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

Adela S. Oliva Chávez, Xiaowei Wang, Liron Marnin, Nathan K. Archer, Holly L. Hammond, Erin E. McClure Carroll, Dana K. Shaw, Brenden G. Tully, Amanda D. Buskirk, Shelby L. Ford, L. Rainer Butler, Preeti Shahi, Kateryna Morozova, Cristina C. Clement, Lauren Lawres, Anya J. O’ Neal, Choukri Ben Mamoun, Kathleen L. Mason, Brandi E. Hobbs, Glen A. Scoles, Eileen M. Barry, Daniel E. Sonenshine, Utpal Pal, Jesus G. Valenzuela, Marcelo B. Sztein, Marcela F. Pasetti, Michael L. Levin, Michail Kotsyfakis, Steven M. Jay, Jason F. Huntley, Lloyd S. Miller, Laura Santambrogio and Joao H. F. Pedra ()
Additional contact information
Adela S. Oliva Chávez: University of Maryland School of Medicine
Xiaowei Wang: University of Maryland School of Medicine
Liron Marnin: University of Maryland School of Medicine
Nathan K. Archer: Johns Hopkins University School of Medicine
Holly L. Hammond: University of Maryland School of Medicine
Erin E. McClure Carroll: University of Maryland School of Medicine
Dana K. Shaw: University of Maryland School of Medicine
Brenden G. Tully: University of Toledo College of Medicine and Life Sciences
Amanda D. Buskirk: University of Maryland School of Medicine
Shelby L. Ford: Centers for Disease Control and Prevention
L. Rainer Butler: University of Maryland School of Medicine
Preeti Shahi: University of Maryland School of Medicine
Kateryna Morozova: Albert Einstein College of Medicine
Cristina C. Clement: Albert Einstein College of Medicine
Lauren Lawres: Yale University School of Medicine
Anya J. O’ Neal: University of Maryland School of Medicine
Choukri Ben Mamoun: Yale University School of Medicine
Kathleen L. Mason: USDA, ARS, Animal Disease Research Unit, Washington State University
Brandi E. Hobbs: University of Maryland School of Medicine
Glen A. Scoles: USDA, ARS, Animal Disease Research Unit, Washington State University
Eileen M. Barry: University of Maryland School of Medicine
Daniel E. Sonenshine: National Institutes of Health
Utpal Pal: University of Maryland
Jesus G. Valenzuela: National Institutes of Health
Marcelo B. Sztein: University of Maryland School of Medicine
Marcela F. Pasetti: University of Maryland School of Medicine
Michael L. Levin: Centers for Disease Control and Prevention
Michail Kotsyfakis: Biology Center of the Czech Academy of Sciences
Steven M. Jay: University of Maryland
Jason F. Huntley: University of Toledo College of Medicine and Life Sciences
Lloyd S. Miller: Johns Hopkins University School of Medicine
Laura Santambrogio: Albert Einstein College of Medicine
Joao H. F. Pedra: University of Maryland School of Medicine

Nature Communications, 2021, vol. 12, issue 1, 1-17

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-23900-8

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