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[Preprint]. 2020 Sep 10:2020.09.07.286344. [Version 1] doi: 10.1101/2020.09.07.286344

Inhibitor binding influences the protonation states of histidines in SARS-CoV-2 main protease

Anna Pavlova, Diane L Lynch, Isabella Daidone, Laura Zanetti-Polzi, Micholas Dean Smith, Chris Chipot, Daniel W Kneller, Andrey Kovalevsky, Leighton Coates, Andrei A Golosov, Callum J Dickson, Camilo Velez-Vega, José S Duca, Josh V Vermaas, Yui Tik Pang, Atanu Acharya, Jerry M Parks, Jeremy C Smith, James C Gumbart
PMCID: PMC7491520  PMID: 32935106

Abstract

The main protease (M pro ) of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is an attractive target for antiviral therapeutics. Recently, many high-resolution apo and inhibitor-bound structures of M pro , a cysteine protease, have been determined, facilitating structure-based drug design. M pro plays a central role in the viral life cycle by catalyzing the cleavage of SARS-CoV-2 polyproteins. In addition to the catalytic dyad His41-Cys145, M pro contains multiple histidines including His163, His164, and His172. The protonation states of these histidines and the catalytic nu-cleophile Cys145 have been debated in previous studies of SARS-CoV M pro , but have yet to be investigated for SARS-CoV-2. In this work we have used molecular dynamics simulations to determine the structural stability of SARS-CoV-2 M pro as a function of the protonation assignments for these residues. We simulated both the apo and inhibitor-bound enzyme and found that the conformational stability of the binding site, bound inhibitors, and the hydrogen bond networks of M pro are highly sensitive to these assignments. Additionally, the two inhibitors studied, the peptidomimetic N3 and an α -ketoamide, display distinct His41/His164 protonation-state-dependent stabilities. While the apo and the N3-bound systems favored N δ (HD) and N ϵ (HE) protonation of His41 and His164, respectively, the α -ketoamide was not stably bound in this state. Our results illustrate the importance of using appropriate histidine protonation states to accurately model the structure and dynamics of SARS-CoV-2 M pro in both the apo and inhibitor-bound states, a necessary prerequisite for drug-design efforts.

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