Identification and characterization of carbapenem binding sites within the RND-transporter AcrB

Biochim Biophys Acta Biomembr. 2019 Jan;1861(1):62-74. doi: 10.1016/j.bbamem.2018.10.012. Epub 2018 Oct 26.

Abstract

Understanding the molecular determinants for recognition, binding and transport of antibiotics by multidrug efflux systems is important for basic research and useful for the design of more effective antimicrobial compounds. Imipenem and meropenem are two carbapenems whose antibacterial activity is known to be poorly and strongly affected by MexAB-OprM, the major efflux pump transporter in Pseudomonas aeruginosa. However, not much is known regarding recognition and transport of these compounds by AcrAB-TolC, which is the MexAB-OprM homologue in Escherichia coli and by definition the paradigm model for structural studies on efflux pumps. Prompted by this motivation, we unveiled the molecular details of the interaction of imipenem and meropenem with the transporter AcrB by combining computer simulations with biophysical experiments. Regarding the interaction with the two main substrate binding regions of AcrB, the so-called access and deep binding pockets, molecular dynamics simulations revealed imipenem to be more mobile than meropenem in the former, while comparable mobilities were observed in the latter. This result is in line with isothermal titration calorimetry, differential scanning experiments, and binding free energy calculations, indicating a higher affinity for meropenem than imipenem at the deep binding pocket, while both sharing similar affinities at the access pocket. Our findings rationalize how different physico-chemical properties of compounds reflect on their interactions with AcrB. As such, they constitute precious information to be exploited for the rational design of antibiotics able to evade efflux pumps.

Keywords: AcrB; Differential scanning experiments; Free energy calculations; Isothermal titration calorimetry; Molecular dynamics simulations; Multi-drug resistance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Bacterial Agents / pharmacology
  • Bacterial Outer Membrane Proteins / chemistry
  • Binding Sites
  • Biological Transport
  • Calorimetry, Differential Scanning
  • Carbapenems / chemistry*
  • Drug Resistance, Multiple, Bacterial / drug effects
  • Escherichia coli / chemistry*
  • Escherichia coli Proteins / chemistry*
  • Microbial Sensitivity Tests
  • Molecular Conformation
  • Molecular Docking Simulation
  • Molecular Dynamics Simulation
  • Multidrug Resistance-Associated Proteins / chemistry*
  • Protein Binding
  • Thermodynamics

Substances

  • AcrB protein, E coli
  • Anti-Bacterial Agents
  • Bacterial Outer Membrane Proteins
  • Carbapenems
  • Escherichia coli Proteins
  • Multidrug Resistance-Associated Proteins