PMC:7408073 / 38099-53763 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":"5.1. ACE2 (and ACE) Hyperactivity: Is It a Matter of (Free) Zinc?\nACE2 and ACE are two zinc metalloprotease that function differently despite their similarities. ACE2 is a monocarboxypeptidase (cleaves a C-terminal single amino acid from its substrate), whereas ACE is a dipeptidylpeptidase (releases a C-terminal dipeptide from its substrate) [86,87]. ACE2 has a substrate preference for hydrolysis between proline and a hydrophobic or basic C-terminal residue [79,86,87] and acts not only on the RAS and bradykinin peptides but also on the C-terminus of the apelin, casomorphin dynorphin peptides [79], possibly inhibiting Apelin-13 hypotensive action [44]. It is expressed in the heart, kidneys, liver, colon, small intestine, lung, brain and testes [39,44,45,46,76,77,87]. Among the tissues expressing ACE2 there are cardiomyocytes, endothelium, alveolar type II cells, ciliated airway cells, vascular smooth muscle cells and testicular Leydig cells [14,39,44,45,46,76,77,87,88,89]. ACE2 is present on the apical surface of epithelial cells of renal tubules, lung alveoli and vascular endothelia, in these last cells the production of Ang (1–7) induces autocrine activation of MasR axis leading to NOS-mediated vasodilation and consequently hypotension [14,44,45,46,86,87,88,89].\nACE2, as well as ACE, is a zinc metalloprotease that can be inhibited by zinc chelating EDTA and activated by high concentrations of chloride or fluoride anions and zinc cation [79,90]. Indeed, both enzymes have chloride- and zinc-binding sites [90]. It is conceivable that these sites are responsible for the anion and zinc activation effect in both homologous enzymes [90]. However, the presence of chloride ions increases Ang I cleavage by ACE and ACE2 (increasing both Ang II and Ang (1–9)) and decreases Ang II cleavage by ACE2, suggesting that chloride induces specific ACE2 conformational changes in its active site (see [44]). To this regard, in plasma samples of COVID–19 patients, chloride range is usually normal or slightly higher (99.6–107.0 mmol/L) than normal values (96.–106.0 mmol/L) [5]. Unfortunately, I was not able to find plasma zinc concentrations in COVID-19 patients. Zinc is involved in several cellular activities and its systemic concentration is tightly regulated by several factors. Of interest, the major transporter/reservoir of zinc in plasma is albumin [91], a protein that was detected at significantly low concentrations in SARS-CoV-2 as well as severe adult respiratory distress syndrome (ARDS, a COVID-19-like disease) (usually \u003c 3.5 g/dL, normal range 3.5–5.4) and inflammatory bowel disease (IBD, a disease with increased ACE2 activity) [6,8,66,92] Since most of zinc in plasma is sequestered by albumin, the total amount of plasma zinc mostly depends on albumin concentration and even small changes in albumin’s capacity for zinc binding may have significant consequences. To this regard, reduced concentrations of plasma albumin is believed to increase plasma levels of free zinc, while reducing the total plasma zinc concentrations [91], a condition that was observed in ARDS patients [93,94]. Indeed, albumin can potentially deplete free bioavailable forms of zinc; vice versa, hypoalbuminaemia may increase free zinc levels in plasma. Therefore, some ARDS patients with low levels of both total zinc and albumin might have rather higher than lower free zinc levels [93]. The free zinc concentration, which describes the fraction of zinc that is loosely bound and easily exchangeable, represents the highly bioavailable (and toxic) part of plasma zinc but it is not clinically detected. To that end, zinc/albumin ratio might be a surrogate marker of free zinc levels. Indeed, only recently it was described a fluorescence-based method for determining the free zinc concentration in human serum samples [95]. With this method it was shown that free zinc concentration in sera from females was significantly lower than in males [95]. Moreover, free zinc concentration did correlate neither with total serum concentrations of zinc (or other metal ions such as iron) nor with age [95]. Notably, increased plasma zinc bioavailability consequent to reduced albumin levels induces zinc import into cells and likely increases the cellular functions associated to cellular zinc concentrations such as ACE and ACE2. Indeed, enzymatic activity of both enzymes seems significantly upregulated in ARDS patients as detected by analysis of Ang peptide concentrations in plasma (see Box later in ARDS topic). In addition, serum albumin levels in COVID-19 were usually very low (in severe forms is usually \u003c 3.1 g/dL) [6,8], raising the possibility of a negative correlation between albumin concentration in plasma and increase of the RAS activity. In line with these hypotheses, both asthmatic/allergic disease patients and chronic kidney disease patients without a history of cardiovascular disease, which are protected from developing COVID-19, showed a significant decrease in both circulating zinc levels and ACE2 activity as compared to normal values [96,97,98,99]. Interestingly, chronic renal disease patients with low zinc levels had normal concentrations of albumin but higher urinary zinc excretion than healthy controls [97], suggesting that low ACE2 activity in chronic renal diseases (and protection from SARS) might derive from a higher free Zn2+ renal excretion. A similar mechanism mediated by a reduction of extracellular levels of free Zn2+ might be hypothesised for asthma patients, as well [98]. Unfortunately, I could not find information on plasma albumin concentrations for asthma patients; nevertheless, we might suppose that in these patients the albumin concentration is in normal range.\nIntriguingly, inhalation exposure to ZnCl2/ZnO/hexachloroethane (the main ingredients in smoke bombs) induces both elevated plasma levels of zinc and ARDS with clinical pictures that strongly resemble those of COVID-19 [100,101,102]. Since both ACE2 and ACE enzymes are activated by high concentrations of chloride and zinc ions [79,90], it is possible to hypothesise an activation of both arms of the RAS in ARDS induced by smoke bombs as well as in COVID-19 patients. In addition, metal fume fever, a flu-like syndrome caused by inhalation of welding fumes (mainly containing zinc) can be a predictor for the development of respiratory symptoms and welders have an increased pneumonia and cardiovascular risk [103,104]. In this regard, metal fume fever has been shown to produce fever, fatigue, muscle ache, cough, dyspnea, and an increase of several cytokines including IL-1β, IL-6, IL-8 and TNF-α [103], symptoms and cytokines that have already been described for COVID-19 patients [2,8,9]. Notably, TNF-α was upregulated early while IL-6 and IL-8 increased later, suggesting a subsequent involvement of these latter cytokines in response to inhalation of welding fumes [103]. Moreover, elevated levels of zinc have been shown not only to stimulate pro-inflammatory cytokine secretion by monocytes, but also inhibit T cell functions (see [102]). Zinc supplementation that has also been proposed for COVID-19 treatment [105,106,107], is able to suppress allogeneic immune response (see [102]) and incubation of blood cells with welding fume particles resulted in a considerable increase not only of pro-inflammatory cytokines (including IL-1β, IL-6, IL-8, TNF-α) but also the tolerogenic cytokine IL-10 [104]. Similarly, in pulmonary arterial hypertension (PAH) as well as SARS-CoV, both arms of the inflammatory system (namely IL-1β, IL-2, IL-4, IL-6, IL-8, IL-10, IL-12 and TNF-α) have been shown to be upregulated [108,109,110], suggesting a common systemic pathway of activation in welding syndrome, ARDS, PAH and SARS-CoV infections. Finally, the correlations between zinc exposure (metal fume) and cytokine storm [103,104] suggests a possible link between free zinc increase and these type of diseases. More information on systemic zinc homeostasis and multiorgan effects of elevated levels of extracellular free zinc (such as in subjects inhaling ZnCl2 smoke) is available in Box 4.\nBox 4 Systemic zinc homeostasis and multiorgan effects of elevated levels of extracellular free zinc.\nZinc absorption occurs throughout the gastrointestinal tract into enterocytes by zinc transporters of the Zrt- and Irt-like protein (ZIP) family that take up Zn2+, but also Cu2+ and Fe2+ ions, both of which can inhibit zinc absorption [111]. The bioavailability of zinc is affected by several factors among them the amount of zinc in food, its chemical form (from very low availability, e.g., zinc oxide, to comparatively high, e.g., zinc chloride salt) and its binding to other (intestinal absorbed or non-absorbed) food components [111]. For example, phytates (components present in foods like rice, cereals and corn) and folic acid can form insoluble complexes with zinc that decrease zinc absorption and increase fecal zinc excretion [111]. On the other hand, Zn2+ can form complexes with most natural amino acids (AA) that for example can come from digested proteins; each Zn2+ can be coordinated with the amine groups and carboxylate anions of two AAs (a molar ratio of 1:2). Interestingly, in an in vitro model, the formulation of either ZnCl2 salt or Zn-AA complexes were absorbed by enterocytes and zinc was released on the opposite side of the enterocyte membrane, thus mimicking the intestinal absorption and release into the blood stream [111]. It is therefore conceivable that zinc chelates of AA, as well as zinc salts, may participate in bioavailability and uptake of zinc. The uptake of zinc-AA complexes by AA transporters of human enterocytes suggests that B0AT1 neutral AA transporter associated with ACE2 [28] might also be involved in zinc-AA uptake (a similar mechanism might be supposable for insulin biosynthesis/secretion in pancreatic β cells [91]). Indeed, a recycling of zinc-AAs, possibly supplied by membrane bound ACE2 monocarboxypeptidase cleavage, for ACE2 synthesis could be also hypothesised.\nPlasma zinc concentration is mainly regulated through a balance between intestinal absorption and renal excretion involving specific mechanisms sensitive to both dietary zinc availability and its cellular utilization. The majority of Zn2+ in blood binds to serum albumin, which represents the major zinc transporter/reservoir protein in plasma. On the other hand, labile-bound pool of Zn2+ labile complexes (e.g., of AA) and free Zn2+ are the biologically available forms of zinc for cellular internalization and/or enzymatic activities (0.1–1% of the total zinc in blood plasma under normal conditions). Free Zn2+ is subsequently accumulated by endothelial cells and zinc uptake and release by endothelial cells is the crucial step for redistribution of Zn2+ from plasma to tissues [91].\nZinc is considered a relatively nontoxic metal; however, several data report that excessive free extracellular zinc is toxic and induce apoptosis in different cell types [91,102]. Plasma excess of free Zn2+ is uptaken by ZIP transporters on the cell surface of each cells in contact with plasma (including immune cells, endothelial cells, neurons and cardiomyocytes), leading to increase of intracellular zinc that can modulate zinc associated cellular functions in both physiological and pathological conditions. Indeed, zinc is an important mediator/messenger involved in several cellular activities and the shift of zinc from plasma to cells may be significant for both normal physiological processes including energy metabolism, blood coagulation, and zinc signalling, and a range of disease states, including neurodegenerative and cardiovascular diseases, metabolic syndrome, inflammation, endothelial stress, diabetes and thrombosis [91]. For example, excess zinc intake has been shown to contribute to both amyloid beta-peptide plaque formation in Alzheimer’s disease and cardiac dysfunction, indicating that free zinc ion may be much more toxic than thought [91]. It has been reported that Alzheimer and other neurodegenerative disease patients show elevated levels not only of Zn2+ but also of other divalent metals such as Fe2+ and Cu2+ [112], suggesting a possible link between the increase metal ions and saturation of ZIP transporters. On the other hand, increased plasma ferritin levels (such as in COVID-19 [2,3,6]) might reduce free Fe2+ and its “competition” with Zn2+ for ZIP transporters, finally increasing cellular zinc uptake and functions. To this regard, EDTA metal chelator has been shown to protect from neural cell death and it was tested in neurodegenerative diseases [102]. Of interest, plasma albumin acts as a transport protein for both metal ions such as zinc and hydrophobic molecules such as free fatty acid (FFA) to allow their systemic distribution. Indeed, albumin is well beyond a mere carrier of metal ions and hydrophobic molecules, and by binding of these different molecules mediates their crosstalk and bioavailability [91]. To this regard, one particularly intriguing allosteric link exists between FFA and zinc binding to albumin [91]. When FFAs with ten or more carbon atoms bind to albumin causes the release of Zn2+, suggesting a possible link between dyslipidemia and toxic effects mediated by consequent increase of free zinc in plasma. For example, endothelial stress and activation and pro-inflammatory action of FFAs may be mediated by their effects on free zinc release from albumin and its consequent efflux from plasma. Different studies have suggested a role of albumin to inhibit interaction of free Zn2+ with amyloid beta-peptides and combat plaque formation in Alzheimer’s disease [91]. Zn2+ has also been shown to promote clot stability by binding to fibrinogen and inhibiting heparin activity [91]. An evidence that has suggested a possible positive correlation between increased levels of FFAs and thrombotic risk [91]. In addition, physiological conditions associated with elevated plasma FFAs, such as physical exercise, can also produce an increased plasma level of free zinc and its downstream physiological events (e.g., activation of the RAS). On the other hand, reduced concentrations of plasma albumin (such as IBD, ARDS and COVID-19) will induce elevated plasma levels of both free FFAs and bioavailable zinc. Intriguingly, ARDS is induced after inhalation exposure to ZnCl2/ZnO/hexachloroethane, the main ingredients in smoke bombs used for crowd dispersal [100,101,102]. To this regard, soldiers that breathed smoke-bomb fumes have been shown to quickly or slowly develope ARDS [100,101]. Interestingly, a patient who had the highest level of serum zinc rapidly developed ARDS that leads to death from multiorgan failure (including respiratory and hepatic failure) [100]. Instead, a slow progressive clinical course was associated with a significant increase of plasma zinc concentration that negatively correlated with pulmonary and liver function [100], finally leading to death for severe respiratory failure three to five weeks after inhalation [100,101]. At autopsy diffuse microvascular obliteration and marked endothelial cell injury was apparent [101]. Widespread occlusion of the pulmonary arteries may contribute to the development of acute pulmonary hypertension and extensive interstitial and intra-alveolar fibrosis was also observed [101]. Other soldiers wearing gas masks, immediately developed severe coughing and dyspnea, and slowly improved their lung function (only twelve months after exposure their lung function tests were nearly normal) [101]. All clinical conditions that strongly resemble those described in COVID-19 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