Synthesis of Bisindole Alkaloids and Their Mode of Action against Methicillin-Resistant Staphylococcus Aureus

ACS Infect Dis. 2024 Jun 14;10(6):1958-1969. doi: 10.1021/acsinfecdis.3c00657. Epub 2024 Jun 6.

Abstract

About 100,000 deaths are attributed annually to infections with methicillin-resistant Staphylococcus aureus (MRSA) despite concerted efforts toward vaccine development and clinical trials involving several preclinically efficacious drug candidates. This necessitates the development of alternative therapeutic options against this drug-resistant bacterial pathogen. Using the Masuda borylation-Suzuki coupling (MBSC) sequence, we previously synthesized and modified naturally occurring bisindole alkaloids, alocasin A, hyrtinadine A and scalaradine A, resulting in derivatives showing potent in vitro and in vivo antibacterial efficacy. Here, we report on a modified one-pot MBSC protocol for the synthesis of previously reported and several undescribed N-tosyl-protected bisindoles with anti-MRSA activities and moderate cytotoxicity against human monocytic and kidney cell lines. In continuation of the mode of action investigation of the previously synthesized membrane-permeabilizing hit compounds, mechanistic studies reveal that bisindoles impact the cytoplasmic membrane of Gram-positive bacteria by promiscuously interacting with lipid II and membrane phospholipids while rapidly dissipating membrane potential. The bactericidal and lipid II-interacting lead compounds 5c and 5f might be interesting starting points for drug development in the fight against MRSA.

Keywords: MRSA; Masuda borylation-Suzuki coupling; Methicillin-resistant Staphylococcus aureus; antibacterial; bisindole; lipid II.

MeSH terms

  • Anti-Bacterial Agents* / chemical synthesis
  • Anti-Bacterial Agents* / chemistry
  • Anti-Bacterial Agents* / pharmacology
  • Cell Line
  • Humans
  • Indole Alkaloids* / chemical synthesis
  • Indole Alkaloids* / chemistry
  • Indole Alkaloids* / pharmacology
  • Indoles / chemical synthesis
  • Indoles / chemistry
  • Indoles / pharmacology
  • Methicillin-Resistant Staphylococcus aureus* / drug effects
  • Microbial Sensitivity Tests*
  • Molecular Structure
  • Staphylococcal Infections / drug therapy
  • Staphylococcal Infections / microbiology
  • Structure-Activity Relationship

Substances

  • Anti-Bacterial Agents
  • Indole Alkaloids
  • Indoles