Synthetic group A streptogramin antibiotics that overcome Vat resistance

Nature. 2020 Oct;586(7827):145-150. doi: 10.1038/s41586-020-2761-3. Epub 2020 Sep 23.

Abstract

Natural products serve as chemical blueprints for most antibiotics in clinical use. The evolutionary process by which these molecules arise is inherently accompanied by the co-evolution of resistance mechanisms that shorten the clinical lifetime of any given class of antibiotics1. Virginiamycin acetyltransferase (Vat) enzymes are resistance proteins that provide protection against streptogramins2, potent antibiotics against Gram-positive bacteria that inhibit the bacterial ribosome3. Owing to the challenge of selectively modifying the chemically complex, 23-membered macrocyclic scaffold of group A streptogramins, analogues that overcome the resistance conferred by Vat enzymes have not been previously developed2. Here we report the design, synthesis, and antibacterial evaluation of group A streptogramin antibiotics with extensive structural variability. Using cryo-electron microscopy and forcefield-based refinement, we characterize the binding of eight analogues to the bacterial ribosome at high resolution, revealing binding interactions that extend into the peptidyl tRNA-binding site and towards synergistic binders that occupy the nascent peptide exit tunnel. One of these analogues has excellent activity against several streptogramin-resistant strains of Staphylococcus aureus, exhibits decreased rates of acetylation in vitro, and is effective at lowering bacterial load in a mouse model of infection. Our results demonstrate that the combination of rational design and modular chemical synthesis can revitalize classes of antibiotics that are limited by naturally arising resistance mechanisms.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acetylation / drug effects
  • Acetyltransferases / genetics
  • Acetyltransferases / metabolism
  • Animals
  • Anti-Bacterial Agents / chemical synthesis*
  • Anti-Bacterial Agents / classification
  • Anti-Bacterial Agents / pharmacology*
  • Bacterial Load / drug effects
  • Binding Sites
  • Cryoelectron Microscopy
  • Drug Design*
  • Drug Resistance, Bacterial / drug effects*
  • Female
  • In Vitro Techniques
  • Mice
  • Microbial Sensitivity Tests
  • Models, Molecular
  • RNA, Transfer / metabolism
  • Ribosomes / drug effects
  • Ribosomes / metabolism
  • Staphylococcus aureus / drug effects
  • Staphylococcus aureus / genetics
  • Staphylococcus aureus / metabolism
  • Streptogramin Group A / chemical synthesis*
  • Streptogramin Group A / chemistry
  • Streptogramin Group A / classification
  • Streptogramin Group A / pharmacology*
  • Virginiamycin / analogs & derivatives
  • Virginiamycin / chemistry
  • Virginiamycin / metabolism

Substances

  • Anti-Bacterial Agents
  • Streptogramin Group A
  • Virginiamycin
  • RNA, Transfer
  • Acetyltransferases
  • virginiamycin acetyltransferase D