Structure-guided development of selective caseinolytic protease P agonists as antistaphylococcal agents

Cell Rep Med. 2024 Dec 17;5(12):101837. doi: 10.1016/j.xcrm.2024.101837. Epub 2024 Nov 29.

Abstract

Methicillin-resistant Staphylococcus aureus is a ubiquitous pathogen, posing a serious threat to human health worldwide. Thus, there is a high demand for antibiotics with distinct targets. Caseinolytic protease P (ClpP) is a promising target for combating staphylococcal infections; however, selectively activating S. aureus ClpP (SaClpP) rather than Homo sapiens ClpP (HsClpP) remains challenging. Herein, we rationally design and identify ZG297 by structure-based strategy. It binds and activates SaClpP instead of HsClpP. This is due to differentiated ligand binding attributed to crossed "tyrosine/histidine" amino acid pairs. ZG297 substantially inhibits the growth of a broad panel of S. aureus strains in vitro, outperforming the selective (R)-ZG197 agonist. ZG297 also functions as a potent antibiotic against multidrug-resistant S. aureus infections in Galleria mellonella larvae, zebrafish, murine skin, and thigh infection models. Collectively, we demonstrate that ZG297 is a safer and more potent antistaphylococcal agent than acyldepsipeptide 4 and (R)-ZG197.

Keywords: ClpP; MRSA; ZG297; antibiotic; antistaphylococcal agents; caseinolytic protease P; methicillin-resistant Staphylococcus aureus; murine skin infection model; murine thigh infection model; selective agonist; structure guided design; tyrosine/histidine pairs.

MeSH terms

  • Animals
  • Anti-Bacterial Agents* / pharmacology
  • Bacterial Proteins / metabolism
  • Endopeptidase Clp* / metabolism
  • Humans
  • Methicillin-Resistant Staphylococcus aureus / drug effects
  • Mice
  • Microbial Sensitivity Tests
  • Moths / microbiology
  • Staphylococcal Infections* / drug therapy
  • Staphylococcal Infections* / microbiology
  • Staphylococcus aureus / drug effects
  • Structure-Activity Relationship
  • Zebrafish*

Substances

  • Endopeptidase Clp
  • Anti-Bacterial Agents
  • Bacterial Proteins