Binding of SARS-CoV-2 and angiotensin-converting enzyme 2: clinical implications
Identifieur interne : 000344 ( Pmc/Corpus ); précédent : 000343; suivant : 000345Binding of SARS-CoV-2 and angiotensin-converting enzyme 2: clinical implications
Auteurs : Eleanor Murray ; Maciej Tomaszewski ; Tomasz J. GuzikSource :
- Cardiovascular Research [ 0008-6363 ] ; 2020.
Url:
DOI: 10.1093/cvr/cvaa096
PubMed: 32301968
PubMed Central: 7184453
Links to Exploration step
PMC:7184453Le document en format XML
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<series><title level="j">Cardiovascular Research</title>
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</TEI>
<pmc article-type="editorial"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Cardiovasc Res</journal-id>
<journal-id journal-id-type="iso-abbrev">Cardiovasc. Res</journal-id>
<journal-id journal-id-type="publisher-id">cardiovascres</journal-id>
<journal-title-group><journal-title>Cardiovascular Research</journal-title>
</journal-title-group>
<issn pub-type="ppub">0008-6363</issn>
<issn pub-type="epub">1755-3245</issn>
<publisher><publisher-name>Oxford University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">32301968</article-id>
<article-id pub-id-type="pmc">7184453</article-id>
<article-id pub-id-type="doi">10.1093/cvr/cvaa096</article-id>
<article-id pub-id-type="publisher-id">cvaa096</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Editors’ Corner</subject>
</subj-group>
</article-categories>
<title-group><article-title>Binding of SARS-CoV-2 and angiotensin-converting enzyme 2: clinical implications</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-4837-4840</contrib-id>
<name><surname>Murray</surname>
<given-names>Eleanor</given-names>
</name>
<xref ref-type="corresp" rid="cvaa096-cor1"></xref>
<xref ref-type="corresp" rid="cvaa096-cor1"></xref>
<pmc-comment>Eleanor.Murray@glasgow.ac.uk </pmc-comment>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0001-8215-6567</contrib-id>
<name><surname>Tomaszewski</surname>
<given-names>Maciej</given-names>
</name>
<xref ref-type="aff" rid="cvaa086-aff2">c2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Guzik</surname>
<given-names>Tomasz J</given-names>
</name>
<xref ref-type="aff" rid="cvaa086-aff1">c1</xref>
</contrib>
</contrib-group>
<aff id="cvaa086-aff1"><label>c1</label>
<institution>Institute of Cardiovascular and Medical Sciences, BHF Glasgow Cardiovascular Research Centre, 126 University Place, University of Glasgow</institution>
, Glasgow G12 8TA,<country country="GB">UK</country>
</aff>
<aff id="cvaa086-aff2"><label>c2</label>
<institution>Division of Cardiovascular Sciences, University of Manchester</institution>
, Manchester,<country country="GB">UK</country>
</aff>
<author-notes><corresp id="cvaa096-cor1"> Corresponding author. Email: <email>Eleanor.Murray@glasgow.ac.uk</email>
</corresp>
</author-notes>
<pub-date pub-type="epub" iso-8601-date="2020-04-17"><day>17</day>
<month>4</month>
<year>2020</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>17</day>
<month>4</month>
<year>2020</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<elocation-id>cvaa096</elocation-id>
<permissions><copyright-statement>Published on behalf of the European Society of Cardiology. All rights reserved. © The Author(s) 2020. For permissions, please email: journals.permissions@oup.com.</copyright-statement>
<copyright-year>2020</copyright-year>
<license license-type="publisher-standard" xlink:href="https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model"><license-p>This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (<ext-link ext-link-type="uri" xlink:href="https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model">https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model</ext-link>
)</license-p>
</license>
<license><license-p>This article is made available via the PMC Open Access Subset for unrestricted re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the COVID-19 pandemic or until permissions are revoked in writing. Upon expiration of these permissions, PMC is granted a perpetual license to make this article available via PMC and Europe PMC, consistent with existing copyright protections.</license-p>
</license>
</permissions>
<self-uri xlink:href="cvaa096.pdf"></self-uri>
<kwd-group><kwd>ACE inhibitor</kwd>
<kwd>SARS-CoV-2</kwd>
<kwd>COVID-19</kwd>
<kwd>Hypertension</kwd>
</kwd-group>
<counts><page-count count="3"></page-count>
</counts>
<custom-meta-group><custom-meta><meta-name>article-lifecycle</meta-name>
<meta-value>PAP</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
<body><p>The emergence and consequent impact of COVID-19 has led to clinicians and academics looking for evidence, with clinical controversies to parallel socio-economical and political ones.</p>
<p>A key clinical controversy has been whether the use of angiotensin-converting enzyme (ACE) inhibitors and angiotensin receptor blockers (ARBs) might be detrimental or beneficial in COVID-19. This is a widely prescribed class of drugs with a strong evidence base in hypertension and cardiovascular risk reduction. Individuals have proposed stopping such drugs due to concern over up-regulation of the ACE2 receptor acting as the SARS-CoV-2 entry point; others paradoxically suggest prescribing this class of drugs to counteract a dysregulated angiotensin–aldosterone system. We therefore explore the links between the renin–angiotensin–aldosterone system (RAAS) and the ACE2 receptor specifically; expanding on the observation that hypertension is prevalent among those diagnosed with COVID-19.</p>
<p><bold>SARS-Cov2 virus:</bold>
the pathogen responsible for COVID-19. The SARS-Cov2 virus achieves cell entry through an S (spike) high-affinity protein binding to the catalytic domain of the ACE2 receptor;<xref rid="cvaa096-B1" ref-type="bibr"><sup>1</sup>
</xref>
pneumocytes are particularly vulnerable.</p>
<p><bold>ACE2:</bold>
the RAAS is well characterized in hypertension, heart failure, and beyond. ACE converts angiotensin I (Ang I) to Ang II, predominantly in the lungs. The effects of Ang II are dependent on receptor binding: AT1 receptor binding stimulates the classical effects of Ang II, ranging from increased oxidative stress, through to vasoconstriction; in principle, AT2 receptor regulates opposing effects. ACE2 is an enzyme attached to cell membranes in the lungs, endothelium, and heart, as well as the kidneys. Its main pharmacological effect is to lower blood pressure by catalysing the cleavage of Ang I to Ang 1-9 and of Ang II to Ang 1-7 (vasodilatory, anti-inflammatory activity). ACE2 has additional affinity for other vasoactive substrates, including apelin-13 and bradykinin. Soluble ACE2 has also been described, cleaved from the cell surface but with a preserved catalytic activity. A sex difference exists, with men displaying higher ACE2 levels.<xref rid="cvaa096-B2" ref-type="bibr"><sup>2</sup>
</xref>
<sup>,</sup>
<xref rid="cvaa096-B3" ref-type="bibr"><sup>3</sup>
</xref>
Circulating levels are low in good health, but rise in heart failure, atrial fibrillation, and kidney disease:
<list list-type="bullet"><list-item><p>In 79 patients with obstructive coronary artery disease (59% on an ACE inhibitor/ARB), the 10-year MACE (major adverse cardiovascular events) rate was higher in those with higher plasma ACE2 activity at baseline (<italic>P</italic>
= 0.035); ACE2 remained an independent predictor in multivariable analysis [hazard ratio (HR) 2.4, 95% confidence interval (CI) 1.2–4.7].<xref rid="cvaa096-B2" ref-type="bibr"><sup>2</sup>
</xref>
</p>
</list-item>
<list-item><p>Hospitalization due to heart failure in the same cohort was associated with higher ACE2 with a HR of 1.0 (95% CI 1.4–11.5, <italic>P</italic>
= 0.009).<xref rid="cvaa096-B2" ref-type="bibr"><sup>2</sup>
</xref>
</p>
</list-item>
<list-item><p>Post-operative ACE2 levels following orthopaedic surgery in 187 patients were significantly greater in patients with a subsequent in-hospital cardiac event (25.3 vs. 39.5 pmol/mL/min, <italic>P</italic>
= 0.012), though this did not remain significant in multivariate analysis.<xref rid="cvaa096-B4" ref-type="bibr"><sup>4</sup>
</xref>
</p>
</list-item>
<list-item><p>In 103 participants, increased ACE2 activity was associated with hypertension, impaired left ventricular systolic function, and older age; atrial fibrillation (<italic>P</italic>
= 0.04) and vascular disease (<italic>P</italic>
< 0.01) were independent predictors of plasma ACE2 activity.<xref rid="cvaa096-B3" ref-type="bibr"><sup>3</sup>
</xref>
ACE inhibitor/ARB use was reported in 28% of controls, 36% of paroxysmal AF, and 55% of persistent AF participants.</p>
</list-item>
</list>
</p>
<p>Differing rates of ACE inhibitor/ARB use between groups is important considering the aforementioned effect on membrane-bound ACE2, and a largely unknown effect on soluble ACE2.</p>
<p><bold>Is ACE2 up-regulated by ACE inhibitor/ARB use, and does this facilitate COVID-19 cell entry and increase severity of infection?:</bold>
The concept of the up-regulation of ACE2 arises from animal studies; with rats demonstrating reduced plasma Ang II, increased ACE2 mRNA, and higher plasma Ang 1-7 in response to lisinopril or enalapril, and the latter two effects also found with losartan.<xref rid="cvaa096-B5" ref-type="bibr"><sup>5</sup>
</xref>
However, conflicting evidence can also be found, with ramipril failing to increase ACE2 despite a similar duration of ACE inhibition.<xref rid="cvaa096-B6" ref-type="bibr"><sup>6</sup>
</xref>
Mechanistically, Ang II induces lysosomal internalization of ACE2, and thus reduces tissue expression; losartan prevents this through interaction and stabilization of ACE2 with AT1 receptors.<xref rid="cvaa096-B7" ref-type="bibr"><sup>7</sup>
</xref>
This leads to the converse argument, that ARBs could reduce SARS-CoV-2 cell entry by reducing availability of binding sites and reducing internalization of ACE2. However, a virus only needs one receptor to infect a cell, and the effect of ARB on Ang II breakdown to Ang 1-7 was not studied.</p>
<p>There has not been any good evidence of ACE2 up-regulation associated with these drugs in humans<xref rid="cvaa096-B2" ref-type="bibr"><sup>2</sup>
</xref>
<sup>,</sup>
<xref rid="cvaa096-B3" ref-type="bibr"><sup>3</sup>
</xref>
and, despite 61% sequence similarity between ACE1 and ACE2, ACE inhibitors do not effect ACE2 receptors. It is notable that animal work is predominantly based on tissue expression, and human work on soluble/circulating ACE2, when the relationship between these remains unclear. Furthermore, mice and rats are not intermediate hosts of SARS-CoV, raising questions about the generalizability of the data to humans.</p>
<p><bold>Loss of regulation of Ang II:</bold>
Considering whether there is evidence of RAAS dysfunction in COVID-19, hypokalaemia has been a reported complication not clearly explained by gastrointestinal loss, and correlating with disease severity, though the study omitted to report medication use.<xref rid="cvaa096-B8" ref-type="bibr"><sup>8</sup>
</xref>
Renal potassium losses (as seen in hyperaldosteronism) may be a consequence of elevated Ang II due to SARS-CoV S protein binding to and reducing ACE2 expression, thus removing the homeostatic mechanism limiting Ang II (<xref ref-type="fig" rid="cvaa096-F1"><italic>Figure 1</italic>
</xref>
).<xref rid="cvaa096-B1" ref-type="bibr"><sup>1</sup>
</xref>
ACE2 knockout mice support the protective effect of regulating Ang II through ACE2 metabolism to Ang 1-7 as, in a viral influenza model, pathology and survival were inferior in knockout animals.<xref rid="cvaa096-B9" ref-type="bibr"><sup>9</sup>
</xref>
Use of losartan to block the AT1 receptor improved lung injury in this mouse model.<xref rid="cvaa096-B9" ref-type="bibr"><sup>9</sup>
</xref>
</p>
<fig id="cvaa096-F1" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>(<italic>A</italic>
) ACE2 contributes to regulation of Ang II, catalysing its conversion to Ang 1-7. (<italic>B</italic>
) SARS-CoV-2 competes with Ang II for ACE2 for cell entry; it may impair regulation of the RAAS. (<italic>C</italic>
) ARB stabilizes ACE2 with AT1 and may reduce availability for SARS-CoV-2 entry whilst reducing aldosterone excess.</p>
</caption>
<graphic xlink:href="cvaa096f1"></graphic>
</fig>
<p><bold>Clinical outcomes with ACE inhibitors/ARBs:</bold>
A study of a cohort of 539 viral pneumonia patients found that ACE inhibitor use was associated with an increased risk of death or need for intubation [odds ratio (OR) 3; 95% CI 1.3–7.0], but continued use during the admission was possibly beneficial (OR 0.25; 95% CI 0.1–0.6).<xref rid="cvaa096-B10" ref-type="bibr"><sup>10</sup>
</xref>
However, demographic and clinical features broken down by ACE inhibitor use/continuation were omitted, despite association of ACE inhibitor use with cardiovascular disease; and discontinuation of the drug was more likely to occur in deteriorating patients.</p>
<p><bold>Long-term outcomes:</bold>
Outcomes of the disease remain largely unknown. Following SARS, lipid metabolism may remain altered even at 12 years follow-up in comparison with both healthy controls (age and body mass index matched) and those with bacterial pneumonia; though the authors hypothesize that this may relate to use of methylprednisolone rather than the virus itself.<xref rid="cvaa096-B15" ref-type="bibr"><sup>15</sup>
</xref>
Compared with healthy controls, higher rates of cardiovascular and glucose metabolism abnormalities were reported, as was further hospitalization.</p>
<sec sec-type="conclusion"><title>Conclusion</title>
<p>In relation to the above evidence, the American College of Physicians, Canadian Cardiovascular Society, European Society of Cardiology Council on Hypertension, European Society of Hypertension, Hypertension Canada, International Society of Hypertension and The Renal Association (UK) have all supported continued ACE inhibitor/ARB use, unless there is an alternative clinical reason to suspend them in the face of COVID-19. The morbidity and mortality risk of stopping such drugs is significant, particularly given the myocardial damage that may occur in COVID-19.<graphic xlink:href="cvaa096f2.jpg" mimetype="image" position="float" orientation="portrait"></graphic>
</p>
<p><bold>Conflict of interest:</bold>
none declared.</p>
</sec>
</body>
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<sec><title>Authors</title>
<fig id="cvaa096-F2" orientation="portrait" position="float"><graphic xlink:href="cvaa096f2"></graphic>
</fig>
<p><bold>Biography:</bold>
Dr Eleanor Charlotte Murray is current Clinical Research Fellow at the University of Glasgow, funded by the European Research Council. Her clinical training is in General Medicine and Nephrology. Current research involves studying the immune system and vascular function in hypertension.</p>
<fig id="cvaa096-F3" orientation="portrait" position="float"><graphic xlink:href="cvaa096f3"></graphic>
</fig>
<p><bold>Biography:</bold>
Maciej Tomaszewski is a Professor of Cardiovascular Medicine at the Division of Cardiovascular Sciences, Faculty of Biology, Medicine and Health, University of Manchester. He also acts as an Honorary Consultant Physician at the Manchester University NHS Foundation Trust. He is a member of the Scientific Council of the International Society of Hypertension and the President-Elect of the Society (2018-2020). He has been a member of Editorial Boards for leading journals in the field of hypertension and he currently chairs the Board of Management of Journal Hypertension.</p>
<fig id="cvaa096-F4" orientation="portrait" position="float"><graphic xlink:href="cvaa096f4"></graphic>
</fig>
<p><bold>Biography:</bold>
Professor Tomasz J. Guzik is the current Editor-in-Chief of Cardiovascular Research. He is the Regius Professor of Physiology and Cardiovascular Pathobiology and an Honorary Consultant Physician in Cardiology at the University of Glasgow. He also serves as a Professor of Medicine at Jagiellonian University Collegium Medicum in Krakow, Poland. Notable recognitions include the honorary Bernard and Joan Marshall Prize in Research Excellence from the BSCR and the prestigious Corcoran Award Lecture at the American Heart Association. He is a recipient of European Research Council Grant. Professor Guzik’ research focusses on vascular biology, hypertension, and clinical immunology.</p>
</sec>
</back>
</pmc>
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