Pan-serotype dengue virus inhibitor JNJ-A07 targets NS4A-2K-NS4B interaction with NS2B/NS3 and blocks replication organelle formation

Nat Commun. 2024 Jul 19;15(1):6080. doi: 10.1038/s41467-024-50437-3.

Abstract

Dengue fever represents a significant medical and socio-economic burden in (sub)tropical regions, yet antivirals for treatment or prophylaxis are lacking. JNJ-A07 was described as highly active against the different genotypes within each serotype of the disease-causing dengue virus (DENV). Based on clustering of resistance mutations it has been assumed to target DENV non-structural protein 4B (NS4B). Using a photoaffinity labeling compound with high structural similarity to JNJ-A07, here we demonstrate binding to NS4B and its precursor NS4A-2K-NS4B. Consistently, we report recruitment of the compound to intracellular sites enriched for these proteins. We further specify the mechanism-of-action of JNJ-A07, which has virtually no effect on viral polyprotein cleavage, but targets the interaction between the NS2B/NS3 protease/helicase complex and the NS4A-2K-NS4B cleavage intermediate. This interaction is functionally linked to de novo formation of vesicle packets (VPs), the sites of DENV RNA replication. JNJ-A07 blocks VPs biogenesis with little effect on established ones. A similar mechanism-of-action was found for another NS4B inhibitor, NITD-688. In summary, we unravel the antiviral mechanism of these NS4B-targeting molecules and show how DENV employs a short-lived cleavage intermediate to carry out an early step of the viral life cycle.

MeSH terms

  • Aminophenols
  • Animals
  • Antiviral Agents* / pharmacology
  • Butyrates
  • DEAD-box RNA Helicases
  • Dengue Virus* / drug effects
  • Dengue Virus* / genetics
  • Dengue Virus* / physiology
  • Dengue* / drug therapy
  • Dengue* / virology
  • Humans
  • Indoles
  • Membrane Proteins
  • Nucleoside-Triphosphatase
  • Organelles / drug effects
  • Organelles / metabolism
  • Protein Binding
  • RNA Helicases / antagonists & inhibitors
  • RNA Helicases / genetics
  • RNA Helicases / metabolism
  • Serine Endopeptidases / genetics
  • Serine Endopeptidases / metabolism
  • Serogroup
  • Viral Nonstructural Proteins* / antagonists & inhibitors
  • Viral Nonstructural Proteins* / genetics
  • Viral Nonstructural Proteins* / metabolism
  • Viral Proteases
  • Virus Replication* / drug effects

Substances

  • Viral Nonstructural Proteins
  • Antiviral Agents
  • RNA Helicases
  • Serine Endopeptidases
  • NS4B protein, Dengue virus
  • NS4A protein, Dengue virus
  • NS2B protein, flavivirus
  • NS3 protein, flavivirus
  • NS3 protease, dengue virus
  • nonstructural protein 2B, Dengue virus
  • (+)-4-(3-((1-(4-chlorophenyl)-2-oxo2-(6-(trifluoromethoxy)indolin-1-yl)ethyl)amino)-5-methoxyphenoxy)butanoic acid
  • Viral Proteases
  • Aminophenols
  • Membrane Proteins
  • Indoles
  • DEAD-box RNA Helicases
  • Nucleoside-Triphosphatase
  • Butyrates