Platelet Activation and Mechanisms of Thromboembolism Formation in Patients with Severe COVID-19. Alternative Mechanisms of Hemostasis System Activity

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Abstract

The review highlights the mechanism of development of hypercoagulation and thrombosis in severe forms of COVID-19. The introduction of the SARS-CoV-2 virus into the host organism is carried out by the interaction of the spike protein S with the angiotensin-converting enzyme ACE-2, which is located in type 2 alveocytes, vascular endothelium, kidneys, liver and other organs. In the event of a serious condition in patients with COVID-19, both nonspecific and adaptive immunity are activated. Stimulation of the complement system with the appearance of C3a, C3b, C5a fragments and the membrane attack complex (MAC) creates conditions for the development of hypercoagulability. The involvement of the renin-angiotensin-aldosterone system in this process and the appearance of angiotensin 2 (Ang-2) further increase the intensity of hypercoagulability. When the SARS-CoV-2 virus enters cells, the protective reaction of the adaptive immune system can turn into a pathological one (a cytokine storm develops), characterized by a high level of pro-inflammatory cytokines IL-1α, IL-6, Il-8, TNF-α, IL-17, etc.) and chemokines (CCL-2, CCL-11, etc.), which ultimately leads to the development of thromboangiopathy or otherwise immunothrombosis in seriously ill patients with COVID-19. Patients with more severe lesions may develop a condition similar to DIC. At the same time, patients with COVID-19 have mild thrombocytopenia, elevated levels of fibrinogen, D-dimer, fibrinogen degradation products (FDP), which indicates intense thrombus formation, as well as short PT and APTT, due to a largely increased level of FVIII. In COVID-19, along with the classical one, an alternative pathway (bypassing thrombin) of regulation of the hemostasis system and thrombus formation appears, mainly associated with the influence of the spike protein S (PS, PROS1) of the SARS-CoV-2 virus and papain-like protease (PROS1). Protein S directly affects the conversion of fibrinogen to fibrin, as well as the activation of individual plasma coagulation factors. The alternative pathway of blood coagulation is also due to the activation of the complement system via the lectin pathway with the inclusion of metalloproteinases MASP-1, 2 and 3. In addition, the S protein activates tPA, which may be accompanied by hyperfibrinolysis. In seriously ill patients with COVID-19, platelets play an important role in the occurrence of thromboembolic complications. During the release reaction, platelets are released from the cytoplasm into the blood α and dense granules containing inflammatory cytokines and chemokines, which enhances the cytokine storm and, consequently, thrombus formation. By acting on the spike protein S, platelets enhance an alternative way of regulating the hemostasis system and thrombus formation.

About the authors

B. I. Kuznik

Chita State Medical Academy

Email: smolyakov@rambler.ru
Russia, Chita

Y. N. Smolyakov

Chita State Medical Academy

Author for correspondence.
Email: smolyakov@rambler.ru
Russia, Chita

N. N. Tsybikov

Chita State Medical Academy

Email: smolyakov@rambler.ru
Russia, Chita

K. G. Shapovalov

Chita State Medical Academy

Email: smolyakov@rambler.ru
Russia, Chita

References

  1. Березовская Г.А., Петрищев Н.Н., Волкова Е.В. и др. Поражение сердечно-сосудистой системы при новой коронавирусной инфекции COVID-19 // Кардиология: новости, мнения, обучение. 2022. Т. 10 (4). С. 37–47. https://doi.org/10.33029/2309-1908-2022-10-4-37-47
  2. Кузник Б.И., Хавинсон В.Х. Влияние тималина на системы иммунитета, гемостаза и уровень цитокинов у пациентов с различными заболеваниями. Перспективы применения при COVID-19 // Врач. 2020. Т. 31 (7). С. 18–26. https://doi.org/10.29296/25877305-2020-07-03
  3. Кузник Б.И., Хавинсон В.Х., Линькова Н.С. COVID-19: влияние на иммунитет, систему гемостаза и возможные пути коррекции // Усп. физиол. наук. 2020. № 4. С. 51–63. https://doi.org/10.31857/S0301179820040037
  4. Кузник Б.И., Шаповалов К.Г., Смоляков Ю.Н. и др. Морфологический состав и показатели свертывающей системы крови у пациентов среднего и пожилого возраста с COVID-19 при лечении тоцилизумабом и тималином // Усп. геронтол. 2022. Т. 35 (3). С. 368–373. https://doi.org/10.34922/AE.2022.35.3.006
  5. Кузник Б.И., Ройтман Е.В., Цыбиков Н.Н. и др. Полипотентные механизмы регуляции системы гемостаза и тромбообразования при COVID-19 // Тромбоз, гемостаз, реология. 2023. № 2. (в печати)
  6. Хавинсон В.Х., Кузник Б.И. Осложнения у больных CОVID-19. Предполагаемые механизмы коррекции // Клин. мед. 2020. Т. 98 (4). С. 256–265.
  7. Ackermann M., Verleden S.E., Kuehnel M. et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in COVID-19 // N. Engl. J. Med. 2020. V. 383 (2). P. 120–128. https://doi.org/10.1056/NEJMoa2015432
  8. Ahmad F., Kannan M., Ansari AW. Role of SARS-CoV-2-induced cytokines and growth factors in coagulopathy and thromboembolism // Cyt. Growth Factor Rev. 2022. V. 63. P. 58–68. https://doi.org/10.1016/j.cytogfr.2021.10.007
  9. Ahmed S., Zimba O., Gasparyan A.Y. Thrombosis in coronavirus disease 2019 (COVID-19) through the prism of Virchow’s triad // Clin. Rheumatol. 2020. V. 39 (9). P. 2529–2543. https://doi.org/10.1007/s10067-020-05275-1
  10. Allaoui A., Khawaja A.A., Badad O. et al. Platelet function in viral immunity and SARS-CoV-2 infection // Semin. Thromb. Hemost. 2021. V. 47 (4). P. 419–426. https://doi.org/10.1055/s-0041-1726033
  11. Al-Samkari H., Leaf R.S.K., Dzik W.H. et al. COVID-19 and coagulation: bleeding and thrombotic manifestations of SARS-CoV-2 infection // Blood. 2020. V. 136 (4). P. 489–500. https://doi.org/10.1182/blood.2020006520
  12. Al-Tamimi A.O., Yusuf A.M., Jayakumar M.N. et al. SARS-CoV-2 infection induces soluble platelet activation markers and PAI-1 in the early moderate stage of COVID-19 // Int. J. Lab. Hematol. 2022. V. 44 (4). P. 712–721. https://doi.org/10.1111/ijlh.13829
  13. Arunachalam P.S., Wimmers F., Mok C.K.P. et al. Systems biological assessment of immunity to mild versus severe COVID-19 infection in humans // Science. 2020. V. 369. P. 1210–1220. https://doi.org/10.1126/science.abc6261
  14. Barale C., Melchionda E., Morotti A., Russo I. Prothrombotic phenotype in COVID-19: focus on platelets // Int. J. Mol. Sci. 2021. V. 22 (24). P. 13638. https://doi.org/10.3390/ijms222413638
  15. Barnes B.J., Adrover J.M., Baxter-Stoltzfus A. et al. Targeting potential drivers of COVID-19: neutrophil extracellular traps // J. Exp. Med. 2020. V. 217 (6). P. e20200652. https://doi.org/10.1084/jem.20200652
  16. Barrett T.J., Cornwell M., Myndzar K. et al. Platelets amplify endotheliopathy in COVID-19 // Sci. Adv. 2021. V. 7 (37). P. eabh2434. https://doi.org/10.1126/sciadv.abh2434
  17. Beura S.K., Panigrahi A.R., Yadav P., Singh S.K. Phytochemicals as potential therapeutics for SARS-CoV-2-induced cardiovascular complications: thrombosis and platelet perspective // Front. Pharmacol. 2021. V. 12. P. 658273. https://doi.org/10.3389/fphar.2021.658273
  18. Bumiller-Bini V., De Freitas Oliveira-Toré C., Carvalho T.M. et al. MASPs at the crossroad between the complement and the coagulation cascades – the case for COVID-19 // Genet. Mol. Biol. 2021. V. 44 (1). P. e20200199. https://doi.org/10.1590/1678-4685-GMB-2020-0199
  19. Bye A.P., Hoepel W., Mitchell J.L. et al. Aberrant glycosylation of anti-SARS-CoV-2 spike IgG is a prothrombotic stimulus for platelets // Blood. 2021. V. 138 (16). P. 1481–1489. https://doi.org/10.1182/blood.2021011871
  20. Canaday D.H. SARS-CoV-2 antibody responses to the ancestral SARS-CoV-2 strain and Omicron BA.1 and BA.4/BA.5 variants in nursing home residents after receipt of bivalent COVID-19 vaccine – Ohio and Rhode Island, September–November 2022 // MMWR. 2023. V. 72 (4). P. 100–106. https://doi.org/10.15585/mmwr.mm7204a4
  21. Candeloro M., Schulman S. Arterial thrombotic events in hospitalized COVID-19 patients: a short review and meta-analysis // Semin. Thromb. Hemost. 2023. V. 49 (1). P. 47–54. https://doi.org/10.1055/s-0042-1749661
  22. Chen J.M. Novel statistics predict the COVID-19 pandemic could terminate in 2022 // J. Med. Virol. 2022. V. 94 (6). P. 2845–2848. https://doi.org/10.1002/jmv.27661
  23. Connors J.M., Levy J.H. COVID-19 and its implications for thrombosis and anticoagulation // Blood. 2020. V. 135 (23). P. 2033–2040. https://doi.org/10.1182/blood.2020006000
  24. Conway E.M., Pryzdial E.L.G. Complement contributions to COVID-19 // Curr. Opin. Hematol. 2022. V. 29 (5). P. 259–265.
  25. Cugno M., Meroni P.L., Gualtierotti R. et al. Complement activation and endothelial perturbation parallel COVID-19 severity and activity // J. Autoimmun. 2021. V. 116. P. 102560. https://doi.org/10.1016/j.jaut.2020.102560
  26. D’Ardes D., Boccatonda A., Cocco G. et al. Impaired coagulation, liver dysfunction and COVID-19: discovering an intriguing relationship // World J. Gastroenterol. 2022. V. 28 (11). P. 1102–1112. https://doi.org/10.3748/wjg.v28.i11.1102
  27. Di Gennaro C., Galdiero M., Scherillo G. et al. Editorial COVID-19 and thrombosis 2023: new waves of SARS-CoV-2 infection, triage organization in emergency department and the association of VOCs/VOI with pulmonary embolism // Viruses. 2022. V. 14 (11). P. 2453. https://doi.org/10.3390/v14112453
  28. Diao B., Wang C.H., Wang R.S. et al. Human kidney is a target for novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection // medRxiv. 2020. https://doi.org/10.1101/2020.03.04.20031120
  29. Escher R., Breakey N., Lämmle B. Severe COVID-19 infection associated with endothelial activation // Thromb. Res. 2020. V. 190. P. 62. https://doi.org/10.1016/j.thromres.2020.04.014
  30. Falcinelli E., Petito E., Gresele P. The role of platelets, neutrophils and endothelium in COVID-19 infection // Expert Rev. Hematol. 2022. V. 15 (8). P. 727–745. https://doi.org/10.1080/17474086.2022.2110061
  31. Fox S.E., Akmatbekov A., Harbert J.L. et al. Pulmonary and cardiac pathology in African American patients with COVID-19: an autopsy series from New Orleans // Lancet Respir. Med. 2020. V. 8 (7). P. 681—686. https://doi.org/10.1016/S2213-2600(20)30243-5
  32. Frithiof R., Rostami E., Kumlien E. et al. Critical illness polyneuropathy, myopathy and neuronal biomarkers in COVID-19 patients: a prospective study // Clin. Neurophysiol. 2021. V. 132 (7). P. 1733–1740. https://doi.org/10.1016/j.clinph.2021.03.016
  33. Fujimura Y., Holland L.Z. COVID-19 microthrombosis: unusually large vWF multimers are a platform for activation of the alternative complement pathway under cytokine storm // Int. J. Hematol. 2022. V. 115 (4). P. 457–469. https://doi.org/10.1007/s12185-022-03324-w
  34. Gao Y., Wang C., Kang K. et al. Cytokine storm may not be the chief culprit for the deterioration of COVID-19 // Viral. Immunol. 2021. V. 34 (5). P. 336–341. https://doi.org/10.1089/vim.2020.0243
  35. Gauchel N., Rieder M., Krauel K. et al. Complement system component dysregulation is a distinctive feature of COVID-19 disease // J. Thromb. Thrombolysis. 2022. V. 53 (4). P. 788–797. https://doi.org/10.1007/s11239-021-02617-x
  36. Ghasemzadeh M., Ahmadi J., Hosseini E. Platelet-leukocyte crosstalk in COVID-19: how might the reciprocal links between thrombotic events and inflammatory state affect treatment strategies and disease prognosis? // Thromb. Res. 2022. V. 213. P. 179–194. https://doi.org/10.1016/j.thromres.2022.03.022
  37. Gorog D.A., Storey R.F., Gurbel P.A. et al. Current and novel biomarkers of thrombotic risk in COVID-19: a Consensus Statement from the International COVID-19 Thrombosis Biomarkers Colloquium // Nat. Rev. Cardiol. 2022. V. 19 (7). P. 475–495. https://doi.org/10.1038/s41569-021-00665-7
  38. Grobbelaar L.M., Venter C., Vlok M. et al. SARS-CoV-2 spike protein S1 induces fibrin(ogen) resistant to fibrinolysis: implications for microclot formation in COVID-19 // Biosci. Rep. 2021. V. 41 (8). P. BSR20210611. https://doi.org/10.1042/BSR20210611
  39. Grobler C., Maphumulo S.C., Grobbelaar L.M. et al. Covid-19: the rollercoaster of fibrin(ogen), D-dimer, von Willebrand factor, P-selectin and their interactions with endothelial cells, platelets and erythrocytes // Int. J. Mol. Sci. 2020. V. 21 (14). P. 5168. https://doi.org/10.3390/ijms21145168
  40. Gu S.X., Tyagi T., Jain K. et al. Thrombocytopathy and endotheliopathy: crucial contributors to COVID-19 thromboinflammation // Nat. Rev. Cardiol. 2021. V. 18 (3). P. 194–209. https://doi.org/10.1038/s41569-020-00469-1
  41. Guan W.J., Ni Z.Y., Hu Y. et al. Clinical characteristics of coronavirus disease 2019 in China // N. Engl. J. Med. 2020. V. 382 (18). P. 1708–1720. https://doi.org/10.1056/NEJMoa2002032
  42. Han H., Yang L., Liu R. et al. Prominent changes in blood coagulation of patients with SARS-CoV-2 infection // Clin. Chem. Lab. Med. 2020. V. 58 (7). P. 1116–1120.
  43. Harrison C. Focus shifts to antibody cocktails for COVID-19 cytokine storm // Nat. Biotechnol. 2020. V. 38 (8). P. 905–908.
  44. Hoffmann M., Kleine-Weber H., Pöhlmann S. A multibasic cleavage site in the spike protein of SARS-CoV-2 is essential for infection of human lung cells // Mol. Cell. 2020. V. 78. P. 779–784. https://doi.org/10.1016/j.molcel.2020.04.022
  45. Hottz E.D., Azevedo-Quintanilha I.G., Palhinha L. et al. Platelet activation and platelet-monocyte aggregate formation trigger tissue factor expression in patients with severe COVID-19 // Blood. 2020. V. 136 (11). P. 1330–1341. https://doi.org/10.1182/blood.2020007252
  46. Iba T., Wada H., Levy J.H. Platelet activation and thrombosis in COVID-19 // Semin. Thromb. Hemost. 2023. V. 49 (1). P. 55–61. https://doi.org/10.1055/s-0042-1749441
  47. Jackson C.B., Farzan M., Chen B., Choe H. Mechanisms of SARS-CoV-2 entry into cells // Nat. Rev. Mol. Cell Biol. 2022. V. 23 (1). P. 3–20. https://doi.org/10.1038/s41580-021-00418-x
  48. Jenny L., Dobó J., Gál P., Schroeder V. MASP-1 induced clotting – the first model of prothrombin activation by MASP-1 // PLoS One. 2015. V. 10 (12). P. e0144633. https://doi.org/10.1371/journal.pone.0144633
  49. Jenny L., Noser D., Larsen J.B. et al. MASP-1 of the complement system alters fibrinolytic behaviour of blood clots // Mol. Immunol. 2019. V. 114. P. 1–9. https://doi.org/10.1016/j.molimm.2019.07.005
  50. Jiang S.Q., Huang Q.F., Xie W.M. et al. The association between severe COVID-19 and low platelet count: evidence from 31 observational studies involving 7613 participants // Br. J. Haematol. 2020. V. 190 (1). P. e29–e33. https://doi.org/10.1111/bjh.16817
  51. Kakodkar P., Kaka N., Baig M.N. A comprehensive literature review on the clinical presentation, and management of the pandemic coronavirus disease 2019 (COVID-19) // Cureus. 2020. V. 12 (4). P. e7560. https://doi.org/10.7759/cureus.7560
  52. Kaur S., Singh A., Kaur J. et al. Upregulation of cytokine signalling in platelets increases risk of thrombophilia in severe COVID-19 patients // Blood Cells Mol. Dis. 2022. V. 94. P. 102653. https://doi.org/10.1016/j.bcmd.2022.102653
  53. Kerch G. Severe COVID-19 A review of suggested mechanisms based on the role of extracellular matrix stiffness // Int. J. Mol. Sci. 2023. V. 24 (2). P. 1187. https://doi.org/10.3390/ijms24021187
  54. Koupenova M. Potential role of platelets in COVID-19: implications for thrombosis // Res. Pract. Thromb. Haemost. 2020. V. 4 (5). P. 737–740. https://doi.org/10.1002/rth2.12397
  55. Kozarcanin H., Lood C., Munthe-Fog L. et al. The lectin complement pathway serine proteases (MASPs) represent a possible crossroad between the coagulation and complement systems in thromboinflammation // J. Thromb. Haemost. 2016. V. 14 (3). P. 531–545. https://doi.org/10.1111/jth.13208
  56. Krarup A., Wallis R., Presanis J.S. et al. Simultaneous activation of complement and coagulation by MBL-associated serine protease 2 // PLoS One. 2007. V. 2 (7). P. e623. https://doi.org/10.1371/journal.pone.0000623
  57. Kuhn C.C., Basnet N., Bodakuntla S. et al. Direct Cryo-ET observation of platelet deformation induced by SARS-CoV-2 spike protein // bioRxiv. Preprint. 2022. https://doi.org/10.1101/2022.11.22.517574
  58. Lee M.H., Perl D.P., Steiner J. et al. Neurovascular injury with complement activation and inflammation in COVID-19 // Brain. 2022. V. 145 (7). P. 2555–2568. https://doi.org/10.1093/brain/awac151
  59. Levi M., Thachil J., Iba T., Levy J.H. Coagulation abnormalities and thrombosis in patients with COVID-19 // Lancet Haematol. 2020. V. 7 (6). P. e438–e440.https://doi.org/10.1016/S2352-3026(20)30145-9
  60. Li T., Yang Y., Li Y. et al. Platelets mediate inflammatory monocyte activation by SARS-CoV-2 spike protein // J. Clin. Invest. 2022. V. 132 (4). P. e150101. https://doi.org/10.1172/JCI150101
  61. Liang Y., Fang D., Gao X. et al. Circulating microRNAs as emerging regulators of COVID-19 // Theranostics. 2023. V. 13 (1). P. 125–147. https://doi.org/10.7150/thno.78164
  62. Liao M., Liu Y., Yuan J. et al. Single-cell landscape of bronchoalveolar immune cells in patients with COVID-19 // Nat. Med. 2020. V. 26 (6). P. 842–844. https://doi.org/10.1038/s41591-020-0901
  63. Lippi G., Favaloro E.J. What we know (and do not know) regarding th pathogenesis of pulmonary thrombosis in COVID-19 // Semin. Thromb. Hemost. 2023. V. 49 (1). P. 27–33. https://doi.org/10.1055/s-0041-1742091
  64. Liu Y., Sun W., Guo Y. et al. Association between platelet parameters and mortality in coronavirus disease 2019: retrospective cohort study // Platelets. 2020. V. 31 (4). P. 490–496. https://doi.org/10.1080/09537104.2020.1754383
  65. Ma L., Sahu S.K., Cano M. et al. Increased complement activation is a distinctive feature of severe SARS-CoV-2 infection // Sci. Immunol. 2021. V. 6. P. eabh2259. https://doi.org/10.1126/sciimmunol.abh2259
  66. Magro C., Mulvey J.J., Berlin D. et al. Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: a report of five cases // Transl. Res. 2020. V. 220. P. 1–13. https://doi.org/10.1016/j.trsl.2020.04.007
  67. McFadyen J.D., Stevens H., Peter K. The emerging threat of (micro)thrombosis in COVID-19 and its therapeutic implications // Circ. Res. 2020. V. 127 (4). P. 571–587. https://doi.org/10.1161/CIRCRESAHA.120.317447
  68. Merad M., Martin J.C. Pathological inflammation in patients with COVID-19: a key role for monocytes and macrophages // Nat. Rev. Immunol. 2020. V. 20 (6). P. 355–362. https://doi.org/10.1038/s41577-020-0331-4
  69. Middleton E.A., He X.Y., Denorme F. et al. Neutrophil extracellular traps contribute to immunothrombosis in COVID-19 acute respiratory distress syndrome // Blood. 2020. V. 136. P. 1169–1179. https://doi.org/10.1182/blood.2020007008
  70. Mizurini D.M., Hottz E.D., Bozza P.T., Monteiro R.Q. Fundamentals in COVID-19-associated thrombosis: molecular and cellular aspects // Front. Cardiovasc. Med. 2021. V. 8. P. 785738. https://doi.org/10.3389/fcvm.2021.785738
  71. Moraes E.C.D.S., Martins-Gonçalves R., Da Silva L.R. et al. Proteomic profile of procoagulant extracellular vesicles reflects complement system activation and platelet hyperreactivity of patients with severe COVID-19 // Front. Cell. Infect. Microbiol. 2022. V. 12. P. 926352. https://doi.org/10.3389/fcimb.2022.926352
  72. Morris G., Bortolasci C.C., Puri B.K. et al. The pathophysiology of SARS-CoV-2: a suggested model and therapeutic approach // Life Sci. 2020. V. 258. P. 118166. https://doi.org/10.1016/j.lfs.2020.118166
  73. Mukund K., Mathee K., Subramaniam S. Plasmin cascade mediates thrombotic events in SARS-CoV-2 infection via complement and platelet-activating systems // IEEE Open J. Eng. Med. Biol. 2020. V. 1. P. 220–227. https://doi.org/10.1109/OJEMB.2020.3014798
  74. Nahum J., Morichau-Beauchant T., Daviaud F. et al. Venous thrombosis among critically ill patients with coronavirus disease 2019 (COVID-19) // JAMA Netw. Open. 2020. V. 3 (5). P. e2010478. https://doi.org/10.1001/jamanetworkopen.2020.10478
  75. Panigada M., Bottino N., Tagliabue P. et al. Hypercoagulability of COVID-19 patients in intensive care unit: a report of thromboelastography findings and other parameters of hemostasis // J. Thromb. Haemost. 2020. V. 18 (7). P. 1738–1742. https://doi.org/10.1111/jth.14850
  76. Parums D.V. Editorial: the XBB.1.5. (“Kraken”) subvariant of Omicron SARS-CoV-2 and its rapid global spread // Med. Sci. Monit. 2023. V. 29. P. e939580. https://doi.org/10.12659/MSM.939580
  77. Passariello M., Vetrei C., Amato F., De Lorenzo C. Interactions of spike-RBD of SARS-CoV-2 and platelet factor 4: new insights in the etiopathogenesis of thrombosis // Int. J. Mol. Sci. 2021. V. 22 (16). P. 8562. https://doi.org/10.3390/ijms22168562
  78. Perico L., Morigi M., Galbusera M. et al. SARS-CoV-2 spike protein 1 activates microvascular endothelial cells and complement system leading to platelet aggregation // Front. Immunol. 2022. V. 13. P. 827146. https://doi.org/10.3389/fimmu.2022.827146
  79. Poor H.D. Pulmonary thrombosis and thromboembolism in COVID-19 // Chest. 2021. V. 160 (4). P. 1471–1480. https://doi.org/10.1016/j.chest.2021.06.016
  80. Qi F., Qian S., Zhang S., Zhang Z. Single cell RNA sequencing of 13 human tissues identify cell types and receptors of human coronaviruses // Biochem. Biophys. Res. Commun. 2020. V. 526 (1). P. 135–140. https://doi.org/10.1016/j.bbrc.2020.03.044
  81. Rohlfing A.K., Rath D., Geisler T., Gawaz M. Platelets and COVID-19 // Hamostaseologie. 2021. V. 41 (5). P. 379–385. https://doi.org/10.1055/a-1581-4355
  82. Santos A.P., Couto C.F., Pereira S.S., Monteiro M.P. Is serotonin the missing link between COVID-19 course of severity in patients with diabetes and obesity? // Neuroendocrinology. 2022. V. 112. P. 1039–1045. https://doi.org/10.1159/000522115
  83. Sastry S., Cuomo F., Muthusamy J. COVID-19 and thrombosis: the role of hemodynamics // Thromb. Res. 2022. V. 212. P. 51–57. https://doi.org/10.1016/j.thromres.2022.02.016
  84. Sheth A.R., Grewal U.S., Patel H.P. et al. Possible mechanisms responsible for acute coronary events in COVID-19 // Med. Hypotheses. 2020. V. 143. P. 110125. https://doi.org/10.1016/j.mehy.2020.110125
  85. Sonmez O., Sonmez M. Role of platelets in immune system and inflammation // Porto Biomed. J. 2017. V. 2 (6). P. 311–314. https://doi.org/10.1016/j.pbj.2017.05.005
  86. Stark K. Platelet-neutrophil crosstalk and netosis // HemaSphere. 2019. V. 3. P. 89–91. https://doi.org/10.1097/HS9.0000000000000231
  87. Suh Y.J., Hong H., Ohana M. et al. Pulmonary embolism and deep vein thrombosis in COVID-19: a systematic review and meta-analysis // Radiology. 2021. V. 298. P. E70–E80. https://doi.org/10.1148/radiol.2020203557
  88. Tang N., Li D., Wang X., Sun Z. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia // J. Thromb. Haemost. 2020. V. 18. P. 844–847. https://doi.org/10.1111/jth.14768
  89. Taus F., Salvagno G., Canè S. et al. Platelets promote thromboinflammation in SARS-CoV-2 pneumonia // Arterioscler. Thromb. Vasc. Biol. 2020. V. 40 (12). P. 2975–2989. https://doi.org/10.1161/ATVBAHA.120.315175
  90. Thachil J., Tang N., Gando S. et al. ISTH interim guidance on recognition and management of coagulopathy in COVID-19 // J. Thromb. Haemost. 2020. V. 18 (5). P. 1023–1026. https://doi.org/10.1111/JTH.14860
  91. Thillai M., Patvardhan C., Swietlik E.M. et al. Functional respiratory imaging identifies redistribution of pulmonary blood flow in patients with COVID-19 // Thorax. 2021. V. 76 (2). P. 182–184. https://doi.org/10.1136/thoraxjnl-2020-215395
  92. Thomas W., Varley J., Johnston A. et al. Thrombotic complications of patients admitted to intensive care with COVID-19 at a teaching hospital in the United Kingdom // Thromb. Res. 2020. V. 191. P. 76–77. https://doi.org/101016/j.thromres.2020.04.028
  93. Tiwari R., Mishra A.R., Mikaeloff F. et al. In silico and in vitro studies reveal complement system drives coagulation cascade in SARS-CoV-2 pathogenesis // Comput. Struct. Biotechnol. J. 2020. V. 18. P. 3734–3744. https://doi.org/10.1016/j.csbj.2020.11.005
  94. Ulanowska M., Olas B. Modulation of hemostasis in COVID-19; blood platelets may be important pieces in the COVID-19 puzzle // Pathogens. 2021. V. 10 (3). P. 370. https://doi.org/10.3390/pathogens10030370
  95. Vadasz Z., Brenner B., Toubi E. Immune-mediated coagulopathy in COVID-19 infection // Semin. Thromb. Hemost. 2020. V. 46 (7). P. 838–840. https://doi.org/10.1055/s-0040-1714272
  96. Varatharajah N., Rajah S. Microthrombotic complications of COVID-19 are likely due to embolism of circulating endothelial derived ultralarge von Willebrand factor (eULvWF) decorated-platelet strings // Fed. Pract. 2020. V. 37 (6). P. 258–259.
  97. Violi F., Pignatelli P., Cammisotto V. et al. COVID-19 and thrombosis: clinical features, mechanism of disease, and therapeutic implications // Kardiol. Pol. 2021. V. 79 (11). P. 1197–1205. https://doi.org/10.33963/KP.a2021.154
  98. Wang J., Doran J. The many faces of cytokine release syndrome-related coagulopathy // Clin. Hematol. Int. 2021. V. 3 (1). P. 3–12. https://doi.org/10.2991/chi.k.210117.001
  99. Wienkamp A.K., Erpenbeck L., Rossaint J. Platelets in the NETworks interweaving inflammation and thrombosis // Front. Immunol. 2022. V. 13. P. 953129. https://doi.org/10.3389/fimmu.2022.953129
  100. Wool G.D., Miller J.L. The impact of COVID-19 disease on platelets and coagulation // Pathobiology. 2021. V. 88 (1). P. 15–27. https://doi.org/10.1159/000512007
  101. Xiang M., Wu X., Jing H. et al. The impact of platelets on pulmonary microcirculation throughout COVID-19 and its persistent activating factors // Front. Immunol. 2022. V. 13. P. 955654. https://doi.org/10.3389/fimmu.2022.955654
  102. Xiao T., Lu J., Zhang J. et al. A trimeric human angiotensin-converting enzyme 2 as an anti-SARS-CoV-2 agent // Nat. Struct. Mol. Biol. 2021. V. 28. P. 202–209. https://doi.org/10.1038/s41594-020-00549-3
  103. Yang X., Yang Q., Wang Y. et al. Thrombocytopenia and its association with mortality in patients with COVID-19 // J. Thromb. Haemost. 2020. V. 18. P. 1469–1472. https://doi.org/10.1111/jth.14848
  104. Ye Q., Wang B., Mao J. The pathogenesis and treatment of the “cytokine storm” in COVID-19 // J. Infect. 2020. V. 80. P. 607–613. https://doi.org/10.1016/j.jinf.2020.03.037
  105. Yu J., Yuan X., Chen H. et al. Direct activation of the alternative complement pathway by SARS-CoV-2 spike proteins is blocked by factor D inhibition // Blood. 2020. V. 136 (18). P. 2080–2089. https://doi.org/10.1182/blood.2020008248
  106. Zhang S., Liu Y., Wang X. et al. SARS-CoV-2 binds platelet ACE2 to enhance thrombosis in COVID-19 // J. Hematol. Oncol. 2020. V. 13 (1). P. 120. https://doi.org/10.1186/s13045-020-00954-7
  107. Zhang Y., Zeng X., Jiao Y. et al. Mechanisms involved in the development of thrombocytopenia in patients with COVID-19 // Thromb. Res. 2020. V. 193. P. 110–115.
  108. Zhou F., Yu T., Du R. et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study // Lancet. 2020. V. 395. P. 1054–1062. https://doi.org/10.1016/S0140-6736(20)30566-3
  109. Zhu A., Real F., Capron C. et al. Infection of lung megakaryo-cytes and platelets by SARS-CoV-2 anticipate fatal COVID-19 // Cell. Mol. Life Sci. 2022. V. 79 (7). P. 365. https://doi.org/10.1007/s00018-022-04318-x
  110. Zuo Y., Yalavarthi S., Shi H. et al. Neutrophil extracellular traps in COVID-19 // JCI Insight. 2020. V. 5 (11). P. e138999. https://doi.org/10.1172/jci.insight.138999

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