PMC:7461420 / 63068-75887 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":"3.1.7 Small molecule inhibitors of Mpro\nBenzotriazole esters (88–91; Figure 26) were discovered as novel nonpeptidic irreversible inhibitors of SARS‐CoV‐1 Mpro. 168 Among them, 91 exhibited the best enzymatic inhibitory activity, but no antiviral activity in cell‐based assays. The covalent binding mode of 91 was confirmed by electrospray ionization mass spectrometry (ESI‐MS) analyses.\nFigure 26 Active esters as SARS‐CoV‐1 Mpro inhibitors. Mpro, main protease; SARS‐CoV, severe acute respiratory syndrome coronavirus With a slight structural modification from benzotriazole ester, Zhang et al. reported a series of active halopyridyl esters containing thiophene, furan, and indole moieties (92–95; Figure 26). Among them, 93 displayed the highest enzymatic inhibitory activity at SARS‐CoV‐1 Mpro. 169 However, no antiviral activity for this compound was communicated. The irreversible binding mode of 93 was confirmed by ESI‐MS analysis. 170 , 171\nGhosh et al. 172 studied the SARs of halopyridinyl indole carboxylates and identified a series of analogs (96–101; Figure 27) as SARS‐CoV‐1 Mpro inhibitors in the nanomolar potency range. The best derivative (100) had high enzymatic inhibitory potency (IC50, 0.030 µM) and antiviral activity (EC50, 6.9 µM). Compound 97 was also observed to inhibit the MERS‐CoV Mpro both in enzymatic and cell‐based (EC50, 12.5 µM) bioassays. 173 This molecule covalently modified Mpro, which was confirmed by MALDI‐TOF studies.\nFigure 27 SAR of halopyridinyl indole carboxylates as SARS‐CoV‐1 Mpro inhibitors. Mpro, main protease; SARS‐CoV, severe acute respiratory syndrome coronavirus 5‐Halopyridinyl esters are troublesome drug candidates because of their potential for rapid hydrolysis by various esterases and other enzymes in mammalian cells. They can potentially also react nonspecifically with other thiols and nucleophiles, a recipe for cytotoxicity. To bypass this problem by developing stable noncovalent inhibitors, Zhang et al. 174 reported a group of methylene ketones and analogous mono‐ and di‐fluorinated methylene ketones based on pyridinyl esters (102 and 103; Figure 28) as SARS‐CoV‐1 Mpro inhibitors. Enzymatic investigations and ESI‐MS experiments illustrate that those inhibitors bind to their target in a noncovalent, reversible manner.\nFigure 28 Etacrynic acid and isatin derivatives as SARS‐CoV‐1 Mpro inhibitors. Mpro, main protease; SARS‐CoV, severe acute respiratory syndrome coronavirus An HPLC‐based screening of electrophilic compounds identified the etacrynic acid‐derived amide 106 and ester 107 as SARS‐CoV‐1 Mpro inhibitors with moderate potency. 175 Etacrynic carboxamide (105; K i, 35.3 µM) bound more strongly to SARS‐CoV‐1 Mpro than to papain protease, while etacrynic acid ester 104 was more active at papain protease (K i, 3.2 µM) than at SARS‐CoV‐1 Mpro (K i, 45.8 µM; Figure 28). SAR studies suggested that chloro substituents were necessary for protease inhibition. Docking studies of 105 to Mpro revealed that it forms hydrogen bonds with Gln189, Glu166, Thr190, and Gln192 with its terminal amino group. The Michael system carbonyl group interacts with Gly143, and the reactive double bond remained next to the Cys145 sulfur.\nPreviously, isatin (2,3‐dioxoindole) derivatives were observed to inhibit rhinovirus 3C protease. 176 Due to the structural similarity between the rhinovirus 3C protease and SARS‐CoV‐1 Mpro, these derivatives were tested against SARS‐CoV‐1 Mpro. Among them, 106 (IC50, 0.95 µM) and 107 (IC50, 0.98 µM) exhibited the best SARS‐CoV‐1 Mpro inhibitory activity in the low micromolar range. 176 SAR studies suggested that the inhibition efficiency was mainly reliant on hydrophobic and electronic properties of the isatin core substitution pattern. Docking studies revealed that the molecules fit well in the active site of the protease. Both carbonyl groups of the isatin core engaged in H‐bonds with NH of Gly143, Ser144, Cys145, and His41. Compounds 106 and 107 176 were more selective for SARS‐CoV‐1 Mpro than other proteases like papain (106, 103 µM; 107, 87.24 µM), chymotrypsin (106, ~1 mM; 107, 10.4 µM), and trypsin (106, 362 µM; 107, 243 µM; Figure 28).\nZhou et al. extended the SAR studies for further activity improvement. Compound 108 bearing carboxamide showed the best SARS‐CoV‐1 Mpro inhibitory activity. However, this derivative did not bind covalently to the Cys145 residue of the active site. 177 Further structural investigations at the carboxamide of 108 with a variety of substituted sulfonamides did not improve the activity. Compound 109 was the best one of that series (Figure 28). 178\nThe modification of 110, identified by high‐throughput screening (HTS; Figure 29), led to pyrazolone and pyrazole derivatives 111 and 112 as SARS‐CoV‐1 Mpro inhibitors. 179 , 180 Taking these as leads, Ramajeyam et al. 181 reported compounds 112–114 to be the best‐performing inhibitors of the series(IC50 5.5, 6.8, 8.4 µM, respectively). They also observed moderate inhibitory activity against CVB3 3Cpro. Structure‐functionality analyses illustrated that the benzylidene ring next to pyrazolone C4 in addition to electron‐withdrawing groups, favors inhibitory activity. Molecular modeling studies of 112 predicted that for its inhibitory function, the N1‐phenyl residue in the Mpro S1 site as well as the carboxyl benzylidene moiety in the S3 pocket are important.\nFigure 29 Pyrazoles and pyrimidines as SARS‐CoV‐1 Mpro inhibitors. Mpro, main protease; SARS‐CoV, severe acute respiratory syndrome coronavirus Kumar et al. described furan‐inserted pyrazolone derivatives as dual SARS‐CoV‐1 Mpro and MERS‐CoV Mpro inhibitors (115–118; Figure 29). 182 Compounds 115, 117, and 118 exhibited the best dual inhibitory activities. Compounds 115 and 116 also displayed inhibitory activity against H5N1 neuraminidase (IC50 2.8, 2.9 µM, respectively). 183 Ramajeyam et al. also disclosed a range of pyrimidine derivatives as SARS‐CoV‐1 Mpro inhibitors (119–121). Compound 121 showed high inhibitory potency with an IC50 value 6.1 µM. 181\nHTS of NIH molecular libraries (~293 000 substances) yielded the dipeptide 122 containing 3‐pyridyl as hit compound against SARS‐CoV‐1 Mpro with an IC50 value of 2.2 µM (Figure 30). Preliminary SAR studies identified 123 and 124 as the most promising inhibitors of the series. 184 , 185\nFigure 30 Simple dipeptide derivatives as SARS‐CoV‐1 Mpro inhibitors. Mpro, main protease; SARS‐CoV, severe acute respiratory syndrome coronavirus The X‐ray crystal structure of 123 attached to SARS‐CoV‐1 Mpro highlighted the compound's identical orientation in the pocket to that of established covalent peptidomimetic inhibitors (Figure 31). The compound with an R‐configuration occupied the S3‐S1' subsites of SARS‐CoV‐1 Mpro. Indeed, only (R)‐123 was able to inhibit the Mpro enzyme with an IC50 value of 1.5 µM, while the (S)‐enantiomer was inactive. (R)‐123 inhibited SARS‐CoV‐1 Mpro in a competitive manner (K i, 1.6 µM) with a noncovalent mode of inhibition. (R)‐123 also showed antiviral activity (12.9 µM) in mock infected and SARS‐CoV‐1 infected Vero E6 cells.\nFigure 31 The X‐ray crystal structure of 123 bound to the binding pocket of SARS‐CoV‐1 Mpro (PDB ID: 3V3M). Pockets S1'–S3 are highlighted. Mpro, main protease; SARS‐CoV, severe acute respiratory syndrome coronavirus [Color figure can be viewed at wileyonlinelibrary.com] To enhance the inhibitory activity, SAR study efforts around P1' of 123 provided compounds containing imidazole (125) and 5‐chlorofuran (126) with equipotent activity to lead 123 (Figure 30). Next, the exploration of P1 3‐pyridyl unit of 123 revealed pyridazine (127) and pyrazine (128) which were only tolerated, albeit without any improvement.\nThe same group of researchers discovered potent, noncovalent SARS‐CoV‐1 Mpro blockers based on a benzotriazole scaffold in an MLPCN screening, 186 resulting in hit compound 129 (Figure 32) with a SARS‐CoV‐1 Mpro IC50 value of 6.2 µM.\nFigure 32 SARS‐CoV‐1 Mpro inhibitors containing the benzotriazole scaffold. Mpro, main protease; SARS‐CoV, severe acute respiratory syndrome coronavirus SAR studies focusing on the benzotriazole moiety of 129 were performed to improve activity. The replacement of this group with 4‐phenyl‐1,2,3‐triazole (as in 130) was somewhat tolerated (IC50 of 11 µM; Figure 32). Further modifications to the acetamide (P2‐P1' region) resulted in molecules bearing a thiophene ring on one side and a branched i‐propyl amide (131) or cyclobutylamide (132) on the other—reaching IC50 values below 5 µM.\nTo cut overall molecular weight of the inhibitors, P3‐truncation was performed, which led to potent derivatives (133–137; Figure 32). Compound 137 displayed extremely high inhibition (IC50, 51 nM).\nSARS‐CoV‐1 Mpro inhibitors were also discovered from medicinal plants. In 2011, Ryu et al. 187 disclosed a range of inhibitors obtained from Torreya nucifera leaves. Of all the isolated chemicals, the biflavone, amentoflavone (138; Figure 33), was identified as a potent noncompetitive inhibitor with an IC50 of 8.3 µM. Docking studies of 138 identified the interactions of Val186 and Gln192 as major sites at the target.\nFigure 33 Flavone and terpenoid derivatives with inhibitory activity against SARS‐CoV‐1 3CLpro. 3CLpro, 3C‐like protease; SARS‐CoV, severe acute respiratory syndrome coronavirus They also isolated a series of terpenoids from T. nucifera as anti‐SARS‐CoV Mpro agents (Figure 33). 187 Among them, ferruginol (139; IC50 49.6 µM) was the most active compound. Additionally, they isolated quinone‐methide triterpenoids celastrol (140), pritimererin (141), and tingenone (142) from methanol extracts of Tripterygium regelii which exhibited fair inhibition activity (IC50 2.6, 9.9, 5.5 µM, respectively). SAR studies indicated that for effective inhibition, the quinone‐methide group in ring A and the more lipophilic ring E were critical. All compounds were characterized as competitive inhibitors using kinetic analyses.\nWen et al. 188 reported abietane‐type diterpenoids and lignoids with a powerful anti‐SARS‐CoV‐1 Mpro effect. Especially betulinic acid (143) and savinin (144) effectively inhibited SARS‐CoV‐1 Mpro (K i 8.2 µM, 9.1 µM, respectively) (Figure 33). These inhibitors acted in a competitive manner.\nLu et al. discovered two hit SARS‐CoV‐1 3CLpro inhibitors, sulfone 145 and dihydroimidazole 146, by structure‐based virtual screening of a compound library of 58 855 chemicals (Figure 34). 189 The central structural elements of the hits, determined in docking experiments, were then used for additional analog searches.\nFigure 34 Structure of SARS‐CoV‐1 Mpro inhibitors 145–149. Mpro, main protease; SARS‐CoV, severe acute respiratory syndrome coronavirus Computational similarity screening discovered 21 analogs from these hits. Among them, the two best compounds 147 and 148 display IC50 values of 0.3 and 3 µM, respectively. A variety of SARS‐CoV‐1 Mpro inhibitors have been identified through virtual screening (VS) as an alternative to HTS. VS of 50 240 structurally diverse small molecules allowed to identify 104 molecules with anti‐SARS‐CoV‐1 activity. Compound 149 (Figure 34) demonstrated potent enzyme inhibition (IC50, 2.5 μM) and an EC50 of 7 μM in Vero cell‐based SARS‐CoV‐1 plaque reduction assays\nVirtual screening identified the serotonin antagonist cinanserin (150, Figure 35) as a potential inhibitor of Mpro. It had previously shown activity against SARS‐CoV‐1 Mpro with an IC50 value of 5 µM. 190 Subsequent tests revealed its anti‐SARS‐CoV‐2 activity (EC50, 20.6 µM) and an IC50 value of 125 µM (SARS‐CoV‐2 Mpro).\nFigure 35 Covalent bond inhibitors of Mpro. Mpro, main protease Their HTS yielded seven primary hits including the approved drugs disulfiram (151) and carmofur (152), as well as ebselen (153), shikonin (154), tideglusib (155), and PX‐12 (156) (Figure 35).\nUsing MS/MS analysis, they deduced that ebselen (153) and 156 are irreversible inhibitors of Mpro by covalently attaching to Cys145 of the catalytic dyad. Molecular docking was used to illustrate how 151, 154, and 155 bind to Mpro. Antiviral activity assays, using real‐time reverse transcription‐PCR, indicated that ebselen and inhibitor “N3” (40; Figure 12) had the strongest antiviral effects. Ebselen displayed an EC50 value of 4.67 µM, and “N3” showed an EC50 value of 16.77 µM in a plaque‐reduction assay. Ebselen's IC50 value for SARS‐CoV‐2 Mpro was reported at 0.67 µM. The activity data of remaining compounds is summarized in Figure 35.\nEbselen has been studied for an array of diseases and has a very low toxicity. 191 , 192 , 193 Its safety has been demonstrated in clinical trials. 191 , 192 , 194 It can therefore be considered a promising molecule for the treatment or prevention of CoV 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