Elucidating the inhibition of peptidoglycan biosynthesis in Staphylococcus aureus by albocycline, a macrolactone isolated from Streptomyces maizeus

Bioorg Med Chem. 2018 Jul 23;26(12):3453-3460. doi: 10.1016/j.bmc.2018.05.017. Epub 2018 May 24.

Abstract

Antibiotic resistance is a serious threat to global public health, and methicillin-resistant Staphylococcus aureus (MRSA) is a poignant example. The macrolactone natural product albocycline, derived from various Streptomyces strains, was recently identified as a promising antibiotic candidate for the treatment of both MRSA and vancomycin-resistant S. aureus (VRSA), which is another clinically relevant and antibiotic resistant strain. Moreover, it was hypothesized that albocycline's antimicrobial activity was derived from the inhibition of peptidoglycan (i.e., bacterial cell wall) biosynthesis. Herein, preliminary mechanistic studies are performed to test the hypothesis that albocycline inhibits MurA, the enzyme that catalyzes the first step of peptidoglycan biosynthesis, using a combination of biological assays alongside molecular modeling and simulation studies. Computational modeling suggests albocycline exists as two conformations in solution, and computational docking of these conformations to an ensemble of simulated receptor structures correctly predicted preferential binding to S. aureus MurA-the enzyme that catalyzes the first step of peptidoglycan biosynthesis-over Escherichia coli (E. coli) MurA. Albocycline isolated from the producing organism (Streptomyces maizeus) weakly inhibited S. aureus MurA (IC50 of 480 μM) but did not inhibit E. coli MurA. The antimicrobial activity of albocycline against resistant S. aureus strains was superior to that of vancomycin, preferentially inhibiting Gram-positive organisms. Albocycline was not toxic to human HepG2 cells in MTT assays. While these studies demonstrate that albocycline is a promising lead candidate against resistant S. aureus, taken together they suggest that MurA is not the primary target, and further work is necessary to identify the major biological target.

Keywords: Albocycline; MRSA; MurA; Peptidoglycan biosynthesis inhibition; VRSA.

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

  • Alkyl and Aryl Transferases / antagonists & inhibitors
  • Alkyl and Aryl Transferases / metabolism*
  • Bacterial Proteins / antagonists & inhibitors
  • Bacterial Proteins / metabolism*
  • Binding Sites
  • Cell Survival / drug effects
  • Drug Resistance, Bacterial / drug effects
  • Escherichia coli / enzymology
  • Hep G2 Cells
  • Humans
  • Inhibitory Concentration 50
  • Lactones / chemistry
  • Lactones / metabolism
  • Lactones / pharmacology
  • Methicillin-Resistant Staphylococcus aureus / drug effects
  • Microbial Sensitivity Tests
  • Molecular Docking Simulation
  • Peptidoglycan / biosynthesis*
  • Peptidoglycan / chemistry
  • Protein Binding
  • Protein Structure, Tertiary
  • Staphylococcus aureus / drug effects
  • Staphylococcus aureus / enzymology*
  • Streptomyces / chemistry*
  • Streptomyces / metabolism

Substances

  • Bacterial Proteins
  • Lactones
  • Peptidoglycan
  • albocycline
  • Alkyl and Aryl Transferases
  • UDP-N-acetylglucosamine 1-carboxyvinyltransferase