PMC:7408073 / 27630-38007 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7408073","sourcedb":"PMC","sourceid":"7408073","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7408073","text":"4. COVID-19 Can Induce RAS-mediated Positive Feedback Loops at Different Levels\nIntriguingly, the binding affinity of ACE2 to SARS-CoV-2 binding domain has been reported to be either equal to or 10- to 20-fold higher than ACE2 binding to SARS-CoV [27,32]. The affinity of spike protein for ACE2 has been shown to correlate with the severity of disease [24]. Although SARS-CoV produces more severe respiratory symptoms than NL63-CoV does, both viral receptor binding domains bind to ACE2 with similar affinity [78], indicating that SARS development is not related to the strength of binding affinity and depends on other mechanisms. In contrast to SARS-CoV, NL63-CoV did not induce ADAM17/TACE-mediated both ACE2 shedding and TNF-α secretion [17], suggesting that increased cleavability of ACE2 receptor and possibly of S1-S2 boundary may be crucial for disease severity. Indeed, the spike glycoprotein of SARS-CoV-2 but not of SARS-CoV, contains a furin-like cleavage site at the S1-S2 boundary which indicates an increased cleavability [13]. Of note, TNF-α and IL-1β were shown to both be upregulated in SARS-CoV-2 [2] and induce viral-independent ACE2 shedding from epithelial airway cells [16]. Moreover, viral-independent ACE2 surface release from epithelial cells was not only inducible by cytokines (e.g., TNF-α and IL-1β) but also constitutively and spontaneously produced when ACE2 surface expression was upregulated [16], for example upon IL-1β stimulation [56]. This suggests that systemic release of proinflammatory cytokines such as TNF-α and IL-1β can mediate an increase of sACE2 and its systemic activity. Of note, activation of ADAM17/TACE metalloprotease was induced by SARS-CoV and necessary for efficient infection (and TNF-α secretion) [17]. Intriguingly, both SARS-CoV infection and concomitant TNF-α secretion were significantly attenuated not only by knock-down of ADAM17/TACE expression by siRNA but also by deletion of the ACE2 cytoplasmic tail which is responsible for ADAM17/TACE activation [17]. Altogether these observations suggest the possibility that SARS-CoV may induce a positive feedback loop leading to surface expression and shedding of both ACE2 and TNF-α. Indeed, upon spike protein binding to ACE2, downstream pathway activation can sustain positive feedback loops at different levels (Figure 2):(1) SARS-CoV can induce IL-1β and TNF-α systemic secretion that can mediate viral-independent surface membrane ACE2 upregulation and shedding. Of note, ACE2 shedding, on one hand, protects from viral infection but, on the other hand, increases circulating/systemic active sACE2, leading to its downstream pathway activation.\n(2) Hypoxia in combination or not with hypercapnia can upregulate the activity of both arms of the renin–angiotensin system by inducing renin, ACE and ACE2 synthesis, which can increase expression of Ang I, Ang II, Ang (1–7), Ang (1–9), Ang (1–5) and the inactive metabolite bradykinin (1–7), but also membrane bound ACE2, finally giving more chances to SARS-CoV-2 entry.\n(3) ACE2 can induce vasodilatative hypotensive effects by Ang II catabolism. Hypotension can induce again renin and ACE upregulation finally providing further Ang II, as a ACE2 substrate for further Ang (1–7) production.\n(4) Ang (1–7) antiproliferative and apoptotic effects, possibly in part through IL-10, may mediate eosinopaenia and lymphopaenia that, on one hand, reduce inflammatory responses but, on the other hand, impair immune system ability to counter virus infection, finally predisposing the organism to further infections. Ang (1–7) immunosuppressive activity, mediated or not by IL-10, may also support the reduced ability to generate an effective immunization to SARS-CoV-2 infection.\n(5) Ang (1–7)/MasR pathway can sustain ACE2 synthesis even in the presence of elevated concentrations of Ang II (such as in hypoxia), by inhibiting Ang II/AT1R-mediated down-modulation of ACE2 activity (see Figure 1).\n(6) Ang (1–7)/MasR pathway can produce cardiac dysfunction and lung alteration leading to systemic hypoxia, which, in turn, upregulates the activity of both arms of the RAS.\n(7) Although the ACE2 catalytic efficiency is 400-fold lower with Ang I than with Ang II [79], high concentration of circulating ACE2 may be able to produce significant increase of Ang (1–9) that, by binding AT2 receptors, can produce arteriolar microvascular thrombosis and local hypoxic conditions finally inducing local upregulation both arms of the RAS.\nFinally, ACE2-loaded SARS-CoV-2 virions and S1-ACE2 complexes may impair both sACE2 proteolytic degradation by blood proteases and its renal excretion, therefore blunting the removal of its systemic enzymatic activity and indicating that circulating viral particles are dangerous even when they are not able to entry into the cells (see Figure 2). On the one hand, ACE2 hypertranscription and consequent increase of membrane (m)ACE2 exposure induced by hypoxia/hypotension may facilitate SARS-CoV-2 entry and its lifecycle into mACE2 expressing cells. On the other hand, the release of ACE2 from the cell membranes and its subsequent activity in the bloodstream and in local (lung/cardiac) extracellular fluids are likely critical steps in contributing to systemic disease pathogenesis. Nevertheless, the same aetiological agent, SARS-CoV-2, can produce a variety of clinical syndromes, which involves several organs in relation to the subject’s predisposition. Although in the present work I have supposed that most of the COVID-19 symptoms might derive from Ang (1–7), Ang II and Ang (1–9) peptide upregulation, the involvement of B1 receptor pathway suppression mediated by ACE2 metabolisation of des-Arg(9)-bradykinin to inactive bradykinin (1–7) or other ACE2-downstream peptides such as apelins, casomorphins and dynorphins cannot be rule out.\nBased on the above observations, in order to block the RAS-induced positive feedback loops, different pharmacological targets can be hypothesized and pursued alone or in combination. They will be discussed in the next section and Box 3.\nBox 3 Possible targets of therapeutic intervention to inhibit the RAS-induced positive feedback loops.\nPharmacological inhibition of enzymes involved in both viral entry, such as TMPRSS2 and ADAM17, and the RAS function such as renin, ACE and ACE2 enzymatic activity or their downstream pathways are expected to stop positive feedback loops and their detrimental consequences.\nInhibition of TMPRSS2 and ADAM17 metalloprotease activity. Inhibition of the serine protease TMPRSS2 (necessary for SARS-CoV-2 entry) by a clinically proven protease inhibitor has been recently suggested by Hoffmann and colleagues [13] and inhibition of ADAM17 enzymatic activity has been already proposed about ten years ago by Haga and colleagues [20]. Indeed, inhibition of ADAM17-mediated ACE2 shedding is expected to increase membrane ACE2 expression and therefore the probability of viral entry; nevertheless, in the early phases of the disease, inhibition of ACE2 circulating activity might be sufficient to inhibit the systemic RAS pathway upregulation and the development of severe forms of COVID-19. It is, in fact, possible that maintenance/recovery of correct organismal immune responses, by preventing ACE2-mediated immune suppression, in concert with cellular adaptive immune responses mediated by apolipoprotein B mRNA editing enzyme, catalytic polypeptide-like (APOBEC) systems [80] may anyway work to induce both an effective “immunization” and the viral eradication.\nInhibition of both arms of the RAS. Among the inhibitors of the RAS pathways, different strategy can be pursued involving either ACE2 enzymatic activity or its upstream renin and ACE enzymatic activity or its downstream MasR pathway. Inhibition of ACE2, ACE and renin enzymatic activities and their involvement in SARS-CoVs will be extensively discussed in the next sections, instead a brief description of MasR inhibition will be presented in the present Box.\nMas receptor pathway inhibition and side effects of using Mas receptor inhibitors. A779 also known as D-Ala7-Ang-(1–7) and D-Pro7-Ang-(1–7) are two distinct MasR antagonists able to prevent Ang-(1–7)-mediated downstream activation in human cells. The existence of several MasR subtypes has been suggested based on the differential capacity of the two MasR blockers to fully inhibit some biological actions of Ang-(1–7) [and perhaps of Ang (1–5), see Figure 1] [39,70]; therefore, differently from ACE2 enzymatic inhibitors, MasR antagonists should be administered in combinations, in order to inhibit ACE2 hyperactivity. In human aortic smooth muscle cells, they have been shown to restore NADPH oxidase/NF-kB/iNOS inflammatory pathway induced by Ang II when it is inhibited by Ang (1–7) co-administration [81]. In mice studies a MasR blocker (A779) administered alone was not associated with systolic blood pressure alterations, and the hypotensive effect produced by rACE2 co-infused with Ang II was unaffected by A779 co-administration, indicating that the hypotensive activity of rACE2 mainly depended on Ang II degradation rather than on increase of Ang (1–7) and MasR activation [82]. In another report, spontaneously hypertensive rats (SHRs) that received A-779 alone for a total of two weeks did not significantly alter basal blood pressure and urinary protein excretion [83]. Moreover, in SHRs treated with A-779 in combination with Ang II, renal injury and interstitial infiltration of macrophages and T cells were surprisingly reduced as compared with SHRs treated with Ang II alone, suggesting a safe use of A-779 drug in in vivo infusions [83]. Another report showed that infusion of A-779 alone for 7 days did not produce a significant effect neither on blood pressure nor on heart rate in SHRs [84]. In a rat model of cardiac arrhythmia, administration of A-779 alone did not cause any significant alteration in the number of arrhythmic events, confirming that A-779 can be safely delivered to rodents in vivo. [85]. Although MasR antagonists has been shown to be safe in acute and chronic in vivo studies either with mice or rats, there are no data on administration in humans and the existence of different MasR subtypes in the vasculature require combinations of MasR antagonists to inhibit an excess of ACE2 activity as for example may occur in COVID-19 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