Tick extracellular vesicles enable arthropod feeding and promote distinct outcomes of bacterial infection

Nat Commun. 2021 Jun 17;12(1):3696. doi: 10.1038/s41467-021-23900-8.

Abstract

Extracellular vesicles are thought to facilitate pathogen transmission from arthropods to humans and other animals. Here, we reveal that pathogen spreading from arthropods to the mammalian host is multifaceted. Extracellular vesicles from Ixodes scapularis enable tick feeding and promote infection of the mildly virulent rickettsial agent Anaplasma phagocytophilum through the SNARE proteins Vamp33 and Synaptobrevin 2 and dendritic epidermal T cells. However, extracellular vesicles from the tick Dermacentor andersoni mitigate microbial spreading caused by the lethal pathogen Francisella tularensis. Collectively, we establish that tick extracellular vesicles foster distinct outcomes of bacterial infection and assist in vector feeding by acting on skin immunity. Thus, the biology of arthropods should be taken into consideration when developing strategies to control vector-borne diseases.

Publication types

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

MeSH terms

  • Anaplasma phagocytophilum / pathogenicity
  • Animals
  • Arthropods / metabolism
  • Arthropods / microbiology
  • Arthropods / physiology
  • Bacterial Infections / immunology*
  • Bacterial Infections / metabolism*
  • Cell Line
  • Dermacentor / metabolism
  • Dermacentor / microbiology
  • Dermacentor / physiology
  • Extracellular Vesicles / metabolism*
  • Extracellular Vesicles / ultrastructure
  • Francisella tularensis / pathogenicity
  • Gene Ontology
  • Humans
  • Inflammation / immunology
  • Inflammation / metabolism
  • Inflammation / parasitology
  • Intravital Microscopy
  • Ixodes / metabolism
  • Ixodes / microbiology
  • Ixodes / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Electron, Transmission
  • Proteomics
  • R-SNARE Proteins / metabolism
  • Skin / immunology
  • Skin / microbiology
  • Skin / parasitology*
  • T-Lymphocytes / metabolism
  • Tandem Mass Spectrometry
  • Ticks / metabolism*
  • Ticks / microbiology*
  • Vesicle-Associated Membrane Protein 2 / metabolism

Substances

  • R-SNARE Proteins
  • Vesicle-Associated Membrane Protein 2