Potentiation of β-lactam antibiotics and β-lactam/β-lactamase inhibitor combinations against MDR and XDR Pseudomonas aeruginosa using non-ribosomal tobramycin-cyclam conjugates

J Antimicrob Chemother. 2019 Sep 1;74(9):2640-2648. doi: 10.1093/jac/dkz228.

Abstract

Objectives: To develop a multifunctional adjuvant molecule that can rescue β-lactam antibiotics and β-lactam/β-lactamase inhibitor combinations from resistance in carbapenem-resistant Pseudomonas aeruginosa clinical isolates.

Methods: Preparation of adjuvant was guided by structure-activity relationships, following standard protocols. Susceptibility and chequerboard studies were assessed using serial 2-fold dilution assays. Toxicity was evaluated against porcine erythrocytes, human embryonic kidney (HEK293) cells and liver carcinoma (HepG2) cells via MTS assay. Preliminary in vivo efficacy was evaluated using a Galleria mellonella infection model.

Results: Conjugation of tobramycin and cyclam abrogates the ribosomal effects of tobramycin but confers a potent adjuvant property that restores full antibiotic activity of meropenem and aztreonam against carbapenem-resistant P. aeruginosa. Therapeutic levels of susceptibility, as determined by CLSI susceptibility breakpoints, were attained in several MDR clinical isolates, and time-kill assays revealed a synergistic dose-dependent pharmacodynamic relationship. A triple combination of the adjuvant with ceftazidime/avibactam (approved), aztreonam/avibactam (Phase III) and meropenem/avibactam enhances the efficacies of β-lactam/β-lactamase inhibitors against recalcitrant strains, suggesting rapid access of the combination to their periplasmic targets. The newly developed adjuvants, and their combinations, were non-haemolytic and non-cytotoxic, and preliminary in vivo evaluation in G. mellonella suggests therapeutic potential for the double and triple combinations.

Conclusions: Non-ribosomal tobramycin-cyclam conjugate mitigates the effect of OprD/OprF porin loss in P. aeruginosa and potentiates β-lactam/β-lactamase inhibitors against carbapenem-resistant clinical isolates, highlighting the complexity of resistance to β-lactam antibiotics. Our strategy presents an avenue to further preserve the therapeutic utility of β-lactam antibiotics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adjuvants, Pharmaceutic / chemistry
  • Adjuvants, Pharmaceutic / therapeutic use
  • Animals
  • Anti-Bacterial Agents / chemistry
  • Anti-Bacterial Agents / therapeutic use*
  • Azabicyclo Compounds / chemistry
  • Azabicyclo Compounds / therapeutic use
  • Carbapenems / chemistry
  • Carbapenems / therapeutic use
  • Ceftazidime / chemistry
  • Ceftazidime / therapeutic use
  • Drug Combinations
  • Erythrocytes
  • HEK293 Cells
  • Heterocyclic Compounds / chemistry
  • Heterocyclic Compounds / therapeutic use*
  • Humans
  • Pseudomonas Infections / drug therapy*
  • Pseudomonas Infections / microbiology
  • Pseudomonas aeruginosa / drug effects*
  • Pseudomonas aeruginosa / enzymology
  • Swine
  • Tobramycin / chemistry
  • Tobramycin / therapeutic use*
  • beta-Lactamase Inhibitors / chemistry
  • beta-Lactamase Inhibitors / therapeutic use*

Substances

  • Adjuvants, Pharmaceutic
  • Anti-Bacterial Agents
  • Azabicyclo Compounds
  • Carbapenems
  • Drug Combinations
  • Heterocyclic Compounds
  • avibactam, ceftazidime drug combination
  • beta-Lactamase Inhibitors
  • cyclam
  • Ceftazidime
  • Tobramycin