Role of endothelial dysfunction in the severity of COVID‑19 infection (Review)
- Authors:
- Tanya Kadiyska
- Ivan Tourtourikov
- Kristiyan Dabchev
- Radostina Cherneva
- Nikolay Stoynev
- Radka Hadjiolova
- Vanyo Mitev
- Demetrios A. Spandidos
- Maria Adamaki
- Vassilis Zoumpourlis
-
Affiliations: Department of Physiology and Pathophysiology, Medical University, 1413 Sofia, Bulgaria, Genetic Medico‑Diagnostic Laboratory Genica, 1612 Sofia, Bulgaria, University Hospital for Respiratory Diseases St. Sophia, 1413 Sofia, Bulgaria, Laboratory of Clinical Virology, Medical School, University of Crete, Heraklion 71003, Greece, Biomedical Applications Unit, Institute Of Chemical Biology, National Hellenic Research Foundation, 11635 Athens, Greece - Published online on: October 3, 2022 https://doi.org/10.3892/mmr.2022.12867
- Article Number: 351
-
Copyright: © Kadiyska et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Yang X, Yu Y, Xu J, Shu H, Xia J, Liu H, Wu Y, Zhang L, Yu Z, Fang M, et al: Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: A single-centered, retrospective, observational study. Lancet Respir Med. 8:475–481. 2020. View Article : Google Scholar : PubMed/NCBI | |
Zoumpourlis V, Goulielmaki M, Rizos E, Baliou S and Spandidos DA: [Comment] The COVID-19 pandemic as a scientific and social challenge in the 21st century. Mol Med Rep. 22:3035–3048. 2020.PubMed/NCBI | |
Magro C, Mulvey JJ, Berlin D, Nuovo G, Salvatore S, Harp J, Baxter-Stoltzfus A and Laurence J: Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: A report of five cases. Transl Res. 220:1–13. 2020. View Article : Google Scholar : PubMed/NCBI | |
Amraei R and Rahimi N: COVID-19, renin-angiotensin system and endothelial dysfunction. Cells. 9:16522020. View Article : Google Scholar : PubMed/NCBI | |
Libby P and Lüscher T: COVID-19 is, in the end, an endothelial disease. Eur Heart J. 41:3038–3044. 2020. View Article : Google Scholar : PubMed/NCBI | |
Wan Y, Shang J, Graham R, Baric RS and Li F: Receptor recognition by the novel coronavirus from Wuhan: An analysis based on decade-long structural studies of SARS coronavirus. J Virol. 94:e00127–e00120. 2020. View Article : Google Scholar : PubMed/NCBI | |
Brassington K, Selemidis S, Bozinovski S and Vlahos R: Chronic obstructive pulmonary disease and atherosclerosis: Common mechanisms and novel therapeutics. Clin Sci (Lond). 136:405–423. 2022. View Article : Google Scholar : PubMed/NCBI | |
Somlyo AV: New roads leading to Ca2+ sensitization. Circ Res. 91:83–84. 2002. View Article : Google Scholar : PubMed/NCBI | |
Kostov K: The causal relationship between endothelin-1 and hypertension: Focusing on endothelial dysfunction, arterial stiffness, vascular remodeling, and blood pressure regulation. Life (Basel). 11:9862021.PubMed/NCBI | |
Kumar A, Choudhury M, Batra SD, Sikri K and Gupta A: In vivo assessment of a single adenine mutation in 5′UTR of endothelin-1 gene in paediatric cases with severe pulmonary hypertension: An observational study. BMC Res Notes. 14:1942021. View Article : Google Scholar : PubMed/NCBI | |
Hasegawa H, Hiki K, Sawamura T, Aoyama T, Okamoto Y, Miwa S, Shimohama S, Kimura J and Masaki T: Purification of a novel endothelin-converting enzyme specific for big endothelin-3. FEBS Lett. 428:304–308. 1998. View Article : Google Scholar : PubMed/NCBI | |
D'Orléans-Juste P, Plante M, Honoré JC, Carrier E and Labonté J: Synthesis and degradation of endothelin-1. Can J Physiol Pharmacol. 81:503–510. 2003. View Article : Google Scholar : PubMed/NCBI | |
Yoshida T, Matsuura K, Goya S, Ma D, Shimada K, Kitpipatkun P, Namiki R, Uemura A, Suzuki K and Tanaka R: Metformin prevents the development of monocrotaline-induced pulmonary hypertension by decreasing serum levels of big endothelin-1. Exp Ther Med. 20:1492020. View Article : Google Scholar : PubMed/NCBI | |
Wagner OF, Christ G, Wojta J, Vierhapper H, Parzer S, Nowotny PJ, Schneider B, Waldhäusl W and Binder BR: Polar secretion of endothelin-1 by cultured endothelial cells. J Biol Chem. 267:16066–16068. 1992. View Article : Google Scholar : PubMed/NCBI | |
Watts SW: Endothelin receptors: What's new and what do we need to know? Am J Physiol Regul Integr Comp Physiol. 298:R254–R260. 2010. View Article : Google Scholar : PubMed/NCBI | |
Wang L, Wang L and Yan F: Understanding the molecular mechanism of endothelin ETA receptor selecting isopeptides endothelin-1 and −3. Biophys J. 121:2490–2502. 2022. View Article : Google Scholar : PubMed/NCBI | |
Ergul A: Endothelin-1 and endothelin receptor antagonists as potential cardiovascular therapeutic agents. Pharmacotherapy. 22:54–65. 2002. View Article : Google Scholar : PubMed/NCBI | |
Ruetten H and Thiemermann C: Endothelin-1 stimulates the biosynthesis of tumour necrosis factor in macrophages: ET-receptors, signal transduction and inhibition by dexamethasone. J Physiol Pharmacol. 48:675–688. 1997.PubMed/NCBI | |
Stencel MG, VerMeer M, Giles J and Tran QK: Endothelial regulation of calmodulin expression and eNOS-calmodulin interaction in vascular smooth muscle. Mol Cell Biochem. 477:1489–1498. 2022. View Article : Google Scholar : PubMed/NCBI | |
Barinda AJ, Arozal W, Sandhiutami NMD, Louisa M, Arfian N, Sandora N and Yusuf M: Curcumin prevents epithelial-to mesenchymal transition-mediated ovarian cancer progression through NRF2/ETBR/ET-1 axis and preserves mitochondria biogenesis in kidney after cisplatin administration. Adv Pharm Bull. 12:128–141. 2022.PubMed/NCBI | |
Nabeh OA, Matter LM, Khattab MA and Menshawey E: The possible implication of endothelin in the pathology of COVID-19-induced pulmonary hypertension. Pulm Pharmacol Ther. 71:1020822021. View Article : Google Scholar : PubMed/NCBI | |
Chow JH, Mazzeffi MA and McCurdy MT: Angiotensin II for the treatment of COVID-19-related vasodilatory shock. Anesth Analg. 131:102–105. 2020. View Article : Google Scholar : PubMed/NCBI | |
Deshotels MR, Xia H, Sriramula S, Lazartigues E and Filipeanu CM: Angiotensin II mediates angiotensin converting enzyme type 2 internalization and degradation through an angiotensin II type I receptor-dependent mechanism. Hypertension. 64:1368–1375. 2014. View Article : Google Scholar : PubMed/NCBI | |
Rahman MM, Hasan M and Ahmed A: Potential detrimental role of soluble ACE2 in severe COVID-19 comorbid patients. Rev Med Virol. 31:e22132021. View Article : Google Scholar : PubMed/NCBI | |
Henry BM, Vikse J, Benoit S, Favaloro EJ and Lippi G: Hyperinflammation and derangement of renin-angiotensin-aldosterone system in COVID-19: A novel hypothesis for clinically suspected hypercoagulopathy and microvascular immunothrombosis. Clin Chim Acta. 507:167–173. 2020. View Article : Google Scholar : PubMed/NCBI | |
Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, Schiergens TS, Herrler G, Wu NH, Nitsche A, et al: SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 181:271–280.e8. 2020. View Article : Google Scholar : PubMed/NCBI | |
Konrath EL, Berger M, Lopes da Rosa R and Beys-da-Silva WO: Acmella oleracea is a medicinal plant that decreases chymase activity, oxidative stress, and inflammation: Possible role in the adjuvant treatment of COVID-19. J Med Food. 24:1243–1244. 2021.PubMed/NCBI | |
Gómez J, Albaiceta GM, García-Clemente M, López-Larrea C, Amado-Rodríguez L, Lopez-Alonso I, Hermida T, Enriquez AI, Herrero P, Melón S, et al: Angiotensin-converting enzymes (ACE, ACE2) gene variants and COVID-19 outcome. Gene. 762:1451022020. View Article : Google Scholar : PubMed/NCBI | |
Carà GA, Pasin L, Alborino E, Zarbock A, Bellomo R and Landoni G: Angiotensin II - A brief review and role in severe SARS-COV-2 sepsis. J Cardiothorac Vasc Anesth [Internet]. 2022 Jul 22;[cited 2022 Sep 16]; Available from:. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9304073/ View Article : Google Scholar : PubMed/NCBI | |
Ravarotto V, Bertoldi G, Stefanelli LF, Nalesso F and Calò LA: Gitelman's and Bartter's Syndromes: From genetics to the molecular basis of hypertension and more. Kidney Blood Press Res. 20:1–9. 2022.PubMed/NCBI | |
Kuba K, Imai Y, Rao S, Jiang C and Penninger JM: Lessons from SARS: Control of acute lung failure by the SARS receptor ACE2. J Mol Med (Berl). 84:814–820. 2006. View Article : Google Scholar : PubMed/NCBI | |
Steardo L, Steardo L and Verkhratsky A: Psychiatric face of COVID-19. Transl Psychiatry. 10:2612020. View Article : Google Scholar : PubMed/NCBI | |
Giannopoulou I, Galinaki S, Kollintza E, Adamaki M, Kympouropoulos S, Alevyzakis E, Tsamakis K, Tsangaris I, Spandidos DA, Siafakas N, et al: COVID-19 and post-traumatic stress disorder: The perfect ‘storm’ for mental health (Review). Exp Ther Med. 22:11622021. View Article : Google Scholar : PubMed/NCBI | |
Liu Y, Yang Y, Zhang C, Huang F, Wang F, Yuan J, Wang Z, Li J, Li J, Feng C, et al: Clinical and biochemical indexes from 2019-nCoV infected patients linked to viral loads and lung injury. Sci China Life Sci. 63:364–374. 2020. View Article : Google Scholar : PubMed/NCBI | |
Seo JW, Kim DY, Yun N and Kim DM: Coronavirus disease 2019-associated coagulopathy. Microorganisms. 10:15562022. View Article : Google Scholar : PubMed/NCBI | |
Kwaan HC and Lindholm PF: The central role of fibrinolytic response in COVID-19-a hematologist's perspective. Int J Mol Sci. 22:12832021. View Article : Google Scholar : PubMed/NCBI | |
Ferrario CM, Jessup J, Chappell MC, Averill DB, Brosnihan KB, Tallant EA, Diz DI and Gallagher PE: Effect of angiotensin-converting enzyme inhibition and angiotensin II receptor blockers on cardiac angiotensin-converting enzyme 2. Circulation. 111:2605–2610. 2005. View Article : Google Scholar : PubMed/NCBI | |
Shyh GI, Nawarskas JJ and Cheng-Lai A: Angiotensin-converting enzyme inhibitors and angiotensin receptor blockers in patients with coronavirus disease 2019: Friend or foe? Cardiol Rev. 28:213–216. 2020. View Article : Google Scholar : PubMed/NCBI | |
Batlle D, Wysocki J and Satchell K: Soluble angiotensin-converting enzyme 2: A potential approach for coronavirus infection therapy? Clin Sci (Lond). 134:543–545. 2020. View Article : Google Scholar : PubMed/NCBI | |
Zhang H, Penninger JM, Li Y, Zhong N and Slutsky AS: Angiotensin-converting enzyme 2 (ACE2) as a SARS-CoV-2 receptor: Molecular mechanisms and potential therapeutic target. Intensive Care Med. 46:586–590. 2020. View Article : Google Scholar : PubMed/NCBI | |
Zhou MS, Schulman IH and Raij L: Nitric oxide, angiotensin II, and hypertension. Semin Nephrol. 24:366–378. 2004. View Article : Google Scholar : PubMed/NCBI | |
Raij L: Nitric oxide, salt sensitivity, and cardiorenal injury in hypertension. Semin Nephrol. 19:296–303. 1999.PubMed/NCBI | |
Li H, Brodsky S, Basco M, Romanov V, De Angelis DA and Goligorsky MS: Nitric oxide attenuates signal transduction: Possible role in dissociating caveolin-1 scaffold. Circ Res. 88:229–236. 2001. View Article : Google Scholar : PubMed/NCBI | |
Massberg S, Sausbier M, Klatt P, Bauer M, Pfeifer A, Siess W, Fässler R, Ruth P, Krombach F and Hofmann F: Increased adhesion and aggregation of platelets lacking cyclic guanosine 3′,5′-monophosphate kinase I. J Exp Med. 189:1255–1264. 1999. View Article : Google Scholar : PubMed/NCBI | |
Takemoto M, Egashira K, Usui M, Numaguchi K, Tomita H, Tsutsui H, Shimokawa H, Sueishi K and Takeshita A: Important role of tissue angiotensin-converting enzyme activity in the pathogenesis of coronary vascular and myocardial structural changes induced by long-term blockade of nitric oxide synthesis in rats. J Clin Invest. 99:278–287. 1997. View Article : Google Scholar : PubMed/NCBI | |
Katoh M, Egashira K, Usui M, Ichiki T, Tomita H, Shimokawa H, Rakugi H and Takeshita A: Cardiac angiotensin II receptors are upregulated by long-term inhibition of nitric oxide synthesis in rats. Circ Res. 83:743–751. 1998. View Article : Google Scholar : PubMed/NCBI | |
Hati S and Bhattacharyya S: Impact of thiol-disulfide balance on the binding of covid-19 spike protein with angiotensin-converting enzyme 2 receptor. ACS Omega. 5:16292–16298. 2020. View Article : Google Scholar : PubMed/NCBI | |
Sasser JM, Pollock JS and Pollock DM: Renal endothelin in chronic angiotensin II hypertension. Am J Physiol Regul Integr Comp Physiol. 283:R243–R248. 2002. View Article : Google Scholar : PubMed/NCBI | |
Ortiz MC, Sanabria E, Manriquez MC, Romero JC and Juncos LA: Role of endothelin and isoprostanes in slow pressor responses to angiotensin II. Hypertension. 37((2 Pt 2)): 505–510. 2001. View Article : Google Scholar : PubMed/NCBI | |
Boulanger CM and Lüscher TF: Differential effect of cyclic GMP on the release of endothelin-1 from cultured endothelial cells and intact porcine aorta. J Cardiovasc Pharmacol. 17 (Suppl 7):S264–S266. 1991. View Article : Google Scholar : PubMed/NCBI | |
Montiel V, Lobysheva I, Gérard L, Vermeersch M, Perez-Morga D, Castelein T, Mesland JB, Hantson P, Collienne C, Gruson D, et al: Oxidative stress-induced endothelial dysfunction and decreased vascular nitric oxide in COVID-19 patients. EBioMedicine. 77:1038932022. View Article : Google Scholar : PubMed/NCBI | |
Mehta PK and Griendling KK: Angiotensin II cell signaling: Physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol. 292:C82–C97. 2007. View Article : Google Scholar : PubMed/NCBI | |
Vanhoutte PM: Endothelium and control of vascular function. State of the Art lecture. Hypertension. 13:658–667. 1989. View Article : Google Scholar : PubMed/NCBI | |
Philogene MC, Johnson T, Vaught AJ, Zakaria S and Fedarko N: Antibodies against angiotensin II type 1 and endothelin A receptors: Relevance and pathogenicity. Hum Immunol. 80:561–567. 2019. View Article : Google Scholar : PubMed/NCBI | |
Lukitsch I, Kehr J, Chaykovska L, Wallukat G, Nieminen-Kelhä M, Batuman V, Dragun D and Gollasch M: Renal ischemia and transplantation predispose to vascular constriction mediated by angiotensin II type 1 receptor-activating antibodies. Transplantation. 94:8–13. 2012. View Article : Google Scholar : PubMed/NCBI | |
Zhang S, Zheng R, Yang L, Zhang X, Zuo L, Yang X, Bai K, Song L, Tian J, Yang J and Liu H: Angiotensin type 1 receptor autoantibody from preeclamptic patients induces human fetoplacental vasoconstriction. J Cell Physiol. 228:142–148. 2013. View Article : Google Scholar : PubMed/NCBI | |
Papola F, Biancofiore V, Angeletti C, Grimaldi A, Carucci AC, Cofini V, Necozione S, Rosciano A, Marinangeli F and Cervelli C: Anti-AT1R autoantibodies and prediction of the severity of Covid-19. Human Immunol. 83:130–133. 2022. View Article : Google Scholar : PubMed/NCBI | |
Ohe H, Uchida Y, Yoshizawa A, Hirao H, Taniguchi M, Maruya E, Yurugi K, Hishida R, Maekawa T, Uemoto S and Terasaki PI: Association of anti-human leukocyte antigen and anti-angiotensin II type 1 receptor antibodies with liver allograft fibrosis after immunosuppression withdrawal. Transplantation. 98:1105–1111. 2014. View Article : Google Scholar : PubMed/NCBI | |
O'Leary JG, Demetris AJ, Philippe A, Freeman R, Cai J, Heidecke H, Smith C, Hart B, Jennings LW, Catar R, et al: Non-HLA antibodies impact on C4d staining, stellate cell activation and fibrosis in liver allografts. Transplantation. 101:2399–2409. 2017. View Article : Google Scholar : PubMed/NCBI | |
Budding K, van de Graaf EA, Hoefnagel T, Kwakkel-van Erp JM, van Kessel DA, Dragun D, Hack CE and Otten HG: Anti-ETAR and anti-AT1R autoantibodies are elevated in patients with endstage cystic fibrosis. J Cyst Fibros. 14:42–45. 2015. View Article : Google Scholar : PubMed/NCBI | |
Cabral-Marques O, Halpert G, Schimke LF, Ostrinski Y, Vojdani A, Baiocchi GC, Freire PP, Filgueiras IS, Zyskind I, Lattin MT, et al: Autoantibodies targeting GPCRs and RAS-related molecules associate with COVID-19 severity. Nat Commun. 13:12202022. View Article : Google Scholar : PubMed/NCBI | |
Abadir PM, Jain A, Powell LJ, Xue QL, Tian J, Hamilton RG, Bennett DA, Finucane T, Walston JD and Fedarko NS: Discovery and validation of agonistic angiotensin receptor autoantibodies as biomarkers of adverse outcomes. Circulation. 135:449–459. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhang Q and Reed EF: The importance of non-HLA antibodies in transplantation. Nat Rev Nephrol. 12:484–495. 2016. View Article : Google Scholar : PubMed/NCBI | |
Saavedra JM: Angiotensin receptor blockers and COVID-19. Pharmacol Res. 156:1048322020. View Article : Google Scholar : PubMed/NCBI | |
Chung MK, Karnik S, Saef J, Bergmann C, Barnard J, Lederman MM, Tilton J, Cheng F, Harding CV, Young JB, et al: SARS-CoV-2 and ACE2: The biology and clinical data settling the ARB and ACEI controversy. EBioMedicine. 58:1029072020. View Article : Google Scholar : PubMed/NCBI | |
Jia H: Pulmonary angiotensin-converting enzyme 2 (ACE2) and inflammatory lung disease. Shock. 46:239–248. 2016. View Article : Google Scholar : PubMed/NCBI | |
Gurwitz D: Angiotensin receptor blockers as tentative SARS-CoV-2 therapeutics. Drug Dev Res. 81:537–540. 2020. View Article : Google Scholar : PubMed/NCBI | |
Fedson DS: Treating the host response to emerging virus diseases: Lessons learned from sepsis, pneumonia, influenza and Ebola. Ann Transl Med. 4:4212016. View Article : Google Scholar : PubMed/NCBI | |
Fang L, Karakiulakis G and Roth M: Are patients with hypertension and diabetes mellitus at increased risk for COVID-19 infection? Lancet Respir Med. 8:e212020. View Article : Google Scholar : PubMed/NCBI | |
Diaz JH: Hypothesis: Angiotensin-converting enzyme inhibitors and angiotensin receptor blockers may increase the risk of severe COVID-19. J Travel Med. 27:taaa0412020. View Article : Google Scholar : PubMed/NCBI | |
Matsuzawa Y, Kimura K, Ogawa H and Tamura K: Impact of renin-angiotensin-aldosterone system inhibitors on COVID-19. Hypertens Res. 45:1147–1153. 2022. View Article : Google Scholar : PubMed/NCBI | |
Martel J, Ko YF, Young JD and Ojcius DM: Could nasal nitric oxide help to mitigate the severity of COVID-19? Microbes Infect. 22:168–171. 2020. View Article : Google Scholar : PubMed/NCBI | |
Lundberg JO, Weitzberg E and Gladwin MT: The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov. 7:156–167. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lundberg JO, Carlström M and Weitzberg E: Metabolic effects of dietary nitrate in health and disease. Cell Metabolism. 28:9–22. 2018. View Article : Google Scholar : PubMed/NCBI | |
Chen L, Liu P, Gao H, Sun B, Chao D, Wang F, Zhu Y, Hedenstierna G and Wang CG: Inhalation of nitric oxide in the treatment of severe acute respiratory syndrome: A rescue trial in Beijing. Clin Infect Dis. 39:1531–1535. 2004. View Article : Google Scholar : PubMed/NCBI | |
Lundberg JO, Farkas-Szallasi T, Weitzberg E, Rinder J, Lidholm J, Anggåard A, Hökfelt T, Lundberg JM and Alving K: High nitric oxide production in human paranasal sinuses. Nat Med. 1:370–373. 1995. View Article : Google Scholar : PubMed/NCBI | |
Runer T, Cervin E, Lindberg S and Uddman R: Nitric oxide is a regulator of mucociliary activity in the upper respiratory tract. Otolaryngol Head Neck Surg. 119:278–287. 1998. View Article : Google Scholar : PubMed/NCBI | |
Nagaki M, Shimura S, Irokawa T, Sasaki T and Shirato K: Nitric oxide regulation of glycoconjugate secretion from feline and human airways in vitro. Respir Physiol. 102:89–95. 1995. View Article : Google Scholar : PubMed/NCBI | |
Xu W, Zheng S, Dweik RA and Erzurum SC: Role of epithelial nitric oxide in airway viral infection. Free Radic Biol Med. 41:19–28. 2006. View Article : Google Scholar : PubMed/NCBI | |
Keyaerts E, Vijgen L, Chen L, Maes P, Hedenstierna G and Van Ranst M: Inhibition of SARS-coronavirus infection in vitro by S-nitroso-N-acetylpenicillamine, a nitric oxide donor compound. Int J Infect Dis. 8:223–226. 2004. View Article : Google Scholar : PubMed/NCBI | |
Åkerström S, Gunalan V, Keng CT, Tan YJ and Mirazimi A: Dual effect of nitric oxide on SARS-CoV replication: Viral RNA production and palmitoylation of the S protein are affected. Virology. 395:1–9. 2009. View Article : Google Scholar : PubMed/NCBI |