PMC:7461420 / 44869-52111 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7461420","sourcedb":"PMC","sourceid":"7461420","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7461420","text":"3.1.4 Inhibitors with aldehyde as a warhead group\nAlthough the above‐described inhibitors with 1,4‐Michael acceptors (e.g., α,β‐vinyl ethyl ester, –CH═CH–C(O)–OEt) showed enzymatic or cell‐based in‐vitro activities, they can be cleaved to their carboxylic acids by plasma esterases; for instance, AG7088 (29) was inactive in the plasma of rodents and rabbits. 144 , 145 Therefore, scientists explored different reactive groups that are stable in vivo.\nBased on the highly potent 1,4‐Michael‐acceptor‐based inhibitor 38, which they had previously developed (see Figure 15), Yang et al. 134 designed a peptide with a new efficient cysteine‐reactive group, using an aldehyde moiety. In addition, the P2‐leucine and the Michael groups of 38 were modified by a cyclohexyl unit and aldehyde group respectively to improve cellular activity. Indeed, the resulting peptide‐aldehyde 41 (Figure 15) showed remarkable activity against SARS‐CoV‐1 and HCoV‐229E Mpro. 134 It displayed promising antiviral activities decreasing viral load by 4.7 log (at 5 µM) for SARS‐CoV‐1 and 5.2 log (at 1.2 µM) for HCoV‐229E. This compound was stable in rat, mouse, and human plasma (even after 120 min, more than 70% of it remained in respective cells).\nFigure 15 SARS‐CoV‐1 and MERS‐CoV Mpro inhibitors with peptide aldehyde functionality. Mpro, main protease; SARS‐CoV, severe acute respiratory syndrome coronavirus Kumar et al. 146 reported another series of peptide‐aldehyde inhibitors with reduced molecular weight. Selected examples (42, 43) are depicted in Figure 15. They were potent, cell‐membrane permeable, dual Mpro inhibitors of SARS‐CoV‐1 and MERS‐CoV, without cytotoxicity (CC50 \u003e 100 µM). Compound 43, in particular, revealed highly potent activity against SARS‐CoV‐1 Mpro (IC50, 0.2 µM) and MERS‐CoV Mpro (IC50, 1.7 µM). It displayed antiviral activity (EC50, 0.06 µM) lowering the viral load and the secretion of virus particles in MERS‐CoV‐infected cells. Also, it displayed broad‐spectrum antiviral activity against other human α‐ and β‐CoVs.\nAkaji et al. discovered a series of SARS‐CoV‐1 Mpro inhibitors derived from its natural peptide substrate. Initially, they designed a pentapeptide (Ac‐Ser‐Val‐Leu‐N(CH3)2Gln‐CHO, 44) with Mpro inhibitory activity of 37 µM. 147 SAR studies of 44 led to inhibitor containing P1‐imidazole with improved potency (45; IC50, 5.7 µM). Further systematic structural modifications, primarily concentrating on P1‐, P2‐, and P4‐moieties, driven by X‐ray structure‐based analyses of the Mpro‐inhibitor complex, led to the identification of inhibitor 46 with remarkable inhibitory activity (IC50, 98 nM). The crystal structure of Mpro with 46 revealed significant binding interactions in the active site. The P1‐imidazole nitrogen atom created a hydrogen bond with the histidine residue's imidazole nitrogen, and the P2‐cyclohexyl moiety fitted well into the S2‐subsite. This compound was characterized as a competitive inhibitor without covalent bond formation.\nThe same research group disclosed a novel series of peptide inhibitors containing a decahydroisoquinoline moiety in place of P2‐cyclohexyl of 46 to reduce the peptidic nature of the inhibitors. A few examples (47–51) are shown in Figure 16. Among them, 49 was moderately more active against SARS‐CoV Mpro when compared to 46. 148 The X‐ray structure of Mpro in complex with 49 revealed that the P2‐decahydroisoquinoline moiety was fittingly placed in the S2‐subsite, while the P1‐imidazole moiety occupied the S1‐subsite. With these key residues located appropriately in their respective pockets, the terminal functional group fits tightly into the active site.\nFigure 16 Peptide inhibitors containing cyclohexyl and decahydroisoquinoline groups [Color figure can be viewed at wileyonlinelibrary.com] This group further extended their study to find inhibitors that interact with S2 to S4 subsites. Taking 49 as a lead, they designed a new compound, by combining a nonprime substituent at the decahydroisoquinoline moiety, as shown in example 52. 149 The resulting 52 showed more than twofold increased Mpro inhibitory activity compared to 49. This indicates that the additional interactions at S2–S4 sites enhance inhibitory activity.\nRather recently, the same research group explored the ability of octahydroisochromene to interact with the hydrophobic S2 pocket as an innovative P2‐moiety. 150 To identify the best specific configuration, all possible diastereomers were evaluated. It was found that the molecule with (1S,3S)‐octahydroisochromene 53–56 could secure the optimal position of the P1‐imidazole as well as the aldehyde functional group at the active site. Additionally, the N‐butyl side chain attached to the 1‐position of the fused ring system was recognized to be important for establishing hydrophobic interactions.\nIn 2018, Groutas et al. 151 disclosed a novel class of dual MERS‐CoV and SARS‐CoV‐1 Mpro inhibitors that contain a P3‐piperidine moiety (58–59; Figure 17). These inhibitors were derived from the dipeptidic‐aldehyde bisulfite adduct 57 (GC376), which was clinically studied as a protease inhibitor for its efficacy against CoVs such as the feline infectious peritonitis virus (FIPV). Compounds 58 and 59 showed potent antiviral activity toward MERS‐CoV in cell‐based bioassays (EC50, 0.5 µM for 58 and 0.8 µM for 59). SAR studies revealed that the piperidine moiety engaged in favorable hydrophobic interactions at the S3 and S4 pockets of the protease.\nFigure 17 Inhibitors with aldehyde, aldehyde bisulfite adduct, and epoxide warhead group The X‐ray crystal structures of MERS‐CoV 3CLpro in complex with inhibitor 59 showed that the piperidine ring is likely projecting toward the S4 subsite. Additionally, 59 was engaged in backbone H‐bonds with Gln192, Gln167, and Glu169.\nAzapeptide epoxides (APEs) are another class of SARS‐CoV‐1 Mpro inhibitors, although they were originally developed for clan CD cysteine peptidases. 152 , 153 The epoxide S,S‐diastereomer 60 (K inact/K i, 1900 (±400) M−1·s−1; Figure 17) exhibited the best inhibitory activity against SARS‐CoV Mpro. 154 The X‐ray structure of Mpro in complex with 60 confirmed the formation of a covalent bond between the cysteine‐S atom and the epoxide C‐3. It is worth noting that the S,S‐configured epoxide is required for the activity.\nVery recently, Dai et al. designed and synthesized two novel peptidomimetic SARS‐CoV‐2 Mpro inhibitors 61 and 62 (Figure 18) which exhibited extremely high inhibitory activity on purified Mpro with IC50 values of 50 and 40 nM, respectively. Furthermore, the group observed high antiviral activity of both compounds in cell‐based assays (61: EC50, 0.42 µM; 62: EC50, 0.33 µM). X‐ray structures were determined for both derivatives in complex with SARS‐CoV‐2 Mpro at 1.5 Å, providing detailed information about the binding pockets. Similar to related molecules that employ the aldehyde moiety as a warhead, a covalent bond with the active‐site Cys145 was demonstrated for both structures. Cytotoxicity assays revealed CC50 values greater than 100 µM. 155\nFigure 18 Peptidomimetic SARS‐CoV‐2 Mpro inhibitors with P3‐indole moiety. 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