Molecular Editing Enhances Oxidation Resistance of Menaquinone-Targeting Antibiotics Lysocin E and WAP-8294A2

Chemistry. 2023 Aug 21;29(47):e202301224. doi: 10.1002/chem.202301224. Epub 2023 Jul 27.

Abstract

Lysocin E (1 a) and WAP-8294A2 (2 a) are peptidic natural products with 37- and 40-membered macrocycles, respectively. Compounds 1 a and 2 a have potent antibacterial activities against Gram-positive bacteria and share a unique mode of action. The electron-rich indole ring of d-Trp-10 of 1 a and 2 a interacts with the electron-deficient benzoquinone ring of menaquinone, which is a co-enzyme in the bacterial respiratory chain. Formation of the electron-donor-acceptor complex causes membrane disruption, leading to cell death. Despite the promising activities of 1 a and 2 a, the susceptibility of Trp-10 to oxidative degradation potentially deters the development of these compounds as antibacterial drugs. To address this issue, we replaced the indole ring with more oxidation-resistant aromatics having a similar shape and electron-rich character. Specifically, analogues with benzofuran (1 b/2 b), benzothiophene (1 c/2 c), and 1-naphthalene (1 d/2 d) rings were designed, and chemically prepared by full solid-phase total syntheses. Antibacterial assays of the six analogues revealed similar activities of 1 d/2 d and markedly reduced activities of 1 b/2 b and 1 c/2 c compared with 1 a/2 a. Equipotent 1 d and 2 d both showed high resistance to oxidation by peroxyl radicals. Hence, the present study demonstrates a new molecular editing strategy for conferring oxidation stability on natural products with pharmacologically useful functions.

Keywords: antibiotics; macrocycles; peptides; reactive oxygen species; structure-activity relationships.

MeSH terms

  • Anti-Bacterial Agents* / chemistry
  • Biological Products*
  • Microbial Sensitivity Tests
  • Vitamin K 2

Substances

  • Anti-Bacterial Agents
  • lysocin E
  • lotilibcin
  • Vitamin K 2
  • Biological Products