Role of Transforming Growth Factor-β in Pathogenesis of Pulmonary Fibrosis in COVID-19, Post-COVID Syndrome, Oncological and Chronic Inflammatory Lung Diseases

Andrey V. Budnevsky , Sergey N. Avdeev , Evgeny S. Ovsyannikov , Viktoria V. Shishkina , Nadezhda G. Alekseeva , Inna M. Perveeva , Avag G. Kitoyan , Lyubov N. Antakova , Anastasia S. Yurchenko

I.P. Pavlov Russian Medical Biological Herald ›› 2024, Vol. 32 ›› Issue (3) : 499 -510.

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I.P. Pavlov Russian Medical Biological Herald ›› 2024, Vol. 32 ›› Issue (3) : 499 -510. DOI: 10.17816/PAVLOVJ625007
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Role of Transforming Growth Factor-β in Pathogenesis of Pulmonary Fibrosis in COVID-19, Post-COVID Syndrome, Oncological and Chronic Inflammatory Lung Diseases

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Abstract

INTRODUCTION: Persistent post-COVID syndrome is the persistent physical, medical and cognitive sequelae of coronavirus disease 2019 (COVID-19), including persistent immunosuppression, pulmonary, cardiac and vascular fibrosis which lead to increased mortality and impair the quality of life of patients.

АIM: To analyze the completed foreign and domestic studies on the pathophysiology of transforming growth factor-β (TGF-β) in conditions of COVID-19, post-COVID syndrome, oncological and chronic inflammatory lung diseases.

Mast cells are among the main producers of inflammatory cytokines in COVID-19, their stimulation leads to the release of many proinflammatory cytokines, such as interleukin 1β, tumor necrosis factor α, interleukin 6, and also TGF-β. The basis of the pathogenesis of post-COVID syndrome is the overexpression of TGF-β leading to a prolonged state of immunosuppression and fibrosis. TGF-β acts as a tumor suppressor inhibiting proliferation and inducing apoptosis in the early stages of oncogenesis; plays an important role in most cellular biological processes leading to remodeling of the airway structures; is involved in epithelial changes, in subepithelial fibrosis, remodeling of smooth muscle of airways and in microvascular changes; induces resistance to glucocorticosteroids; stimulates the production of blood coagulation factor XII, thereby leading to development of potentially fatal complications, such as pulmonary embolism and ischemic stroke.

CONCLUSION: In this literature review, a structured analysis of a multicomponent role of TGF-β in the pathogenesis of post-COVID syndrome, pulmonary fibrosis in COVID-19, tumors of respiratory system, chronic obstructive pulmonary disease, bronchial asthma, is given. A possible use of TGF-β as a biomarker of severe and moderate degree of COVID-19 is substantiated.

Keywords

transforming growth factor β / COVID-19 / mast cells / chronic obstructive pulmonary disease / tumors

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Andrey V. Budnevsky, Sergey N. Avdeev, Evgeny S. Ovsyannikov, Viktoria V. Shishkina, Nadezhda G. Alekseeva, Inna M. Perveeva, Avag G. Kitoyan, Lyubov N. Antakova, Anastasia S. Yurchenko. Role of Transforming Growth Factor-β in Pathogenesis of Pulmonary Fibrosis in COVID-19, Post-COVID Syndrome, Oncological and Chronic Inflammatory Lung Diseases. I.P. Pavlov Russian Medical Biological Herald, 2024, 32(3): 499-510 DOI:10.17816/PAVLOVJ625007

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References

[1]

Oronsky B, Larson C, Hammond TC, et al. A Review of Persistent Post-COVID Syndrome (PPCS). Clin Rev Allergy immunol. 2023;64(1): 66–74. doi: 10.1007/s12016-021-08848-3

[2]

Oronsky B., Larson C., Hammond T.C., et al. A Review of Persistent Post-COVID Syndrome (PPCS) // Clin. Rev. Allergy Immunol. 2023. Vol. 64, No. 1. P. 66–74. doi: 10.1007/s12016-021-08848-3

[3]

Walkey AJ, Summer R, Ho V, et al. Acute respiratory distress syndrome: epidemiology and management approaches. Clin Epidemiol. 2012;4:159–69. doi: 10.2147/clep.s288000

[4]

Walkey A.J., Summer R., Ho V., et al. Acute respiratory distress syndrome: epidemiology and management approaches // Clin. Epidemiol. 2012. Vol. 4. P. 159–169. doi: 10.2147/clep.s28800

[5]

Williams AE, Chambers RC. The mercurial nature of neutrophils: still an enigma in ARDS?. Am J Physiol Lung Cell Mol Physiol. 2014;306(3):L217–30. doi: 10.1152/ajplung.00311.2013

[6]

Williams A.E., Chambers R.C. The mercurial nature of neutrophils: still an enigma in ARDS? // Am. J. Physiol. Lung Cell. Mol. Physiol. 2014. Vol. 306, No. 3. P. L217–L230. doi: 10.1152/ajplung.00311.2013

[7]

Burnham EL, Janssen WJ, Riches DW, et al. The fibroproliferative response in acute respiratory distress syndrome: mechanisms and clinical significance. Eur Respir J. 2014;43(1):276–85. doi: 10.1183/09031936.00196412

[8]

Burnham E.L., Janssen W.J., Riches D.W., et al. The fibroproliferative response in acute respiratory distress syndrome: mechanisms and clinical significance // Eur. Respir. J. 2014. Vol. 43, No. 1. P. 276–285. doi: 10.1183/09031936.00196412

[9]

Wismans LV, Lopuhaä B, de Koning W, et al. Increase of mast cells in COVID-19 pneumonia may contribute to pulmonary fibrosis and thrombosis. Histopathology. 2023;82(3):407–19. doi: 10.1111/his.14838

[10]

Wismans L.V., Lopuhaä B., de Koning W., et al. Increase of mast cells in COVID-19 pneumonia may contribute to pulmonary fibrosis and thrombosis // Histopathology. 2023. Vol. 82, No. 3. Р. 407–419. doi: 10.1111/his.14838

[11]

David CJ, Massagué J. Contextual determinants of TGFβ action in development, immunity and cancer. Nat Rev Mol Cell Biol. 2018;19(7): 419–35. doi: 10.1038/s41580-018-0007-0

[12]

David C.J., Massagué J. Contextual determinants of TGFβ action in development, immunity and cancer // Nat. Rev. Mol. Cell Biol. 2018. Vol. 19, No. 7. P. 419–435. doi: 10.1038/s41580-018-0007-0

[13]

Saito A, Horie M, Nagase T. TGF-β Signaling in Lung Health and Disease. Int J Mol Sci. 2018;19(8):2460. doi: 10.3390/ijms190824600

[14]

Saito A., Horie M., Nagase T. TGF-β Signaling in Lung Health and Disease // Int. J. Mol. Sci. 2018. Vol. 19, No. 8. P. 2460. doi: 10.3390/ijms19082460

[15]

Shi M, Zhu J, Wang R, et al. Latent TGF-β structure and activation. Nature. 2011;474(7351):343–9. doi: 10.1038/nature10152

[16]

Shi M., Zhu J., Wang R., et al. Latent TGF-β structure and activation // Nature. 2011. Vol. 474, No. 7351. P. 343–349. doi: 10.1038/nature10152

[17]

Gordon KJ, Blobe GC. Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim Biophys Acta. 2008;1782(4):197–228. doi: 10.1016/j.bbadis.2008.01.006

[18]

Gordon K.J., Blobe G.C. Role of transforming growth factor-beta superfamily signaling pathways in human disease // Biochim. Biophys. Acta. 2008. Vol. 1782, No. 4. P. 197–228. doi: 10.1016/j.bbadis.2008.01.006

[19]

Kanzaki T, Olofsson A, Morén A, et al. TGF-beta 1 binding protein: a component of the large latent complex of TGF-beta 1 with multiple repeat sequences. Cell. 1990;61(6):1051–61. doi: 10.1016/0092-8674(90)90069-q

[20]

Kanzaki T., Olofsson A., Morén A., et al. TGF-beta 1 binding protein: A component of the large latent complex of TGF-beta 1 with multiple repeat sequences // Cell. 1990. Vol. 61, No. 6. P. 1051–1061. doi: 10.1016/0092-8674(90)90069-q

[21]

Minton K. Extracellular matrix: Preconditioning the ECM for fibrosis. Nat Rev Mol Cell Biol. 2014;15(12):766–7. doi: 10.1038/nrm3906

[22]

Minton K. Extracellular matrix: Preconditioning the ECM for fibrosis // Nat. Rev. Mol. Cell Biol. 2014. Vol. 15, No. 12. P. 766–767. doi: 10.1038/nrm3906

[23]

Xu P, Liu J, Derynck R. Post-translational regulation of TGF-β receptor and Smad signaling. FEBS Lett. 2012;586(14):1871–84. doi: 10.1016/j.febslet.2012.05.010

[24]

Xu P., Liu J., Derynck R. Post-translational regulation of TGF-β receptor and Smad signaling // FEBS Lett. 2012. Vol. 586, No. 14. P. 1871–1884. doi: 10.1016/j.febslet.2012.05.010

[25]

Massagué J. TGFβ signalling in context. Nat Rev Mol Cell Biol. 2012;13(10):616–30. doi: 10.1038/nrm3434

[26]

Massagué J. TGFβ signalling in context // Nat. Rev. Mol. Cell Biol. 2012. Vol. 13, No. 10. P. 616–630. doi: 10.1038/nrm3434

[27]

Muppala S, Xiao R, Krukovets I, et al. Thrombospondin-4 mediates TGF-β-induced angiogenesis. Oncogene. 2017;36(36):5189–98. doi: 10.1038/onc.2017.140

[28]

Muppala S., Xiao R., Krukovets I., et al. Thrombospondin-4 mediates TGF-β-induced angiogenesis // Oncogene. 2017. Vol. 36, No. 36. P. 5189–5198. doi: 10.1038/onc.2017.140

[29]

Robertson IB, Horiguchi M, Zilberberg L, et al. Latent TGF-β-binding proteins. Matrix Biol. 2015;47:44–53. doi: 10.1016/j.matbio.2015.05.005

[30]

Robertson I.B., Horiguchi M., Zilberberg L., et al. Latent TGF-β-binding proteins // Matrix Biol. 2015. Vol. 47. P. 44–53. doi: 10.1016/j.matbio.2015.05.005

[31]

Moustakas A, Heldin C–H. Non-Smad TGF-beta signals. J Cell Sci. 2005;118(Pt 16):3573–84. doi: 10.1242/jcs.02554

[32]

Moustakas A., Heldin C.–H. Non-Smad TGF-beta signals // J. Cell Sci. 2005. Vol. 118, Pt. 16. P. 3573–3584. doi: 10.1242/jcs.02554

[33]

Galvão F Jr, Grokoski KC, da Silva BB, et al. The amyloid precursor protein (APP) processing as a biological link between Alzheimer's disease and cancer. Ageing Res Rev. 2019;49:83–91. doi: 10.1016/j.arr.2018.11.007

[34]

Galvão F. Jr., Grokoski K.C., da Silva B.B., et al. The amyloid precursor protein (APP) processing as a biological link between Alzheimer's disease and cancer // Ageing Res. Rev. 2019. Vol. 49. P. 83–91. doi: 10.1016/j.arr.2018.11.007

[35]

Johnson HE, Toettcher JE. Signaling Dynamics Control Cell Fate in the Early Drosophila Embryo. Dev Cell. 2019;48(3):361–70.e3. doi: 10.1016/j.devcel.2019.01.009

[36]

Johnson H.E., Toettcher J.E. Signaling Dynamics Control Cell Fate in the Early Drosophila Embryo // Dev. Cell. 2019. Vol. 48, № 3. P. 361–370.e3. doi: 10.1016/j.devcel.2019.01.009

[37]

Böhmer RM. IL-3-dependent early erythropoiesis is stimulated by autocrine transforming growth factor beta. Stem Cells. 2004;22(2): 216–24. doi: 10.1634/stemcells.22-2-216

[38]

Böhmer R.M. IL-3-dependent early erythropoiesis is stimulated by autocrine transforming growth factor beta // Stem Cells. 2004. Vol. 22, No. 2. P. 216–224. doi: 10.1634/stemcells.22-2-216

[39]

Jinnin M, Ihn H, Tamaki K. Characterization of SIS3, a novel specific inhibitor of Smad3, and its effect on transforming growth factor-beta1-induced extracellular matrix expression. Mol Pharmacol. 2006;69(2):597–607. doi: 10.1124/mol.105.017483

[40]

Jinnin M., Ihn H., Tamaki K. Characterization of SIS3, a novel specific inhibitor of Smad3, and its effect on transforming growth factor-beta1-induced extracellular matrix expression // Mol. Pharmacol. 2006. Vol. 69, No. 2. P. 597–607. doi: 10.1124/mol.105.017483

[41]

Ota K, Quint P, Weivoda MM, et al. Transforming growth factor beta 1 induces CXCL16 and leukemia inhibitory factor expression in osteoclasts to modulate migration of osteoblast progenitors. Bone. 2013;57(1):68–75. doi: 10.1016/j.bone.2013.07.023

[42]

Ota K., Quint P., Weivoda M.M., et al. Transforming growth factor beta 1 induces CXCL16 and leukemia inhibitory factor expression in osteoclasts to modulate migration of osteoblast progenitors // Bone. 2013. Vol. 57, No. 1. P. 68–75. doi: 10.1016/j.bone.2013.07.023

[43]

Batra V, Musani AI, Hastie AT, et al. Bronchoalveolar lavage fluid concentrations of transforming growth factor (TGF)-beta1, TGF-beta2, interleukin (IL)-4 and IL-13 after segmental allergen challenge and their effects on alpha-smooth muscle actin and collagen III synthesis by primary human lung fibroblasts. Clin Exp Allergy. 2004;34(3): 437–44. doi: 10.1111/j.1365-2222.2004.01885.x

[44]

Batra V., Musani A.I., Hastie A.T., et al. Bronchoalveolar lavage fluid concentrations of transforming growth factor (TGF)-beta1, TGF-beta2, interleukin (IL)-4 and IL-13 after segmental allergen challenge and their effects on alpha-smooth muscle actin and collagen III synthesis by primary human lung fibroblasts // Clin. Exp. Allergy. 2004. Vol. 34, No. 3. P. 437–444. doi: 10.1111/j.1365-2222.2004.01885.x

[45]

Chiang C–H, Chuang C–H, Liu S–L. Transforming growth factor-β1 and tumor necrosis factor-α are associated with clinical severity and airflow limitation of COPD in an additive manner. Lung. 2014;192(1): 95–102. doi: 10.1007/s00408-013-9520-2

[46]

Chiang C.–H., Chuang C.–H., Liu S.–L. Transforming growth factor-β1 and tumor necrosis factor-α are associated with clinical severity and airflow limitation of COPD in an additive manner // Lung. 2014. Vol. 192, No. 1. P. 95–102. doi: 10.1007/s00408-013-9520-2

[47]

Hinz B. The extracellular matrix and transforming growth factor-β1: Tale of a strained relationship. Matrix Biol. 2015;47:54–65. doi: 10.1016/j.matbio.2015.05.006

[48]

Hinz B. The extracellular matrix and transforming growth factor-β1: Tale of a strained relationship // Matrix Biol. 2015. Vol. 47. P. 54–65. doi: 10.1016/j.matbio.2015.05.006

[49]

Brown SD, Baxter KM, Stephenson ST, et al. Airway TGF-β1 and oxidant stress in children with severe asthma: association with airflow limitation. J Allergy Clin Immunol. 2012;129(2):388–96.e1-8. doi: 10.1016/j.jaci.2011.11.037

[50]

Brown S.D., Baxter K.M., Stephenson S.T., et al. Airway TGF-β1 and oxidant stress in children with severe asthma: association with airflow limitation // J. Allergy Clin. Immunol. 2012. Vol. 129, No. 2. P. 388–396.e1-8. doi: 10.1016/j.jaci.2011.11.037

[51]

Harris WT, Muhlebach MS, Oster RA, et al. Transforming growth factor-beta(1) in bronchoalveolar lavage fluid from children with cystic fibrosis. Pediatr Pulmonol. 2009;44(11):1057–64. doi: 10.1002/ppul.21079

[52]

Harris W.T., Muhlebach M.S., Oster R.A., et al. Transforming growth factor-beta(1) in bronchoalveolar lavage fluid from children with cystic fibrosis // Pediatr. Pulmonol. 2009. Vol. 44, No. 11. P. 1057–1064. doi: 10.1002/ppul.21079

[53]

Thomas BJ, Kan-O K, Loveland KL, et al. In the Shadow of Fibrosis: Innate Immune Suppression Mediated by Transforming Growth Factor-β. Am J Respir Cell Mol Biol. 2016;55(6):759–66. doi: 10.1165/rcmb.2016-0248ps

[54]

Thomas B.J., Kan-O K., Loveland K.L., et al. In the Shadow of Fibrosis: Innate Immune Suppression Mediated by Transforming Growth Factor-β // Am. J. Respir. Cell Mol. Biol. 2016. Vol. 55, No. 6. P. 759–766. doi: 10.1165/rcmb.2016-0248ps

[55]

Matsumoto K, Inoue H. Viral infections in asthma and COPD. Respir Investig. 2014;52(2):92–100. doi: 10.1016/j.resinv.2013.08.005

[56]

Matsumoto K., Inoue H. Viral infections in asthma and COPD // Respir. Investig. 2014. Vol. 52, No. 2. P. 92–100. doi: 10.1016/j.resinv.2013.08.005

[57]

Xia YC, Radwan A, Keenan CR, et al. Glucocorticoid Insensitivity in Virally Infected Airway Epithelial Cells Is Dependent on Transforming Growth Factor-β Activity. PLoS Pathog. 2017;13(1):e1006138. doi: 10.1371/journal.ppat.1006138

[58]

Xia Y.C., Radwan A., Keenan C.R., et al. Glucocorticoid Insensitivity in Virally Infected Airway Epithelial Cells Is Dependent on Transforming Growth Factor-β Activity // PLoS Pathog. 2017. Vol. 13, No. 1. P. e1006138. doi: 10.1371/journal.ppat.1006138

[59]

Korkut A, Zaidi S, Kanchi RS, et al. A Pan-Cancer Analysis Reveals High-Frequency Genetic Alterations in Mediators of Signaling by the TGF-β Superfamily. Cell Syst. 2018;7(4):422–37.e7. doi: 10.1016/j.cels.2018.08.010

[60]

Korkut A., Zaidi S., Kanchi R.S., et al. A Pan-Cancer Analysis Reveals High-Frequency Genetic Alterations in Mediators of Signaling by the TGF-β Superfamily // Cell Syst. 2018. Vol. 7, No. 4. P. 422–437.e7. doi: 10.1016/j.cels.2018.08.010

[61]

Cortez VS, Ulland TK, Cervantes–Barragan L, et al. SMAD4 impedes the conversion of NK cells into ILC1-like cells by curtailing non-canonical TGF-β signaling. Nat Immunol. 2017;18(9):995–1003. doi: 10.1038/ni.3809

[62]

Cortez V.S., Ulland T.K., Cervantes–Barragan L., et al. SMAD4 impedes the conversion of NK cells into ILC1-like cells by curtailing non-canonical TGF-β signaling // Nat. Immunol. 2017. Vol. 18, No. 9. P. 995–1003. doi: 10.1038/ni.3809

[63]

Wang Y, Chu J, Yi P, et al. SMAD4 promotes TGF-β-independent NK cell homeostasis and maturation and antitumor immunity. J Clin Invest. 2018;128(11):5123–36. doi: 10.1172/jci121227

[64]

Wang Y., Chu J., Yi P., et al. SMAD4 promotes TGF-β-independent NK cell homeostasis and maturation and antitumor immunity // J. Clin. Invest. 2018. Vol. 128, No. 11. P. 5123–5136. doi: 10.1172/jci121227

[65]

Frey B, Rückert M, Deloch L, et al. Immunomodulation by ionizing radiation-impact for design of radio-immunotherapies and for treatment of inflammatory diseases. Immunol Rev. 2017;280(1):231–48. doi: 10.1111/imr.12572

[66]

Frey B., Rückert M., Deloch L., et al. Immunomodulation by ionizing radiation-impact for design of radio-immunotherapies and for treatment of inflammatory diseases // Immunol. Rev. 2017. V ol. 280, No. 1. P. 231–248. doi: 10.1111/imr.12572

[67]

Wang E–Y, Chen H, Sun B–Q, et al. Serum levels of the IgA isotype switch factor TGF-β1 are elevated in patients with COVID-19. FEBS Lett. 2021;595(13):1819–24. doi: 10.1002/1873-3468.14104

[68]

Wang E.–Y., Chen H., Sun B.–Q., et al. Serum levels of the IgA isotype switch factor TGF-β1 are elevated in patients with COVID-19 // FEBS Lett. 2021. Vol. 595, No. 13. P. 1819–1824. doi: 10.1002/1873-3468.14104

[69]

Chen W. A potential treatment of COVID-19 with TGF-β blockade. Int J Biol Sci. 2020;16(11):1954–5. doi: 10.7150/ijbs.46891

[70]

Chen W. A potential treatment of COVID-19 with TGF-β blockade // Int. J. Biol. Sci. 2020. Vol. 16, No. 11. P. 1954–1955. doi: 10.7150/ijbs.46891

[71]

Budnevsky AV, Ovsyannikov ES, Shishkina VV, et al. Possible Unexplored Aspects of Covid-19 Pathogenesis: The Role of Carboxypeptidase A3. International Journal of Biomedicine. 2022;12(2):179–82. doi: 10.21103/Article12(2)_RA1

[72]

Budnevsky A.V., Ovsyannikov E.S., Shishkina V.V., et al. Possible Unexplored Aspects of COVID-19 Pathogenesis: The Role of Carboxypeptidase A3 // International Journal of Biomedicine. 2022. Vol. 12, No. 2. P. 179–182. doi: 10.21103/Article12(2)_RA1

[73]

Budnevsky AV, Ovsyannikov ES, Tokmachev RE, et al. The role of mast cells in the pathogenesis of COVID-19. Pakistan Journal of Medical & Health Sciences. 2022;16(06):422–4. doi: 10.53350/pjmhs22166422

[74]

Budnevsky A.V., Ovsyannikov E.S., Tokmachev R.E., et al. The role of mast cells in the pathogenesis of COVID-19 // Pakistan Journal of Medical & Health Sciences. 2022. Vol. 16, No. 06. P. 422–424. doi: 10.53350/pjmhs22166422

[75]

Delpino MV, Quarleri J. SARS-CoV-2 Pathogenesis: Imbalance in the Renin-Angiotensin System Favors Lung Fibrosis. Front Cell Infect Microbiol. 2020;10:340. doi: 10.3389/fcimb.2020.00340

[76]

Delpino M.V., Quarleri J. SARS-CoV-2 Pathogenesis: Imbalance in the Renin-Angiotensin System Favors Lung Fibrosis // Front. Cell. Infect. Microbiol. 2020. Vol. 10. P. 340. doi: 10.3389/fcimb.2020.00340

[77]

Ongchai S, Somnoo O, Kongdang P, et al. TGF-β1 upregulates the expression of hyaluronan synthase 2 and hyaluronan synthesis in culture models of equine articular chondrocytes. J Vet Sci. 2018; 19(6):735–43. doi: 10.4142/jvs.2018.19.6.735

[78]

Ongchai S., Somnoo O., Kongdang P., et al. TGF-β1 upregulates the expression of hyaluronan synthase 2 and hyaluronan synthesis in culture models of equine articular chondrocytes // J. Vet. Sci. 2018. Vol. 19, No. 6. P. 735–743. doi: 10.4142/jvs.2018.19.6.735

[79]

Shi Y, Wang Y, Shao C, et al. COVID-19 infection: the perspectives on immune responses. Cell Death Differ. 2020;27(5):1451–4. doi: 10.1038/s41418-020-0530-3

[80]

Shi Y., Wang Y., Shao C., et al. COVID-19 infection: the perspectives on immune responses // Cell Death Differ. 2020. Vol. 27, No. 5. P. 1451–1454. doi: 10.1038/s41418-020-0530-3

[81]

Debuc B, Smadja DM. Is COVID-19 a New Hematologic Disease? Stem Cell Rev Rep. 2021;17(1):4–8. doi: 10.1007/s12015-020-09987-4

[82]

Debuc B., Smadja D.M. Is COVID-19 a New Hematologic Disease? // Stem Cell Rev. Rep. 2021. Vol. 17, No. 1. P. 4–8. doi: 10.1007/s12015-020-09987-4

[83]

Magro C, Mulvey JJ, 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;220:1–13. doi: 10.1016/j.trsl.2020.04.007

[84]

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. Vol. 220. P. 1–13. doi: 10.1016/j.trsl.2020.04.007

[85]

Lodigiani C, Iapichino G, Carenzo L, et al. Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy. Thromb Res. 2020;191:9–14. doi: 10.1016/j.thromres.2020.04.024

[86]

Lodigiani C., Iapichino G., Carenzo L., et al. Venous and arterial thromboembolic complications in COVID-19 patients admitted to an academic hospital in Milan, Italy // Thromb. Res. 2020. Vol. 191. P. 9–14. doi: 10.1016/j.thromres.2020.04.024

[87]

Renné T, Stavrou EX. Roles of Factor XII in Innate Immunity. Front Immunol. 2019;10:2011. doi: 10.3389/fimmu.2019.02011

[88]

Renné T., Stavrou E.X. Roles of Factor XII in Innate Immunity // Front. Immunol. 2019. Vol. 10. P. 2011. doi: 10.3389/fimmu.2019.02011

[89]

Göbel K, Eichler S, Wiendl H, et al. The Coagulation Factors Fibrinogen, Thrombin, and Factor XII in Inflammatory Disorders — A Systematic Review. Front Immunol. 2018;9:1731. doi: 10.3389/fimmu.2018.01731

[90]

Göbel K., Eichler S., Wiendl H., et al. The Coagulation Factors Fibrinogen, Thrombin, and Factor XII in Inflammatory Disorders — A Systematic Review // Front. Immunol. 2018. Vol. 9. P. 1731. doi: 10.3389/fimmu.2018.01731

[91]

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. 2022;10:1054–62. doi: 10.1016/s0140-6736(20)30566-3

[92]

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. Vol. 395, No. 10229. P. 1054–1062. doi: 10.1016/s0140-6736(20)30566-3

[93]

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;58(7):1116–20. doi: 10.1515/cclm-2020-0188

[94]

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. Vol. 58, No. 7. P. 1116–1120. doi: 10.1515/cclm-2020-0188

[95]

Rovina N, Akinosoglou K, Eugen–Olsen J, et al. Soluble urokinase plasminogen activator receptor (suPAR) as an early predictor of severe respiratory failure in patients with COVID-19 pneumonia. Crit Care. 2020;24(1):187. doi: 10.1186/s13054-020-02897-4

[96]

Rovina N., Akinosoglou K., Eugen–Olsen J., et al. Soluble urokinase plasminogen activator receptor (suPAR) as an early predictor of severe respiratory failure in patients with COVID-19 pneumonia // Crit. Care. 2020. Vol. 24, No. 1. P. 187. doi: 10.1186/s13054-020-02897-4

[97]

Overed–Sayer C, Rapley L, Mustelin T, et al. Are mast cells instrumental for fibrotic diseases? Front Pharmacol. 2014;4:174. doi: 10.3389/fphar.2013.00174

[98]

Overed–Sayer C., Rapley L., Mustelin T., et al. Are mast cells instrumental for fibrotic diseases? // Front. Pharmacol. 2014. Vol. 4. P. 174. doi: 10.3389/fphar.2013.00174

[99]

Budnevsky AV, Avdeev SN, Ovsyannikov ES, et al. The role of mast cells and their proteases in lung damage associated with COVID-19. Pulmonologiya. 2023;33(1):17–26. (In Russ). doi: 10.18093/0869-0189-2023-33-1-17-26

[100]

Будневский А.В., Авдеев С.Н., Овсянников Е.С., и др. Роль тучных клеток и их протеаз в поражении легких у пациентов с COVID-19 // Пульмонология. 2023. Т. 33, № 1. С. 17–26. doi: 10.18093/0869-0189-2023-33-1-17-26

[101]

Budnevsky AV, Avdeev SN, Kosanovic D, et al. Role of mast cells in the pathogenesis of severe lung damage in COVID-19 patients. Respir Res. 2022;23(1):371. doi: 10.1186/s12931-022-02284-3

[102]

Budnevsky A.V., Avdeev S.N., Kosanovic D., et al. Role of mast cells in the pathogenesis of severe lung damage in COVID-19 patients // Respir. Res. 2022. Vol. 23, No. 1. P. 371. doi: 10.1186/s12931022-02284-3

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