Structural insights into alterations in the substrate spectrum of serine-β-lactamase OXA-10 from Pseudomonas aeruginosa by single amino acid substitutions

Emerg Microbes Infect. 2024 Dec;13(1):2412631. doi: 10.1080/22221751.2024.2412631. Epub 2024 Oct 22.

Abstract

The extensive use of β-lactam antibiotics has led to significant resistance, primarily due to hydrolysis by β-lactamases. OXA class D β-lactamases can hydrolyze a wide range of β-lactam antibiotics, rendering many treatments ineffective. We investigated the effects of single amino acid substitutions in OXA-10 on its substrate spectrum. Broad-spectrum variants with point mutations were searched and biochemically verified. Three key residues, G157D, A124T, and N73S, were confirmed in the variants, and their crystal structures were determined. Based on an enzyme kinetics study, the hydrolytic activity against broad-spectrum cephalosporins, particularly ceftazidime, was significantly enhanced by the G157D mutation in loop 2. The A124T or N73S mutation close to loop 2 also resulted in higher ceftazidime activity. All structures of variants with point mutations in loop 2 or nearby exhibited increased loop 2 flexibility, which facilitated the binding of ceftazidime. These results highlight the effect of a single amino acid substitution in OXA-10 on broad-spectrum drug resistance. Structure-activity relationship studies will help us understand the drug resistance spectrum of β-lactamases, enhance the effectiveness of existing β-lactam antibiotics, and develop new drugs.

Keywords: OXA-10; broad-spectrum cephalosporins; single amino acid substitutions; substrate specificity; β-lactamase resistance.

MeSH terms

  • Amino Acid Substitution*
  • Anti-Bacterial Agents* / pharmacology
  • Ceftazidime / pharmacology
  • Cephalosporins / pharmacology
  • Crystallography, X-Ray
  • Humans
  • Hydrolysis
  • Kinetics
  • Microbial Sensitivity Tests
  • Models, Molecular
  • Point Mutation
  • Protein Conformation
  • Pseudomonas aeruginosa* / drug effects
  • Pseudomonas aeruginosa* / enzymology
  • Pseudomonas aeruginosa* / genetics
  • Structure-Activity Relationship
  • Substrate Specificity
  • beta-Lactamases* / chemistry
  • beta-Lactamases* / genetics
  • beta-Lactamases* / metabolism

Substances

  • beta-Lactamases
  • Anti-Bacterial Agents
  • beta-lactamase OXA-10
  • Ceftazidime
  • Cephalosporins

Grants and funding

This work was supported by the Bio & Medical Technology Development Program of the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (NRF-2021R1A2C3004826 and NRF-2017M3A9E4078017) and by the Science Research Center (SRC) of the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (RS-2024-00407469).