Novel lipoglycopeptides as inhibitors of bacterial signal peptidase I

J Biol Chem. 2004 Aug 27;279(35):36250-8. doi: 10.1074/jbc.M405884200. Epub 2004 Jun 1.

Abstract

Signal peptidase (SPase) I is responsible for the cleavage of signal peptides of many secreted proteins in bacteria. Because of its unique physiological and biochemical properties, it serves as a potential target for development of novel antibacterial agents. In this study, we report the production, isolation, and structure determination of a family of structurally related novel lipoglycopeptides from a Streptomyces sp. as inhibitors of SPase I. Detailed spectroscopic analyses, including MS and NMR, revealed that these lipoglycopeptides share a common 14-membered cyclic peptide core, an acyclic tripeptide chain, and a deoxy-alpha-mannose sugar, but differ in the degree of oxidation of the N-methylphenylglycine residue and the length and branching of the fatty acyl chain. Biochemical analysis demonstrated that these peptides are potent and competitive inhibitors of SPase I with K(i) 50 to 158 nm. In addition, they showed modest antibacterial activity against a panel of pathogenic Gram-positive and Gram-negative bacteria with minimal inhibitory concentration of 8-64 microm against Streptococcus pneumonniae and 4-8 microm against Escherichia coli. Notably, they mechanistically blocked the protein secretion in whole cells as demonstrated by inhibiting beta-lactamase release from Staphylococcus aureus. Taken together, the present discovery of a family of novel lipoglycopeptides as potent inhibitors of bacterial SPase I may lead to the development of a novel class of broad-spectrum antibiotics.

MeSH terms

  • Binding, Competitive
  • Chromatography, High Pressure Liquid
  • Chromatography, Liquid
  • Escherichia coli / metabolism
  • Fermentation
  • Glycine / chemistry
  • Glycopeptides / chemistry
  • Glycopeptides / pharmacology*
  • Gram-Negative Bacteria / metabolism
  • Inhibitory Concentration 50
  • Kinetics
  • Magnetic Resonance Spectroscopy
  • Mass Spectrometry
  • Membrane Proteins / chemistry*
  • Models, Chemical
  • Peptides / chemistry
  • Protein Sorting Signals
  • Protons
  • Serine Endopeptidases / chemistry*
  • Spectrometry, Mass, Electrospray Ionization
  • Spectrophotometry
  • Staphylococcus aureus / metabolism
  • Streptococcus pneumoniae / metabolism
  • Streptomyces / metabolism
  • Time Factors
  • beta-Lactamases / metabolism

Substances

  • Glycopeptides
  • Membrane Proteins
  • Peptides
  • Protein Sorting Signals
  • Protons
  • Serine Endopeptidases
  • type I signal peptidase
  • beta-Lactamases
  • Glycine