A mosquito salivary protein-driven influx of myeloid cells facilitates flavivirus transmission

EMBO J. 2024 May;43(9):1690-1721. doi: 10.1038/s44318-024-00056-x. Epub 2024 Feb 20.

Abstract

Mosquitoes transmit many disease-relevant flaviviruses. Efficient viral transmission to mammalian hosts requires mosquito salivary factors. However, the specific salivary components facilitating viral transmission and their mechanisms of action remain largely unknown. Here, we show that a female mosquito salivary gland-specific protein, here named A. aegypti Neutrophil Recruitment Protein (AaNRP), facilitates the transmission of Zika and dengue viruses. AaNRP promotes a rapid influx of neutrophils, followed by virus-susceptible myeloid cells toward mosquito bite sites, which facilitates establishment of local infection and systemic dissemination. Mechanistically, AaNRP engages TLR1 and TLR4 of skin-resident macrophages and activates MyD88-dependent NF-κB signaling to induce the expression of neutrophil chemoattractants. Inhibition of MyD88-NF-κB signaling with the dietary phytochemical resveratrol reduces AaNRP-mediated enhancement of flavivirus transmission by mosquitoes. These findings exemplify how salivary components can aid viral transmission, and suggest a potential prophylactic target.

Keywords: Flavivirus; Mosquito salivary protein; NF-κB; Neutrophil; Toll-like receptor.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Aedes* / metabolism
  • Aedes* / virology
  • Animals
  • Dengue / metabolism
  • Dengue / transmission
  • Dengue / virology
  • Dengue Virus / physiology
  • Female
  • Insect Proteins / metabolism
  • Mice
  • Mosquito Vectors / virology
  • Myeloid Cells / metabolism
  • Myeloid Cells / virology
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / metabolism
  • NF-kappa B / metabolism
  • Salivary Proteins and Peptides / metabolism
  • Signal Transduction
  • Zika Virus Infection / metabolism
  • Zika Virus Infection / transmission
  • Zika Virus Infection / virology
  • Zika Virus* / physiology

Substances

  • Salivary Proteins and Peptides
  • Insect Proteins
  • NF-kappa B
  • Myeloid Differentiation Factor 88