PMC:7352545 / 69053-80835 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7352545","sourcedb":"PMC","sourceid":"7352545","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7352545","text":"7. Pharmacology of Glycan-Related Anti-SARS-CoV-2 Agents\nThe emerging CoV-pandemic requires therapeutic agents to block the recognition, binding, replication, amplification and propagation of the CoV in humans. Protease inhibitors, RNA synthase inhibitors and S2 inhibitors are potential targets, and several agents are currently being evaluated. Efficient therapeutic drugs are the most reliable option for patients. The first attachment step of the viral amplification cycle is initiated on the respiratory cell surfaces, driven by the viral S protein. This is a potential therapeutic target. Soon after the SARS-CoV-2 outbreak initiated, the CoV S glycoprotein was demonstrated to recognize ACE2 as a binding receptor on human cells. Human TMPRSS2 enzyme influences the CoV S glycoprotein activation, to facilitate virus infection. ACE2 binding and TMPRSS2 activation facilitate the CoVs to attach to human host cells. Mouse, nonhuman primate and human cells have been analyzed using single-cell RNA new generation sequencing (NGS). For example, for human infection, CoVs can enter nasal goblet secretory cells, because these cells express the proteins required for SARS-CoV-2 infection. In the lungs, the proteins are stored in the alveoli like air sacs of type II pneumocytes. In the intestine, the two proteins are expressed in entero-epithelial cells. ACE2 gene expression correlates with the IFN-related genes [137]. ACE2 helps lung cells to tolerate cellular damage. Therefore, CoVs may evolutionally take advantage of the defense mechanisms of host cells, hijacking such host-borne proteins.\nIn SARS-CoV-2, the ACE2 receptor is an attachment, entry and infection receptor into the cell, when the S glycoprotein is cleaved by a specific serine protease. SARS-CoV-2 infection is regulated by glycosylated SARS-CoV-2 viral particles and glycosylated ACE2 in the lung epithelial cells. RBD of the CoV S glycoprotein recognizes ACE2 [82]. Amino acid residues 442, 472, 479, 480 and 487 located on the receptor-binding motif (RBM) of the S glycoprotein RBD recognize human ACE2 [138]. Trimeric viral S glycoprotein is glycosylated and cleaved by a protease, furin, into two subunits, S1 and S2. Subunit S1 is further cleaved into the SA and SB domains and the SB domain recognizes human ACE2. The N-glycosylated S2 subunit is involved in virus-ACE2 complex formation [139]. Therefore, the glycosylated ACE2 receptor is a key molecule for virus binding and fusion.\nPlasma sera prepared from infected patients is an alternative medication. The WHO has suggested this trial since the 2014 Ebola epidemic and 2015 MERS-CoV outbreak. In addition, Mab therapy is another option. For example, LCA50 Mab mimics produced by modification of plasma antibodies isolated from MERS-CoV patients was valuable [140]. Low molecular molecules are being examined for anti-virus activities from alkaloids, glycan derivatives and terpenoids. Recently, anti-CoV drugs are being approached using molecular modeling, docking and simulation methods. Computation-assisted drugs via molecular modeling and docking toward drug targets are applied as anti-viral compounds against CoVs. They target human ACE2, PLpro (PDB: 3e9s), the CoV main proteinase (PDB: 6Y84), 3-chymotrypsin-like (3C-like protease; 3CLpro), RdRp, helicase, N7 methyltransferase, human DDP4, RBD, protease cathepsin L, type II TM Ser protease or TMPRSS2. CoV 3CLpro (PDB: 6WX4) and the PLpro cleave the polyproteins to assemble virus proteins. For newborn RNA genomes, RdRp is used as a replicase for the complementary RNA strand synthesis, which uses the virus RNA template.\n\n7.1. N-Glycosylation Inhibition by Chloroquine (CLQ) and Hydroxychloroquine (CLQ-OH)\nCLQ and CLQ-OH are under investigation worldwide to treat COVID-19 (Figure 10). CLQ and its derivative CLQ-OH block CoV replication, amplification and spread in in vitro culture via inhibition of ACE2 receptor glycosylation. In HCoVs, interaction of the S glycoprotein with gangliosides initially occur as the first entry step during the replication cycle of the virus. CLQ and CLQ-OH have been alternative drugs for RA and several autoimmune diseases for 70 years, although they are anti-malaria prophylaxis drugs. CLQ-OH is an aminoquinoline with less toxicity than CLQ. CLQ-OH bears an N-hydroxyethyl side chain, which increases its solubility compared to CLQ [141]. CLQ-OH modulates activated immune cells via downregulation of TLR signaling and IL-6 production [142]. Clinical trials are also under consideration for the efficacy and safety of these drugs. Regarding the action mechanism(s), CLQ and CLQ-OH-mediated inhibition of ACE2 terminal glycosylation was considered. In in vitro Vero E6 cells, CLQ significantly inhibits SARS-CoV spread by interfering with ACE2 function, acting at the entry and post-entry steps of SARS-CoV-2 replication and infection. The binding affinity of ACE2 to S glycoprotein is simulated to be lowered by treatment with CLQ-OH or CLQ. CLQ may modify the binding affinity between ACE2 and S glycoprotein by alterations in ACE2 glycosylation or modification. CLQ-OH (EC50 0.72 μM) and CLQ (EC50, 5.47 μM) inhibit SARS-CoV-2 [143].\nUsing computer simulation techniques, CLQ and CLQ-OH have been suggested to recognize the enzymatic active site of the UDP-GlcNAc 2-epimerase, known as an essential enzyme in SA biosynthesis [144], blocking the sialylation of host cells. The mechanism underlying the glycosylation inhibition may support the antiviral properties of CLQ and CLQ-OH through interactions of CLQ or CLQ-OH with NDP-saccharide mutases or glycosyltransferases [145]. CLQ was reported to inhibit quinone reductase 2 [146], known as a catalytic mimetic or structural neighbor of UDP-GlcNAc 2-epimerases [147,148]. If CLQ or CLQ-OH inhibits SA synthesis, the inhibitory properties may support the antiviral activity of CLQ or CLQ-OH against SARS-CoVs because the SARS-CoV receptor ACE2 contains SA species. In fact, CLQ exhibits in vitro anti-SARS-CoV-1 activity via defective glycosylation of viral ACE2 in Vero cells [149]. In addition. the interference of CLQ or CLQ-OH with SA synthesis may broadly be applicable as an antiviral because the HcoVs or other orthomyxoviruses also utilize SAs as entry molecules [150]. However, the detailed mechanisms should be further elucidated. The CLQ treatment efficacy in Covid-19 patients has, however, not been conclusively determined.\n\n7.2. Interaction of Membrane Gangliosides in Lipid Rafts with CLQ and CLQ-OH\nLipid rafts are also viral attachment sites. Viruses such as IBV, dengue virus, Ebola virus, hepatitis C virus, HIV, human herpes virus 6, measles virus, Newcastle disease virus, poliovirus, West Nile virus, foot-and-mouth disease virus, simian virus 40, rotavirus, influenza virus and Marburg virus also use lipid rafts for virus entry [151,152,153,154,155,156]. In avian CoV IBV, structural proteins of the IBV virus are co-localized with PM lipid rafts embedded with the ganglioside GM1. HCoV-229E entry is prevented by cholesterol depleted conditions because HCoV-229E clusters in caveolae-associated lipid rafts [157]. Caveolae of caveolin-1, -2 and -3 are cross-linked [158] and control the molecular distribution between rafts and caveolae in a regulatory mechanism. S protein-CD13 cross-linking occurs via CD13-caveolin-1 sequestering. HCoV-229E particles similarly exhibit a longitudinal distribution property. HCoV-229E-colocalized caveolin-1 undergoes the next step of virus infection. Caveolin-1 knockdown inhibited HCoV-229E endocytosis and entry and thus caveolin-1 is essential for HCoV-229E infection. TGEV also endocytoses by a clathrin-mediated mechanism in MDCK cells [159]. Other viruses including HCoV-OC43 also use an entry receptor sequestered to cross-linked caveolae [160]. In SARS-CoV, the first entry step to host cells needs ACE2 in intact lipid rafts by the S glycoprotein [151]. ACE2 is associated with caveolin-1 and GM1 in membrane rafts depending on its cell-type specific localization [161]. Raft integrity with cholesterol and ACE2 is necessary for SARS-CoV pseudovirus entry into Vero E6 cells and for SARS-CoV-microdomain-based entry. C-type lectin, CD209 L (L-SIGN), can also form lipid rafts and acts as a SARS-CoV receptor [162]. Information of the CoV entry pathways is important for therapeutic designation of SARS-CoV-targeting drugs, for example, if agents disrupt lipid-raft localization of the ACE2 receptor.\nCLQ binds the SAs and gangliosides in lipid rafts with a high affinity. Therefore, CLQ or CLQ-OH prevents the S glycoprotein–ganglioside binding. CLQ (or CLQ-OH) binding to SA consequently prevents S glycoprotein binding to host receptors. The N-terminal region of SARS-CoV-2 S glycoprotein interacts with gangliosides. A ganglioside-binding site (GBS) or ganglioside-binding domain (GBD) is present in the NTD of the S glycoprotein of SARS-CoV-2. Using molecular modeling and simulation technology, CLQ has been suggested to recognize the SAs and gangliosides. Human type Neu5Ac binds to CLQ and CLQ-OH. Thus, SAs are binding targets of CLQ and CLQ-OH. CLQ and CLQ-OH have two specific recognition sites in the polar sugar residues of ganglioside GM1. The first site is found at the tip of the sugar residues of GM1 with an interaction energy of −47 kJ/mol. The CLQ rings face the GalNAc residue of GM1, while the second site is in a large region of the sugar-ceramide junction and the sugar residues. Several amino acid residues of the S protein NTD, which are Phe-135, Asn-137 and Arg-158, recognize the ganglioside GM1. The S glycoprotein NTD-GM1 complex is suggested to form a trimolecular complex with two molecules of ganglioside GM1 anchored to the NTD of S protein [163]. The ACE2-binding RBD is suggested to be a potential GBS located on a differential site of the S glycoprotein NTD. The protein sequence interfacing surface of the NTD is the consensus GBDs [164]. The amino acids Gly, Pro and/or Ser residues found in GBD motifs are in the same 111–158 amino acids of the NTD as the ganglioside-attachment interface. The GBD is conserved throughout viral isolates from worldwide COVID-19 patients. The GBD potentially increases viral attachment ability to PM lipid rafts and contact between host ACE-2 and S protein [165]. The interaction between CLQ-OH and 9-O-acetyl-NeuAc is also similar to the 9-O-acetyl-NeuAc-CLQ interaction. The CLQ-OH OH group enhances the interaction of CLQ with SA via a hydrogen bond [163]. In conditions with CLQ or CLQ-OH derivative treatment, the S glycoprotein cannot bind to gangliosides in in silico studies, which are used to uncover the action mechanism. CLQ and CLQ-OH prevent the binding of S glycoprotein to gangliosides. The CLQ-SA complex is formed in a mixed surface and balls by the positioning of the negative charged COOH group of Neu5Ac and one of the two cationic charges of CLQ [163]. CoVs preferentially bind to 9-O-acetyl-NeuAc [60], differentiating with other viral properties.\nAs CLQ interacts with the GM1 sugar part, the N-terminal domain of the S protein loses viral attachment capacity to the cell receptors [166]. The S protein NTD and the CLQ/CLQ-OH maintain the same position during GM1 binding, consequently preventing GM1 binding to the S protein and the drug at the same time, because the NTD and the CLQ/CLQ-OH simultaneously recognize GM1. Asn-167 forms a hydrogen bond with the GalNAc residue, whereas an aromatic Phe-135 stacks to the Glc residue of GM1. Therefore, the antiviral activities of CLQ and CLQ-OH is to block the interaction between the SARS-CoV-2 S glycoprotein and gangliosides on host cell surfaces. The lipid composition of host cell PM can also be a potential target for preventive and therapeutic drugs against such 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