Journal Article

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

Oliva Chávez, Adela S., Scoles, Glen A., Kotsyfakis, Michail, Neal, Anya J. O, Valenzuela, Jesus G., Sztein, Marcelo B., Sonenshine, Daniel E., Ford, Shelby L., Jay, Steven M., Butler, L. Rainer, Shahi, Preeti, Miller, Lloyd S., Marnin, Liron, Barry, Eileen M., Shaw, Dana K., Tully, Brenden G., Mamoun, Choukri Ben, Pasetti, Marcela F., Pal, Utpal, Carroll, Erin E. McClure, Mason, Kathleen L., Buskirk, Amanda D., Wang, Xiaowei, Santambrogio, Laura, Archer, Nathan K., Morozova, Kateryna, Clement, Cristina C., Lawres, Lauren, Huntley, Jason F., Pedra, Joao H. F., Hobbs, Brandi E., Hammond, Holly L., Levin, Michael L.

2021

Overview

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. Extracellular vesicles have been implicated in the transmission of pathogens from the arthropod to the human host. Here the authors show that tick-derived extracellular vesicles play a role in feeding and modulate the outcome of bacterial infection.

• Publisher: Nature Publishing Group UK,Nature Publishing Group,Nature Portfolio
• Subject: 101/28 / 101/58 / 13/1 / 13/106 / 13/21 / 13/31 / 13/89 / 13/95 / 14 / 14/19 / 14/34 / 14/63 / 38 / 42 / 631/250/255 / 631/326/41 / 631/326/421 / 631/601/1466 / 64 / 64/60 / 96 / 96/95 / Anaplasma phagocytophilum / Anaplasma phagocytophilum - pathogenicity / Animals / Arthropoda / Arthropods / Arthropods - metabolism / Arthropods - microbiology / Arthropods - physiology / Bacteria / Bacterial diseases / Bacterial infections / Bacterial Infections - immunology / Bacterial Infections - metabolism / Bacterial vesicles / Cell Line / Dermacentor - metabolism / Dermacentor - microbiology / Dermacentor - physiology / Dermacentor andersoni / ecosystems / exosomes / Extracellular vesicles / Extracellular Vesicles - metabolism / Extracellular Vesicles - ultrastructure / Feeding / Francisella tularensis / Francisella tularensis - pathogenicity / Gene Ontology / hematophagy / homeostasis / Humanities and Social Sciences / Humans / immunity / Infections / Infectious diseases / inflammation / Inflammation - immunology / Inflammation - metabolism / Inflammation - parasitology / Intravital Microscopy / Ixodes - metabolism / Ixodes - microbiology / Ixodes - physiology / Ixodes scapularis / Lymphocytes / Lymphocytes T / Male / mammals / Mice / Mice, Inbred C57BL / Mice, Knockout / Microorganisms / Microscopy, Electron, Transmission / morbidity / mortality / multidisciplinary / Pathogens / Proteomics / R-SNARE Proteins - metabolism / Science / Science (multidisciplinary) / Skin - immunology / Skin - microbiology / Skin - parasitology / SNAP receptors / Synaptobrevin / T-Lymphocytes - metabolism / Tandem Mass Spectrometry / ticks / Ticks - metabolism / Ticks - microbiology / Vector-borne diseases / Vesicle-Associated Membrane Protein 2 - metabolism / Vesicles / virulence