PMC:7571312 / 10193-34225 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7571312","sourcedb":"PMC","sourceid":"7571312","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7571312","text":"Results and Discussion\n\nChemistry\nCentral to our strategy of examining ketone-based thiophiles was the preparation of an array of intermediates containing diverse methylketone moieties and protecting groups. The preparation of halomethylketone intermediates was accomplished in a two-step procedure by the generation of a diazoketone intermediate31 or directly by a modified Kowalski–Haque reaction,32 as depicted in Scheme 1.\nScheme 1 Preparation of P1 Synthetic Intermediates\n(i) 3 M NaOH, MeOH (95%), (ii) isobutylchloroformate (IBCF), triethylamine (TEA), tetrahydrofuran (THF), (iii) CH2N2/ether (92%), (iv) 4 M HCl/dioxane (83%), (v) 1.0 equiv 48% HBr (83%), (vi) HNCH3(OCH3), EDC, HOBt, NMM, dichloromethane (DCM) (79%), (vii) Mg, HgCl2, BOM-Cl, THF, −78°C (50%), and (viii) lithium diisopropylamide (LDA), ClCH2I, THF (54%). Saponification of amino ester 5(33) afforded the corresponding amino acid 6 in nearly quantitative yield. Acid 6 was treated with isobutylchloroformate and triethylamine, and the resulting mixed anhydride was reacted with diazomethane34 to provide high isolated yields of 7. Diazoketone 7 was treated with hydrochloric acid for simultaneous nitrogen deprotection and conversion to the chloromethylketone (CMK) intermediate 10. Alternatively, the N-Boc-protected bromomethylketone was prepared by treatment of 7 with stoichiometric quantities of 48% HBr in dichloromethane to provide 11. Another preparation of CMK intermediates that avoids the use of diazomethane was accomplished by the reaction of 5 with excess LDA and chloroiodomethane to afford 8 in moderate yields. A direct approach to oxymethylketone intermediate 9 was achieved by conversion of acid 6 to the corresponding Weinreb amide followed by treatment with the Grignard generated from benzyl chloromethyl ether.35\nA key element for rapid access to substituted methylketone derivatives was the generation of the fully elaborated CMK 12 (Scheme 2). The utility of the CMK moiety to prepare acyloxy- and hydroxy-substituted methylketones is well established. Elaboration of 10 in a sequence of deprotection/1-[bis(dimethylamino)methylene]-1H-1,2,3-triazolo[4,5-b]pyridinium 3-oxid hexafluorophosphate (HATU)-mediated peptide couplings provided CMK derivative 12 in moderate yield with no epimerization observed. Reaction of 12 with various carboxylic acids in the presence of cesium fluoride at 60 °C provided acyloxymethylketones 13–28. Using this synthetic approach with substitution of P2 and amine capping structural elements provided inhibitors 3 and 29–31.\nScheme 2 Preparation of Substituted Acyloxymethylketones and Aminomethylketones\n(i) Boc-Leu-OH, HATU, NMM, N,N-dimethylformamide (DMF), 0 °C (64%), (ii) 4 M HCl/dioxane, (iii) HATU, 4-MeO-2-indolecarboxylic acid, NMM, DMF, 0 °C (61%), and (iv) CsF, DMF, carboxylic acid, 60 °C (43–91%). Hydroxymethylketone (HMK) derivatives were accessed by two complimentary approaches illustrated in Scheme 3. Elaboration of the P1′-protected oxygen intermediate 9 by sequential amide bond coupling reactions provided benzylether derivatives such as 34 in moderate yields with a low propensity for epimerization at the P1 center. Hydrogenolytic debenzylation readily afforded the final HMK inhibitors exemplified by 36. Alternatively, fully elaborated CMK derivatives such as 35 were reacted with benzoylformic acid followed by methanolysis to generate HMK final products such as 36.36 Alkylation of the terminal hydroxyl was achieved under microwave-assisted conditions in the presence of silver (I) oxide to afford alkoxymethylketone inhibitors, as illustrated by 37. Using these two synthetic approaches with substitution of P2 and amine capping structural elements provided inhibitors 4 and 38–50.\nScheme 3 Preparation of Hydroxymethylketone Derivatives\n(i) 4 M HCl/dioxane, (ii) Boc-Leu-OH, HATU, NMM, DMF, 0 °C, (iii) HATU, 4-MeO-2-indolecarboxylic acid, NMM, 0 °C, (iv) Pd/C, H2, EtOH (77%), (v) CsF, DMF, benzoylformic acid, 60 °C, and then MeOH, cat. K2CO3 (53%), and (vi) CH3I, Ag2O, DCE (9%).\n\nBiological Evaluation\n\nIrreversible Inhibitors of SARS CoV-1 3CLpro\nThe warhead reactivity and binding affinity to P1′ are both important design considerations to ensure specificity of irreversible inhibitors. Krantz has demonstrated that the inherent chemical reactivity of acyloxymethylketones can be tuned to inhibit cysteine proteases through the modulation of substituent effects on the carboxylate leaving group.37 The importance of leaving group “strength” was confirmed by the strong dependence between the pKa of the leaving carboxylate and cathepsin B enzyme inhibition. These otherwise weak electrophiles are elegant “quiescent” inhibitors that harness the very same interactions with catalytic residues that lead to proteolysis rate acceleration. Molecular modeling of a 2,6-dichlorobenzoate design with SARS CoV-1 3CLpro indicated that a low strain conformation of the ketone carbonyl was aligned in the oxyanion hole and the substituted benzoate is accommodated within the P1′ site. A series of acyloxymethylketone derivatives were prepared, as depicted in Table 1.\nTable 1 SARS CoV-1 3CLpro Inhibition Data for Acyloxymethylketone Inhibitors\n    SARS CoV-1 3CLpro FRETa\nentry R kobs/I (M–1 s–1) IC50 (nM)\n12   283,039 ± 22,586  \n13 Me   220 ± 0.5\n14 cyc-propyl   182 ± 6\n15 tert-butyl   230 ± 5\n16 Ph   86 ± 3\n17 4-OMe-Ph   79 ± 3\n18 4-Me-Ph   87 ± 2\n19 4-CN-Ph   53 ± 1\n20 4-F-Ph   82 ± 3\n21 4-Cl-Ph   97 ± 3\n22 2,6-(Cl)2-Ph 62,993 ± 2,501  \n23 2,6-(F)2-Ph 12,776 ± 594  \n24 2-OH-4-Cl-Ph 11,525 ± 40  \n25 2-F, 4-CN-Ph 13,321 ± 2,309  \n26 2,6-(Me)2-Ph   74 ± 4\n27 2,6-(MeO)2-Ph   205 ± 2\n28 2-CN-Ph   17 ± 2\na See the Experimental Section for details on assay methods; the values were calculated from at least eight data points with at least two independent determinations. As expected, chloromethylketone 12 is a potent irreversible inhibitor of SARS CoV-1 3CLpro. Compounds 22–25 possess the most electron-deficient benzoate leaving groups and display kinetics consistent with irreversible inhibition. The remaining entries appear to be reversible inhibitors in the time scale of the assay, with 28 possessing the most potent IC50. A crystal structure (PDB code 6XHN)38 of 28 in complex with SARS CoV-1 3CLpro at 2.25 Å shows a covalent adduct, which demonstrates the bimodal activity of certain acyloxy inhibitors (Figure 4). In this structure, the electron density for the 2-cyanobenzoate moiety is absent and the 3CLpro active-site cysteine (Cys145) sulfur forms a covalent bond to the methylene carbon (1.8 Å C–S bond length). The ketone carbonyl is positioned within the oxyanion hole and as such engaging in hydrogen bonds with backbone NH groups of Gly143 and Cys145. A detailed analysis of an extended hydrogen bond network from catalytic His41 reveals that the side-chain imidazole serves as a hydrogen bond donor to the interior of the protease. Specifically, the imidazole hydrogen is directed toward a lone pair electron acceptor from a structural water. We can conclude that this water must be an acceptor to His41 as one of the water hydrogens is engaged with acceptor electrons on the side chain of Asp187, and the second hydrogen engages a terminating acceptor backbone carbonyl on Asp176 through a short network that includes the side chains of an internal, neutral His164 and Thr175.\nFigure 4 Cocrystal structure of the covalent adduct of 28 bound to SARS CoV-1 3CLpro (PDB code 6XHN). The Connolly surface for the inhibitor binding pocket is shown in gray. The bonds are represented as dashed lines, with the bond length between heavy atoms depicted. The 2,6-dichlorobenzoate derivative 22 displays the highest levels of potency in the SARS CoV-1 3CLpro and in antiviral cytopathic effect assays in Vero 76 cells (EC50 = 0.29 ± 0.19 μM).39 We note here that the assay in Vero 76 cells provided data establishing antiviral activity, but the translation of potency measured in Vero cells, which have high efflux potential, to the potency achievable in human lung cells was unknown (vide infra). As expected, 22 possesses low levels of reactivity toward endogenous nucleophiles such as glutathione (t1/2 \u003e 60 min)40 and exhibits high levels of stability in human plasma (t1/2 \u003e 240 min).41 Although 22 displays a promising activity profile, it possesses very poor solubility in clinically relevant IV vehicle formulations, thus limiting its development as an IV clinical agent.\nTo improve the solubility characteristics of inhibitors incorporating the lipophilic 2,6-dichlorobenzoate, a limited set of inhibitors containing smaller or more polar amine capping fragments were prepared (Table 2). Replacement of the 4-methoxy indole cap present in 22 with a benzimidazole provided 31. This inhibitor displayed potent irreversible inhibition kinetics but did not improve solubility compared to 22. Reduction in the size of the P2 capping element as represented by 29 and 30 provided derivatives that possessed weak reversible SARS CoV-1 3CLpro inhibition.\nTable 2 SARS CoV-1 3CLpro Inhibition Data for P3-Modified Acyloxymethylketone Inhibitors\na See the Experimental Section for details on assay methods; the values were calculated from at least eight data points with at least two independent determinations. Another design to replace the 4-methoxy indole was the (2R)-tetrahydrofuran-2-carboxylate, which molecular modeling suggested could make additional favorable protein interactions with a Gln189 side chain and led to the preparation of 3. Initially, this derivative appeared to display reversible binding kinetics. However, further kinetic studies of compound 3 with the SARS CoV-1 3CLpro protein demonstrated irreversible time-dependent inactivation of this enzyme (kobs/I = 5834 ± 151 M–1 s–1). Additionally, 3 possessed potent antiviral activity in Vero cells (EC50 = 2.4 μM) and solubility in vehicle formulations almost 20-fold higher than 22. Evaluation of the pharmacokinetic profile of 3 in rat suggested that this inhibitor possessed properties potentially sufficient for an IV continuous infusion dosing paradigm.42\nAlthough irreversible inhibition can provide an extended pharmacodynamic effect when protein resynthesis rate is slow compared to drug clearance, such extended effects for 3CLpro inhibition were not necessarily expected. The 3CLpro-mediated proteolysis of newly expressed viral polyproteins is essential to virus replication; however, this activity only occurs during a single step in the virus life cycle that closely follows each cell infection. Viral particles themselves are not reliant on 3CLpro activity nor are the remaining coronavirus life cycle steps. Each event of cell infection initiates newly synthesized 3CLpro. Because detailed kinetics of this process are not understood, reversible and irreversible inhibitors were investigated equally.\n\nReversible Inhibitors of SARS CoV-1 3CLpro\nPeptidyl HMK inhibitors and their corresponding ethers have been designed as potent reversible cysteine protease inhibitors of cathepsin K34 and cruzain.43 High-resolution crystal structures of two such inhibitors complexed with cruzain highlighted the presence of a strong hydrogen bond between the catalytic His and the α-hydroxyl moiety of the inhibitor but interestingly no covalent bond between the active-site Cys and the ketone pharmacophore. Utilizing the crystal structure of 28 in complex with SARS CoV-1 3CLpro, molecular modeling of an HMK-based design indicated the potential for establishing a covalent bond between the sulfur of the active-site cysteine (Cys145) and the HMK carbonyl as well as hydrogen bond interactions between catalytic His41 and the terminal hydroxy moiety. Additionally, the structure of 28 suggested the possibility to increase the lipophilic filling of the deep hydrophobic S2 pocket as a strategy to increase binding affinity. To evaluate these structure-based observations, a series of reversible HMK inhibitors containing P2 diversity were prepared as depicted in Table 3.\nTable 3 SARS 3CLpro Inhibition Data for P2-Modified HMK Inhibitors\na\u0026b See the Experimental Section for details on assay methods; the values were calculated from at least eight data points with at least two independent determinations.\nc This value is a Ki measurement.\nd These values are from a single determination. As suggested by molecular modeling, the S2 site appears to accommodate a variety of linear, branched, and cyclic alkyl moieties (entries 36 and 39–41). Interestingly, the P2 Phe derivative 42 displayed less potent inhibition of the SARS CoV-1 3CLpro than the corresponding saturated analogue 41. Also noteworthy is the large attenuation in enzyme inhibition seen with P2-N-methyl-Leu inhibitor 38 (IC50 = 83 nM) as compared to 4 (Ki = 4 nM). This loss of potency is consistent with the inhibitor ligand interactions observed with 2 and 4 that show the P2 NH involved in a hydrogen bond with the side-chain amide of Gln189. Additionally, the methyl substitution in 38 would be expected to alter the conformation of the 4-methoxy indole cap and perturb the observed ligand–enzyme hydrogen bond network present in 2 and 4.\nThe results for 4 and the other examples in Table 3 reveal a high antiviral EC50/enzyme IC50 ratio, which may arise from poor cell permeability. Indeed, these HMK inhibitors exhibit very low permeability and high levels of efflux beyond the sensitivity of the Caco-2 in vitro assay. However, the impact of high efflux on antiviral potencies from Vero 76 cells (derived from monkey kidney) versus disease-relevant human lung epithelial cells is unknown. To better understand the observed high antiviral EC50/enzyme IC50 ratio for 4, we evaluated the role of efflux in the Vero 76 cell line by the in vitro experimental design discussed further below. Concurrently, a strategy to design molecules reducing efflux by active transporters, such as P-glycoprotein, was pursued to decrease high antiviral EC50/enzyme IC50 ratios. An analysis of the physicochemical properties of 4 suggested that increasing logP, reducing polar surface area (PSA), and reducing the number of hydrogen bond donors/acceptors were design strategies with the potential to improve cellular permeability and reduce efflux.\nAn examination of the crystal structure of 2 in complex with SARS CoV-1 3CLpro suggested a limited functional role for the 4-methoxy substituent contained in the P3 indole cap. Additionally, the terminal α-hydroxyl moiety located at P1′ appeared to provide a potential opportunity to remove a hydrogen bond donor. Although it was anticipated that the α-hydroxyl moiety would form a hydrogen bond to the catalytic His41, the directionality of this interaction was uncertain. As noted earlier, His41 presents a hydrogen bond donor to the interior of the protease, leaving an acceptor to participate in the proton transfer cycling from neutral to cationic in the putative catalytic mechanism44 of proteolysis. If His41 is protonated in the inhibitor-bound complex, a lone pair from the α-hydroxyl moiety would function as a hydrogen bond acceptor from the proton on the His residue. On the other hand, if His41 is deprotonated, the hydrogen of the α-hydroxyl moiety would act as a hydrogen bond donor to the nitrogen lone pair of the His residue. Consistent with the strategy to decrease PSA and hydrogen bond donors, a series of inhibitors were prepared that contained alterations to the P3 cap and substitution of the α-hydroxyl group.\nTable 4 summarizes this effort where two of the optimal P2 residues (Leu and β-tert-butyl-Ala) were conserved. Removal of the methoxy group from the indole generally led to slightly weaker potency in both the enzymatic and antiviral assays across pairs (43 vs 36, 44 vs 37, 50 vs 48 and 49 vs 4) and therefore no improvement in the antiviral/protease inhibition ratio. The impact of more significant changes to the P3 cap is illustrated by tetrahydrofuranyl derivatives 46 and 47. These derivatives lack the lipophilic aryl ring and NH hydrogen bond donor present in the indole P3 cap and exhibit a pronounced reduction in enzymatic and antiviral potency. A noteworthy reduction in biochemical and antiviral potency was observed in comparing each hydroxymethylketone derivative with its corresponding ether counterpart. These results suggest that modest structural and physicochemical alterations of 4 fail to significantly decrease the high EC50/IC50 ratios for this class of peptidomimetics. However, in vitro analysis of 4 revealed this derivative to possess high levels of metabolic stability in human liver microsomes (t1/2 = 107 min).45 Further evaluation of this breakthrough derivative in several aqueous-based formulations suitable for IV administration indicated high levels of solubility.46\nTable 4 SARS CoV-1 3CLpro Inhibition Data for P3- and P2-Modified Hydroxymethyl and Alkoxymethylketone Inhibitors\na\u0026b See the Experimental Section for details on assay methods; the values were calculated from at least eight data points with at least two independent determinations.\nc This value is a Ki measurement.\nd These values are from a single determination. Cocrystal structures of 4 bound to the 3CLpro of both SARS CoV-1 and CoV-2 were solved at 1.47 and 1.26 Å resolutions, respectively (PDB codes 6XHL and 6XHM).47 As expected, the ligand binding sites of the main protease from SARS CoV-1 and SARS CoV-2 are conserved in sequence and are nearly identical structurally. The schematic diagram in Figure 5 is representative of the covalent adduct between 4 and the 3CLpro from both CoV-1 and CoV-2. The warhead HMK carbonyl carbon of 4 forms a covalent bond to the 3CLpro active-site cysteine (Cys145) sulfur generating a tetrahedral carbinol complex (1.8 Å C–S bond length). This carbinol hydroxyl forms hydrogen bonds with the backbone NH of Cys145 and with the amide NH of Gly143 via a bridging water molecule. Another key active-site interaction is the hydrogen bond between the primary alcohol moiety of 4 and the catalytic His41. Similar interactions between catalytic His residues and the OH moiety of HMK in other protease–inhibitor complexes have been reported.43\nFigure 5 Cocrystal structure of the covalent adduct of 4 bound to SARS CoV-2 3CLpro (6XHM). The Connolly surface for the inhibitor binding pocket is shown in gray. The bonds are represented as dashed lines, with the bond length between heavy atoms depicted. The schematic rendering of the active site with dashed lines represented as hydrogen bonds with key residues and curved lines to show S1 and S2 binding pockets is depicted. In S1, the lactam carbonyl of 4 forms a strong hydrogen bond with the side chain of His163, while the lactam NH is within the hydrogen-bonding distance but poorly aligned with the side-chain oxygen of Glu166 and the backbone oxygen of Phe140. These three residues partially define the bottom and edge of the S1 pocket. Additionally, the backbone carbonyl and NH of Glu166 form β-sheet-like hydrogen-bonding interactions with the NH and C2-carbonyl of the indole fragment of 4. The NH of the P2 Leu of inhibitor 4 and the side chain of Gln189 form a hydrogen bond, while the carbonyl of P2 Leu is exposed to the solvent. The inhibitor P1 NH forms a strong hydrogen bond with the backbone carbonyl of His164. The inhibitor’s lipophilic leucine residue is bound to the SARS 3CLpro in the hydrophobic S2 pocket formed by residues Asp187, Arg188, Gln189, Met49, and His41. The indole portion of 4 does not protrude into the S3 pocket but rather rests across a partially collapsed S3, making extended van der Waals interactions across the 189–191 residue backbone atoms. The closed S3 is the only significant conformational difference compared to a recently reported structure of SARS CoV-2 3CLpro inhibited by α-ketoamides.8 The energetics of this extended interaction, the associated protein conformation stabilities, or warhead difference may contribute to the 3-order-of-magnitude increased SARS CoV-2 3CLpro potency of HMK 4 (see below) compared to that of the referenced ketoamides.\nHydroxymethylketone 4 was evaluated against a panel of other viral and human proteases (Table 5). In general, 4 is highly selective for 3CLpro inhibition, displaying IC50 values of \u003e10 μM against many of the other proteases and possessing modest levels of inhibition of cathepsin B (IC50 = 1.3 μM) and rhinovirus 3Cpro (IC50 = 1.7 μM). High levels of similarity between the catalytic sites of 3CLpro proteases suggest the potential of 4 as a pan-coronavirus inhibitor. Testing revealed that 4 demonstrates potent inhibition of the related hCoV 229E protease (IC50 = 0.004 μM) but more importantly, given the current global pandemic, potently inhibits SARS CoV-2 3CLpro with a Ki of 0.27 nM.\nTable 5 Protease Inhibition by 4\nprotease source % inhibition @ 10 μMa IC50 (μM)a\n3CLpro SARS CoV-1   0.004 ± 0.0003b\n3CLpro SARS CoV-2 0.00027 ± 0.0001b\ncathepsin B human 93 1.3 ± 0.1\ncathepsin D human 3 \u003e10\nleukocyte elastase human –31 \u003e10\nchymotrypsin human 8 \u003e10\nthrombin human –28 \u003e10\npepsin human –2 \u003e10\ncaspase 2 human –20 \u003e10\nHIV-1 HIV-1 0 \u003e10\nHCV HCV 16 \u003e10\nHRV HRV   1.7 ± 1\nhCoV 229E human   0.004 ± 0.0004\na See the Experimental Section for details on assay methods; the values were calculated from at least eight data points with at least two independent determinations.\nb For SARS CoV-1 and CoV-2 3CLpro, Ki values are reported here. The antiviral specificity of 4 was evaluated against a panel of viruses (Table 6). No antiviral activity was observed when 4 was tested against two human rhinovirus strains (HRV-14 and HRV-16), human immunodeficiency virus-1 (HIV-1), or human cytomegalovirus (HCMV) in cell culture. This compound also does not inhibit the HCV replicon. As anticipated by the potent hCoV 229E protease activity, 4 is a potent inhibitor of the human coronavirus hCoV 229E in MRC-5 cells (human lung-derived) with an EC50 of 0.090 μM.\nTable 6 Viral Inhibition by 4\nvirus EC50 (μM)a CC50 (μM)a\nSARS CoV-1 4.8 ± 2.2 452\nhCoV 229E 0.09 ± 0.04 \u003e40\nHRV-14 \u003e100 \u003e1,260\nHRV-16 \u003e100 \u003e1,260\nHIV-1 RF \u003e32 \u003e32\nHCV replicon \u003e320 \u003e320\nHCMV RC256 \u003e100 \u003e100\na See the Experimental Section for details on assay methods; the values were calculated from at least eight data points with at least two independent determinations. The hCoV 229E antiviral potency is more than 50-fold greater than that for SARS CoV-1 in the Vero 76 line, even though 4 possesses nearly equivalent 3CLpro biochemical potency for the hCoV 229E and CoV-1 viruses. While undefined differences between hCoV 229E and SARS CoV-1 could account for these large differences in antiviral EC50/enzyme IC50 ratios, different active transporter expression levels between MRC-5 and Vero 76 cell lines may also be a contributing factor. Consistent with the previously stated goal to characterize the impact of efflux on potency measured in the SARS CoV-1 antiviral assay, we co-dosed a known P-glycoprotein transport inhibitor at a fixed concentration (0.5 μM CP-100356)48 in a full dose–response of inhibitor 4. This resulted in a pronounced potency shift of SARS CoV-1 antiviral activity (EC50 = 0.11 μM) that now more closely matched the antiviral potency seen for hCoV 229E. As a control, the same co-dosing of efflux inhibitor led to no such shift in the hCoV 229E antiviral potency of 4, demonstrating that the human lung-derived MRC-5 cells show less P-glycoprotein-based transporter under similar assay conditions. These results suggest that the high antiviral EC50/enzyme IC50 ratio observed in Vero 76 cells is an artifact of the high efflux potential of that assay cell line and may underestimate the antiviral potency in human lung cells, the relevant tissue for SARS and COVID-19. Assays to directly measure the antiviral potency of 4 against SARS CoV-2 in clinically relevant human lung cells are currently under 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