Design of novel and highly selective SARS-CoV-2 main protease inhibitors

Antimicrob Agents Chemother. 2024 Oct 8;68(10):e0056224. doi: 10.1128/aac.00562-24. Epub 2024 Sep 3.

Abstract

We have synthesized a novel and highly selective severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) main protease peptide mimetic inhibitor mimicking the replicase 1ab recognition sequence -Val-Leu-Gln- and utilizing a cysteine selective acyloxymethyl ketone as the electrophilic warhead to target the active site Cys145. Utilizing a constrained cyclic peptide that locks the conformation between the P3 (Val) and P2 (Leu) residues, we identified a highly selective inhibitor that fills the P2 pocket occupied by the leucine residue sidechain of PF-00835231 and the dimethyl-3-azabicyclo-hexane motif in nirmatrelvir (PF-07321332). This strategy resulted in potent and highly selective Mpro inhibitors without inhibiting essential host cathepsin cysteine or serine proteases. The lead prototype compound 1 (MPro IC50 = 230 ± 18 nM) also inhibits the replication of multiple SARS-CoV-2 variants in vitro, including SARS-CoV-2 variants of concern, and can synergize at lower concentrations with the viral RNA polymerase inhibitor, remdesivir, to inhibit replication. It also reduces SARS-CoV-2 replication in SARS-CoV-2 Omicron-infected Syrian golden hamsters without obvious toxicities, demonstrating in vivo efficacy. This novel lead structure provides the basis for optimization of improved agents targeting evolving SARS-CoV-2 drug resistance that can selectively act on Mpro versus host proteases and are less likely to have off-target effects due to non-specific targeting. Developing inhibitors against the active site of the main protease (Mpro), which is highly conserved across coronaviruses, is expected to impart a higher genetic barrier to evolving SARS-CoV-2 drug resistance. Drugs that selectively inhibit the viral Mpro are less likely to have off-target effects warranting efforts to improve this therapy.

Keywords: SARS-CoV-2; benzoxazepine; peptide mimetic; protease inhibitor.

MeSH terms

  • Adenosine Monophosphate* / analogs & derivatives
  • Adenosine Monophosphate* / pharmacology
  • Alanine / analogs & derivatives
  • Alanine / pharmacology
  • Animals
  • Antiviral Agents* / chemistry
  • Antiviral Agents* / pharmacology
  • Betacoronavirus / drug effects
  • COVID-19 / virology
  • COVID-19 Drug Treatment
  • Catalytic Domain
  • Chlorocebus aethiops
  • Coronavirus 3C Proteases* / antagonists & inhibitors
  • Cricetinae
  • Drug Design
  • Humans
  • Lactams
  • Leucine
  • Mesocricetus
  • Nitriles
  • Peptides, Cyclic / chemistry
  • Peptides, Cyclic / pharmacology
  • Proline
  • Protease Inhibitors* / chemistry
  • Protease Inhibitors* / pharmacology
  • SARS-CoV-2* / drug effects
  • Vero Cells
  • Viral Nonstructural Proteins / antagonists & inhibitors
  • Viral Nonstructural Proteins / metabolism
  • Virus Replication* / drug effects

Substances

  • Antiviral Agents
  • Protease Inhibitors
  • Coronavirus 3C Proteases
  • Adenosine Monophosphate
  • nirmatrelvir
  • Alanine
  • remdesivir
  • Peptides, Cyclic
  • Viral Nonstructural Proteins
  • Lactams
  • Leucine
  • Nitriles
  • Proline

Supplementary concepts

  • SARS-CoV-2 variants