Chrysophaentins are competitive inhibitors of FtsZ and inhibit Z-ring formation in live bacteria

Bioorg Med Chem. 2013 Sep 15;21(18):5673-8. doi: 10.1016/j.bmc.2013.07.033. Epub 2013 Jul 25.

Abstract

The bacterial cell division protein FtsZ polymerizes in a GTP-dependent manner to form a Z-ring that marks the plane of division. As a validated antimicrobial target, considerable efforts have been devoted to identify small molecule FtsZ inhibitors. We recently discovered the chrysophaentins, a novel suite of marine natural products that inhibit FtsZ activity in vitro. These natural products along with a synthetic hemi-chrysophaentin exhibit strong antimicrobial activity toward a broad spectrum of Gram-positive pathogens. To define their mechanisms of FtsZ inhibition and determine their in vivo effects in live bacteria, we used GTPase assays and fluorescence anisotropy to show that hemi-chrysophaentin competitively inhibits FtsZ activity. Furthermore, we developed a model system using a permeable Escherichia coli strain, envA1, together with an inducible FtsZ-yellow fluorescent protein construct to show by fluorescence microscopy that both chrysophaentin A and hemi-chrysophaentin disrupt Z-rings in live bacteria. We tested the E. coli system further by reproducing phenotypes observed for zantrins Z1 and Z3, and demonstrate that the alkaloid berberine, a reported FtsZ inhibitor, exhibits auto-fluorescence, making it incompatible with systems that employ GFP or YFP tagged FtsZ. These studies describe unique examples of nonnucleotide, competitive FtsZ inhibitors that disrupt FtsZ in vivo, together with a model system that should be useful for in vivo testing of FtsZ inhibitor leads that have been identified through in vitro screens but are unable to penetrate the Gram-negative outer membrane.

Keywords: Antibiotics; Bacterial cytoskeleton; Drug resistant bacteria; Natural products.

Publication types

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

MeSH terms

  • Amidohydrolases / genetics
  • Amidohydrolases / metabolism
  • Anti-Bacterial Agents / chemistry*
  • Anti-Bacterial Agents / isolation & purification
  • Anti-Bacterial Agents / pharmacology
  • Bacterial Proteins / antagonists & inhibitors*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Benzyl Compounds / chemical synthesis
  • Benzyl Compounds / chemistry*
  • Benzyl Compounds / isolation & purification
  • Benzyl Compounds / pharmacology
  • Berberine / chemistry
  • Berberine / pharmacology
  • Cytoskeletal Proteins / antagonists & inhibitors*
  • Cytoskeletal Proteins / metabolism
  • Escherichia coli / drug effects
  • Escherichia coli / metabolism
  • Ethers, Cyclic / chemistry*
  • Ethers, Cyclic / isolation & purification
  • Ethers, Cyclic / pharmacology
  • GTP Phosphohydrolases / metabolism
  • Gram-Positive Bacteria / drug effects
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Microscopy, Fluorescence
  • Recombinant Fusion Proteins / biosynthesis
  • Recombinant Fusion Proteins / genetics

Substances

  • Anti-Bacterial Agents
  • Bacterial Proteins
  • Benzyl Compounds
  • Cytoskeletal Proteins
  • Ethers, Cyclic
  • FtsZ protein, Bacteria
  • Luminescent Proteins
  • Recombinant Fusion Proteins
  • chrysophaentin A
  • hemi-chrysophaetin
  • yellow fluorescent protein, Bacteria
  • Berberine
  • Amidohydrolases
  • UDP-3-O-acyl-N-acetylglucosamine deacetylase
  • GTP Phosphohydrolases