A novel 12-membered ring non-antibiotic macrolide EM982 attenuates cytokine production by inhibiting IKKβ and IκBα phosphorylation

J Biol Chem. 2024 Jun;300(6):107384. doi: 10.1016/j.jbc.2024.107384. Epub 2024 May 16.

Abstract

Antimicrobial resistance poses a serious threat to human health worldwide and its incidence continues to increase owing to the overuse of antibiotics and other factors. Macrolide antibiotics such as erythromycin (EM) have immunomodulatory effects in addition to their antibacterial activity. Long-term, low-dose administration of macrolides has shown clinical benefits in treating non-infectious inflammatory respiratory diseases. However, this practice may also increase the emergence of drug-resistant bacteria. In this study, we synthesized a series of EM derivatives, and screened them for two criteria: (i) lack of antibacterial activity and (ii) ability to suppress tumor necrosis factor-α (TNF-α) production in THP-1 cells stimulated with lipopolysaccharide. Among the 37 synthesized derivatives, we identified a novel 12-membered ring macrolide EM982 that lacked antibacterial activity against Staphylococcus aureus and suppressed the production of TNF-α and other cytokines. The effects of EM982 on Toll-like receptor 4 (TLR4) signaling were analyzed using a reporter assay and Western blotting. The reporter assay showed that EM982 suppressed the activation of transcription factors, NF-κB and/or activator protein 1 (AP-1), in HEK293 cells expressing human TLR4. Western blotting showed that EM982 inhibited the phosphorylation of both IκB kinase (IKK) β and IκBα, which function upstream of NF-κB, whereas it did not affect the phosphorylation of p38 mitogen-activated protein kinase, extracellular signal-regulated kinase, and c-Jun N-terminal kinase, which act upstream of AP-1. These results suggest that EM982 suppresses cytokine production by inhibiting phosphorylation of IKKβ and IκBα, resulting in the inactivation of NF-κB.

Keywords: Toll-like receptor 4 (TLR4); antibiotics; cell signaling; drug development; immunosuppression; macrolide derivatives.

MeSH terms

  • Anti-Bacterial Agents / chemistry
  • Anti-Bacterial Agents / pharmacology
  • Cytokines* / metabolism
  • Erythromycin / chemistry
  • Erythromycin / pharmacology
  • Humans
  • I-kappa B Kinase* / metabolism
  • Macrolides / chemistry
  • Macrolides / pharmacology
  • NF-KappaB Inhibitor alpha* / metabolism
  • NF-kappa B / metabolism
  • Phosphorylation / drug effects
  • Signal Transduction / drug effects
  • Staphylococcus aureus / drug effects
  • THP-1 Cells
  • Toll-Like Receptor 4 / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • I-kappa B Kinase
  • NF-KappaB Inhibitor alpha
  • Cytokines
  • Erythromycin
  • Tumor Necrosis Factor-alpha
  • IKBKB protein, human
  • Anti-Bacterial Agents
  • Macrolides
  • NF-kappa B
  • Toll-Like Receptor 4
  • NFKBIA protein, human