74. Chen T., Li Y., Sun R., Hu H., Liu Y., Herrmann M., et al. Receptor-Mediated NETosis on Neutrophils. Front Immunol 2021; 12: 775267.
  75. Vorobjeva N.V., Chernyak B.V. NETosis: Molecular Mechanisms, Role in Physiology and Pathology. Biochemistry (Mosc) 2020; 85: 1178–90. doi: 10.1134/S0006297920100065
  76. 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: 559. doi: 10.3390/ijms22020559
  77. von Köckritz-Blickwede M., Winstel V. Molecular Prerequisites for Neutrophil Extracellular Trap Formation and Evasion Mechanisms of Staphylococcus Aureus. Front Immunol 2022; 13: 836278.
  78. Yipp B.G., Kubes P. NETosis: How Vital Is It? Blood 2013; 122: 2784–94. doi: 10.1182/blood-2013-04-457671
  79. Pilsczek F.H., Salina D., Poon K.K.H., Fahey C., Yipp B.G., Sibley C.D., et al. A Novel Mechanism of Rapid Nuclear Neutrophil Extracellular Trap Formation in Response to Staphylococcus Aureus. J Immunol 2010; 185: 7413–25. doi: 10.4049/jimmunol.1000675
  80. Martinod K., Demers M., Fuchs T.A., Wong S.L., Brill A., Gallant M., et al. Neutrophil Histone Modification by Peptidylarginine Deiminase 4 Is Critical for Deep Vein Thrombosis in Mice. Proc Natl Acad Sci U S A 2013; 110: 8674–9. doi: 10.1073/pnas.1301059110

Дополнительные файлы

Доп. файлы
Действие
1. JATS XML
Скачать

© Свешникова А.Н., Адаманская Е.А., Пантелеев М.А., 2024

Creative Commons License
Эта статья доступна по лицензии Creative Commons Attribution 4.0 International License.