Cited by 19Renin-Angiotensin System StudiesCoagulation, Bradykinin, Polyphosphates, and AngioedemaEicosanoids and Hypertension Pharmacology

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Counter-regulatory renin-angiotensin system in hypertension: Review and update in the era of COVID-19 pandemic

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Chen, Hongyin, Peng, Jiangyun, Wang, Tengyao, Wen, Jielu, Chen, Sifan, Huang, Yu, Zhang, Yang·2023·Biochemical Pharmacology

DOI 10.1016/j.bcp.2022.115370PMC PMC9721294

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Abstract

Cardiovascular disease is the major cause of mortality and disability, with hypertension being the most prevalent risk factor. Excessive activation of the renin-angiotensin system (RAS) under pathological conditions, leading to vascular remodeling and inflammation, is closely related to cardiovascular dysfunction. The counter-regulatory axis of the RAS consists of angiotensin-converting enzyme 2 (ACE2), angiotensin (1-7), angiotensin (1-9), alamandine, proto-oncogene Mas receptor, angiotensin II type-2 receptor and Mas-related G protein-coupled receptor member D. Each of these components has been shown to counteract the effects of the overactivated RAS. In this review, we summarize the latest insights into the complexity and interplay of the counter-regulatory RAS axis in hypertension, highlight the pathophysiological functions of ACE2, a multifunctional molecule linking hypertension and COVID-19, and discuss the function and therapeutic potential of targeting this counter-regulatory RAS axis to prevent and treat hypertension in the context of the current COVID-19 pandemic.

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Time-Resolved Quantitative Phosphoproteomics: New Insights into Angiotensin-(1–7) Signaling Networks in Human Endothelial Cells
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Plasma levels of soluble ACE2are associated with sex, Metabolic Syndrome, and its biomarkers in a large cohort, pointing to a possible mechanism for increased severity in COVID-19
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Association of angiotensin-converting enzyme 2 gene A/G polymorphism and elevated blood pressure in Chinese patients with metabolic syndrome
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Deletion of angiotensin-converting enzyme 2 promotes the development of atherosclerosis and arterial neointima formation
Sahara, M., Ikutomi, M., Morita, T., Minami, Y., Nakajima, T., Hirata, Y., Nagai, R., & Sata, M. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvt245 · Cited by 74
Angiotensin-(1–7) infusion is associated with increased blood pressure and adverse cardiac remodelling in rats with subtotal nephrectomy
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Species-specific inhibitor sensitivity of angiotensin-converting enzyme 2 (ACE2) and its implication for ACE2 activity assays
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Ablation of angiotensin (1-7) receptor Mas in C57Bl/6 mice causes endothelial dysfunction
Rabelo, L. A., Xu, P., Todiraş, M., Sampaio, W. O., Buttgereit, J., Bäder, M., Santos, R. A. S., & Alenina, N. V. (2008) · Journal of the American Society of Hypertension · doi:10.1016/j.jash.2008.05.003 · Cited by 73
Angiotensin(1–7) potentiates bradykinin-induced vasodilatation in man
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A dramatic rise in serum ACE2 activity in a critically ill COVID-19 patient
Nagy, B., Fejes, Z., Szentkereszty, Z., Sütő, R., Várkonyi, I. Z., Ajzner, É., Kappelmayer, J., Papp, Z., Tóth, A., & Fagyas, M. (2020) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2020.11.184 · Cited by 73
Changes in Blood Pressure Outcomes Among Hypertensive Individuals During the COVID-19 Pandemic: A Time Series Analysis in Three US Healthcare Organizations
Gotanda, H., Liyanage-Don, N. A., Moran, A. E., Krousel-Wood, M. A., Green, J. B., Zhang, Y., & Nuckols, T. K. (2022) · Hypertension · doi:10.1161/hypertensionaha.122.19861 · Cited by 73
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Clinical phenotypes and outcomes associated with SARS-CoV-2 variant Omicron in critically ill French patients with COVID-19
de Prost, N., Audureau, É., Heming, N., Gault, E., Pham, T. O., Chaghouri, A., de Montmollin, N., Voiriot, G., Morand‐Joubert, L., Joseph, A., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33801-z · Cited by 70
Inhibition of Angiotensin-Converting Enzyme 2 Exacerbates Cardiac Hypertrophy and Fibrosis in Ren-2 Hypertensive Rats
Trask, A. J., Groban, L., Westwood, B. M., Varagić, J., Ganten, D., Gallagher, P. E., Chappell, M. C., & Ferrario, C. M. (2010) · American Journal of Hypertension · doi:10.1038/ajh.2010.51 · Cited by 69
Effects of Angiotensin-(1-7) on Forearm Circulation in Normotensive Subjects and Patients With Essential Hypertension
Sasaki, S., Higashi, Y., Nakagawa, K., Matsuura, H., Kajiyama, G., & Oshima, T. (2001) · Hypertension · doi:10.1161/01.hyp.38.1.90 · Cited by 69
Expression of an angiotensin-(1-7)-producing fusion protein in rats induced marked changes in regional vascular resistance
Santos, G. A. B., Sampaio, W. O., Reudelhuber, T. L., Bäder, M., Campagnole‐Santos, M. J., & Santos, R. A. S. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01245.2006 · Cited by 69
Angiotensin (1-7) and Alamandine: Similarities and differences
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Antihypertensive drugs are associated with reduced fatal outcomes and improved clinical characteristics in elderly COVID-19 patients
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Long term predictors of breathlessness, exercise intolerance, chronic fatigue and well-being in hospitalized patients with COVID-19: A cohort study with 4 months median follow-up
Tleyjeh, I. M., Saddik, B. A., Ramakrishnan, R. K., AlSwaidan, N., Alanazi, A. S., Alhazmi, D., Aloufi, A., AlSumait, F., Berbari, E. F., & Halwani, R. (2021) · Journal of Infection and Public Health · doi:10.1016/j.jiph.2021.11.016 · Cited by 69
Newly Discovered Components and Actions of the Renin–Angiotensin System
Carey, R. M. (2013) · Hypertension · doi:10.1161/hypertensionaha.113.01111 · Cited by 68
Impact of AT2-receptor stimulation on vascular biology, kidney function, and blood pressure
Steckelings, U. M., Danyel, L. A., Schmerler, P., et al. (2013) · Integrated Blood Pressure Control · doi:10.2147/ibpc.s34425 · Cited by 67
Plasma Angiotensin Peptide Profiling and ACE (Angiotensin-Converting Enzyme)-2 Activity in COVID-19 Patients Treated With Pharmacological Blockers of the Renin-Angiotensin System
Kintscher, U., Slagman, A. C., Domenig, O., Röhle, R., Konietschke, F., Poglitsch, M., & Möckel, M. (2020) · Hypertension · doi:10.1161/hypertensionaha.120.15841 · Cited by 67
Chronic infusion of angiotensin-(1-7) into the lateral ventricle of the brain attenuates hypertension in DOCA-salt rats
Guimarães, P. S., Santiago, N. M., Xavier, C. H., Velloso, E. P. P., Fontes, M. A. P., Santos, R. A. S., & Campagnole‐Santos, M. J. (2012) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00075.2012 · Cited by 66
Angiotensin‐(1–7) through AT2receptors mediates tyrosine hydroxylase degradation via the ubiquitin–proteasome pathway
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Effect of Angiotensin-(1-7) and Bradykinin in Patients With Heart Failure Treated With an ACE Inhibitor
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Angiotensin‐converting enzyme 2 antagonizes angiotensin II‐induced pressor response and NADPH oxidase activation in Wistar–Kyoto rats and spontaneously hypertensive rats
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Association Between Blood Pressure Control and Coronavirus Disease 2019 Outcomes in 45 418 Symptomatic Patients With Hypertension
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Comparative Impacts of ACE (Angiotensin-Converting Enzyme) Inhibitors Versus Angiotensin II Receptor Blockers on the Risk of COVID-19 Mortality
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Beta‐Adrenergic Blockers as a Potential Treatment for COVID‐19 Patients
Vasanthakumar, N. (2020) · BioEssays · doi:10.1002/bies.202000094 · Cited by 63
Angiotensin-(1–7) upregulates cardiac nitric oxide synthase in spontaneously hypertensive rats
Costa, M. A., Verrilli, M. A. L., Gómez, K. A., Nakagawa, P., Peña, C., Arranz, C. T., & Gironacci, M. M. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00850.2009 · Cited by 61
Over-expression of angiotensin II type 2 receptor (agtr2) reduces atherogenesis and modulates LOX-1, endothelial nitric oxide synthase and heme-oxygenase-1 expression
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Soluble ACE2 as a potential therapy for COVID-19
Krishnamurthy, S., Lockey, R. F., & Kolliputi, N. (2021) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00478.2020 · Cited by 61
Biological activities of angiotensin II-(1–6)-hexapeptide and angiotensin II-(1–7)-heptapeptide in man
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Adenoviral Delivery of Angiotensin-(1-7) or Angiotensin-(1-9) Inhibits Cardiomyocyte Hypertrophy via the Mas or Angiotensin Type 2 Receptor
Flores‐Muñoz, M., Godinho, B. M. D. C., Almalik, A., & Nicklin, S. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045564 · Cited by 60
Is the use of ACE inb/ARBs associated with higher in-hospital mortality in Covid-19 pneumonia patients?
Selçuk, M., Çınar, T., Keskin, M., Çiçek, V., Kılıç, Ş., Kenan, B., Doğan, S., Asal, S., Günay, N., Yıldırım, E., et al. (2020) · Clinical and Experimental Hypertension · doi:10.1080/10641963.2020.1783549 · Cited by 60
Correlation of angiotensin-converting enzyme 2 gene polymorphisms with stage 2 hypertension in Han Chinese
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Impairment of the angiotensin-converting enzyme 2–angiotensin-(1-7)-Mas axis contributes to the acceleration of two-kidney, one-clip Goldblatt hypertension
Bürgelová, M., Vaňourková, Z., Thumová, M., Dvořák, P., Opočenský, M., Kramer, H. J., Želízko, M., Malý, J., Bäder, M., & Červenka, L. (2009) · Journal of Hypertension · doi:10.1097/hjh.0b013e32832f0d06 · Cited by 59
Baroreflex Improvement in SHR After ACE Inhibition Involves Angiotensin-(1-7)
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Compound 21 Induces Vasorelaxation via an Endothelium- and Angiotensin II Type 2 Receptor-Independent Mechanism
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AT 2 Receptor Activation Prevents Sodium Retention and Reduces Blood Pressure in Angiotensin II–Dependent Hypertension
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Increased circulating levels of angiotensin-(1-7) in severely ill COVID-19 patients
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Blunted peripheral but not cerebral vasodilator function in young otherwise healthy adults with persistent symptoms following COVID-19
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Association of angiotensin-converting enzyme and angiotensin-converting enzyme-2 gene polymorphisms with essential hypertension in the population of Odisha, India
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Favorable Vascular Actions of Angiotensin-(1–7) in Human Obesity
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Imatinib and methazolamide ameliorate COVID-19-induced metabolic complications via elevating ACE2 enzymatic activity and inhibiting viral entry
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Angiotensin-(1–7) abrogates mitogen-stimulated proliferation of cardiac fibroblasts
McCollum, L. T., Gallagher, P. E., & Tallant, E. A. (2012) · Peptides · doi:10.1016/j.peptides.2012.01.020 · Cited by 56
Spironolactone may provide protection from SARS-CoV-2: Targeting androgens, angiotensin converting enzyme 2 (ACE2), and renin-angiotensin-aldosterone system (RAAS)
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Angiotensin-(1-7) Reduces Norepinephrine Release Through a Nitric Oxide Mechanism in Rat Hypothalamus
Gironacci, M. M., Vatta, M. S., Rodriguez–Fermepin, M., Fernández, B. E., & Peña, C. (2000) · Hypertension · doi:10.1161/01.hyp.35.6.1248 · Cited by 55
Functional rescue of a defective angiotensin II AT1 receptor mutant by the Mas protooncogene
dos Santos, E. L., Reis, R. I., Silva, R. G., et al. (2007) · Regulatory Peptides · doi:10.1016/j.regpep.2006.12.030 · Cited by 54
Angiotensin-(1–7) attenuates hypertension in exercise-trained renal hypertensive rats
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Association between circulating levels of ACE2-Ang-(1–7)-MAS axis and ACE2 gene polymorphisms in hypertensive patients
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Clinical grade ACE2 as a universal agent to block SARS‐CoV‐2 variants
Monteil, V., Eaton, B., Postnikova, E. N., Murphy, M. J., Braunsfeld, B., Crozier, I., Kricek, F., Niederhöfer, J., Schwarzböck, A., Breid, H., et al. (2022) · EMBO Molecular Medicine · doi:10.15252/emmm.202115230 · Cited by 54
The Effect of the Thioether‐Bridged, Stabilized Angiotensin‐(1–7) Analogue Cyclic Ang‐(1–7) on Cardiac Remodeling and Endothelial Function in Rats with Myocardial Infarction
Durik, M., van Veghel, R., Kuipers, A., Rink, R., Akanbi, M. H. J., Moll, G. N., Danser, A. H. J., & Roks, A. J. M. (2011) · International Journal of Hypertension · doi:10.1155/2012/536426 · Cited by 53
A Single β-Amino Acid Substitution to Angiotensin II Confers AT2Receptor Selectivity and Vascular Function
Jones, E. S., Borgo, M. P. D., Kirsch, J. F., Clayton, D., Bosnyak, S., Welungoda, I., Hausler, N. E., Unabia, S. E., Perlmutter, P., Thomas, W. G., et al. (2011) · Hypertension · doi:10.1161/hypertensionaha.110.164301 · Cited by 53
Reduction of angiotensin A and alamandine vasoactivity in the rabbit model of atherogenesis: differential effects of alamandine and A ng(1‐7)
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Systematic profiling of ACE2 expression in diverse physiological and pathological conditions for COVID‐19/SARS‐CoV‐2
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Angiotensin-(1–7) stimulates high atrial pacing-induced ANP secretion via Mas/PI3-kinase/Akt axis and Na+/H+exchanger
Shah, A., Gul, R., Yuan, K., et al. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00608.2009 · Cited by 49
Spironolactone: An Anti-androgenic and Anti-hypertensive Drug That May Provide Protection Against the Novel Coronavirus (SARS-CoV-2) Induced Acute Respiratory Distress Syndrome (ARDS) in COVID-19
Cadegiani, F., Wambier, C. G., & Goren, A. (2020) · Frontiers in Medicine · doi:10.3389/fmed.2020.00453 · Cited by 49
Engineered ACE2-Fc counters murine lethal SARS-CoV-2 infection through direct neutralization and Fc-effector activities
Chen, Y., Sun, L., Ullah, I., Beaudoin-Bussières, G., Anand, S. P., Hederman, A. P., Tolbert, W. D., Sherburn, R. T., Nguyen, D. N. P., Marchitto, L., et al. (2022) · Science Advances · doi:10.1126/sciadv.abn4188 · Cited by 49
Identification of Physiologically Active Substances as Novel Ligands for MRGPRD
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Gene Therapy With Angiotensin-(1-9) Preserves Left Ventricular Systolic Function After Myocardial Infarction
Fattah, C., Nather, K., McCarroll, C. S., Hortigon-Vinagre, M. P., Zamora, V., Flores‐Muñoz, M., McArthur, L., Zentilin, L., Giacca, M., Touyz, R. M., et al. (2016) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2016.09.946 · Cited by 47
Downregulation of Membrane-bound Angiotensin Converting Enzyme 2 (ACE2) Receptor has a Pivotal Role in COVID-19 Immunopathology
Vieira, C. C., Nery, L., Martins, L. D. B. U., Jabour, L. G. P. P., Dias, R. F., & Silva, A. C. S. E. (2020) · Current Drug Targets · doi:10.2174/1389450121666201020154033 · Cited by 46
Angiotensin-(1-9) reduces cardiovascular and renal inflammation in experimental renin-independent hypertension
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Alpha-1 adrenergic receptor antagonists to prevent hyperinflammation and death from lower respiratory tract infection
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Angiotensin-(1-7) Does Not Affect Vasodilator or TPA Responses to Bradykinin in Human Forearm
Wilsdorf, T., Gainer, J. V., Murphey, L. J., Vaughan, D. E., & Brown, N. J. (2001) · Hypertension · doi:10.1161/01.hyp.37.4.1136 · Cited by 44
A Place in Our Hearts for the Lowly Angiotensin 1-7 Peptide?
Reudelhuber, T. L. (2006) · Hypertension · doi:10.1161/01.hyp.0000209020.69734.73 · Cited by 44
Evidence for Mas-Mediated Bradykinin Potentiation by the Angiotensin-(1-7) Nonpeptide Mimic AVE 0991 in Normotensive Rats
Carvalho, M. B. L., Duarte, F. V., Faria-Silva, R., et al. (2007) · Hypertension · doi:10.1161/hypertensionaha.107.094987 · Cited by 44
Angiotensin-(1-7): Translational Avenues in Cardiovascular Control
Medina, D., & Arnold, A. C. (2019) · American Journal of Hypertension · doi:10.1093/ajh/hpz146 · Cited by 44
Alamandine attenuates angiotensin II-induced vascular fibrosis via inhibiting p38 MAPK pathway
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Emerging Role of Angiotensin Type 2 Receptor (AT2R)/Akt/NO Pathway in Vascular Smooth Muscle Cell in the Hyperthyroidism
Carrillo-Sepúlveda, M. A., Ceravolo, G. S., Fürstenau, C. R., Monteiro, P. D. S., Bruno-Fortes, Z., de Carvalho, M. H. C., Laurindo, F. R. M., Tostes, R. C., Webb, R. C., & Barreto‐Chaves, M. L. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061982 · Cited by 42
Increasing Angiotensin-(1–7) Levels in the Brain Attenuates Metabolic Syndrome–Related Risks in Fructose-Fed Rats
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Angiotensin Type-2 Receptors Influence the Activity of Vasopressin Neurons in the Paraventricular Nucleus of the Hypothalamus in Male Mice
de Kloet, A. D., Pitra, S., Wang, L. A., Hiller, H., Pioquinto, D. J., Smith, J. A., Sumners, C., Stern, J. E., & Krause, E. G. (2016) · Endocrinology · doi:10.1210/en.2016-1131 · Cited by 42
Alamandine reverses hyperhomocysteinemia‐induced vascular dysfunction via PKA ‐dependent mechanisms
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Gender differences in the attenuation of salt-induced hypertension by angiotensin (1-7)
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Altered regional blood flow distribution in Mas-deficient mice
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Blocking mineralocorticoid receptor with spironolactone may have a wide range of therapeutic actions in severe COVID-19 disease
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Associations between the Severity of the Post-Acute COVID-19 Syndrome and Echocardiographic Abnormalities in Previously Healthy Outpatients Following Infection with SARS-CoV-2
Tudoran, C., Tudoran, M., Pop, G. N., Giurgi-Oncu, C., Cut, T. G., Lăzureanu, V. E., Oancea, C. I., Pârv, F., Ciocârlie, T., & Bende, F. (2021) · Biology · doi:10.3390/biology10060469 · Cited by 41
Nebivolol reduces cardiac angiotensin II, associated oxidative stress and fibrosis but not arterial pressure in salt-loaded spontaneously hypertensive rats
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Alamandine attenuates arterial remodelling induced by transverse aortic constriction in mice
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Activation of angiotensin-(1–7)/Mas axis in the brain lowers blood pressure and attenuates cardiac remodeling in hypertensive transgenic (mRen2)27 rats
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G. Wirnsberger, V. Monteil, B. Eaton, E. Postnikova, M. Murphy, B. Braunsfeld, I. Crozier, F. Kricek, J. Niederhofer, A. Schwarzbock, H. Breid, A.S. Jimenez, A. Bugajska-Schretter, A. Dohnal, C. Ruf, R. Gugenberger, A. Hagelkruys, N. Montserrat, M.R. Holbrook, C. Oostenbrink, R.H. Shoemaker, A. Mirazimi, J.M. Penninger, Clinical grade ACE2 as a universal agent to block SARS-CoV-2 variants, bioRxiv (2021) 459744. · DOI

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Authors: Chen, H., Peng, J., Wang, T., Wen, J., Chen, S., Huang, Y., & Zhang, Y.
Affiliations: Sun Yat-sen University (CN)
Corresponding author: Zhang, Yang
ORCID: Chen, Hongyin
Peng, Jiangyun
Chen, Sifan
Zhang, Yang
Venue: Biochemical Pharmacology
Publisher: Elsevier BV
Published: 2023-02
Volume: 208
Pages: 115370
ISSN: 0006-2952 (ISSN-L)
DOI: 10.1016/j.bcp.2022.115370
PMC: PMC9721294
OpenAlex: W4310726093
Cited by: 19
References: 440
Citations by year: 2026: 3 · 2025: 5 · 2024: 5 · 2023: 6
FWCI: 0.81
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Biochemical Pharmacology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
CityU Scholars (submittedVersion, cc-by-nc-nd)
Funders: Basic and Applied Basic Research Foundation of Guangdong Province (2021B1515020005)
National Natural Science Foundation of China (82000462)
Research Grants Council, University Grants Committee (SRFS2021-4S04)
Topics: Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Renin-Angiotensin System Studies
Health Sciences › Medicine › Hematology › Coagulation, Bradykinin, Polyphosphates, and Angioedema
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Eicosanoids and Hypertension Pharmacology
Keywords: hypertension, angiotensin-converting enzyme 2, angiotensin-(1-7), angiotensin-(1-9), alamandine, Mas receptor, angiotensin II type 2 receptor, COVID-19 pandemic, vascular remodeling, cardiovascular inflammation, antihypertensive therapy
MeSH terms: Angiotensin-Converting Enzyme 2, COVID-19, Angiotensin I, Humans, Hypertension, Peptide Fragments, Renin-Angiotensin System, Receptors, G-Protein-Coupled, Pandemics

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Counter-regulatory renin-angiotensin system in hypertension: Review and update in the era of COVID-19 pandemic

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