Structural characterization and bioactivity profiling of the fungal peptaibiotic tolypin reveal protective effects against influenza viruses

Arch Pharm (Weinheim). 2024 Oct;357(10):e2400384. doi: 10.1002/ardp.202400384. Epub 2024 Jul 19.

Abstract

In a bioprospection for new antivirals, we tested nonribosomally biosynthesized polypeptide antibiotics in MDCK II cells for their actions on influenza A and B viruses (IAV/IBV). Only tolypin, a mixture of closely related 16-residue peptaibiotics from the fungus Tolypocladium inflatum IE 1897, showed promising activity. It was selected for further investigation and structural characterization by ultrahigh performance liquid chromatography coupled to high-resolution mass spectrometry (UHPLC-HR-MS/MS) and ultrahigh performance liquid chromatography coupled to in-source collision-induced dissociation tandem mass spectrometry (UHPLC-isCID-HR-MS/MS), revealing 12 partially co-eluting individual peptides that were fully sequenced. Since tolypin-related efrapeptins are potent inhibitors of F1/Fo-ATPase, we screened tolypin for its toxicity against MDCK II cells and larvae of the greater wax moth Galleria mellonella. We found that a nontoxic concentration of tolypin (1 µg/mL) reduced the titer of two IBV strains by 4-5 log values, and that of an H3N2 strain by 1-2 log values, but the H1N1pdm strain was not affected. The higher concentrations of tolypin were cytostatic to MDCK II cells, shifted their metabolism from oxidative phosphorylation to glycolysis, and induced paralysis in G. mellonella, supporting the inhibition of F1/Fo-ATPase as the mode of action. Our results lay the foundations for future work to investigate the interplay between viral replication and cellular energy metabolism, as well as the development of drugs that target host factors.

Keywords: Tolypocladium; UHPLC‐HR‐MS/MS; cellular energy metabolism; influenza virus; microheterogeneity.

MeSH terms

  • Animals
  • Antiviral Agents* / chemistry
  • Antiviral Agents* / pharmacology
  • Chromatography, High Pressure Liquid
  • Dogs
  • Dose-Response Relationship, Drug
  • Hypocreales / chemistry
  • Influenza A Virus, H1N1 Subtype / drug effects
  • Influenza A Virus, H3N2 Subtype / drug effects
  • Influenza A virus / drug effects
  • Influenza B virus* / drug effects
  • Larva / drug effects
  • Madin Darby Canine Kidney Cells
  • Moths / drug effects
  • Moths / virology
  • Peptaibols / chemistry
  • Peptaibols / pharmacology
  • Structure-Activity Relationship
  • Tandem Mass Spectrometry

Substances

  • Antiviral Agents
  • Peptaibols