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

Author

Listed:
  • Adela S. Oliva Chávez

    (University of Maryland School of Medicine
    Texas A&M University)

  • 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
    Excerpta Medica)

  • Dana K. Shaw

    (University of Maryland School of Medicine
    Washington State University)

  • Brenden G. Tully

    (University of Toledo College of Medicine and Life Sciences)

  • Amanda D. Buskirk

    (University of Maryland School of Medicine
    Microbiology Assessment Branch III, U.S. Food and Drug Administration)

  • 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
    Weill Cornell 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
    USDA, ARS, Invasive Insect Biocontrol and Behavior Laboratory)

  • Eileen M. Barry

    (University of Maryland School of Medicine)

  • Daniel E. Sonenshine

    (National Institutes of Health
    Old Dominion University)

  • Utpal Pal

    (University of Maryland)

  • Jesus G. Valenzuela

    (National Institutes of Health)

  • Marcelo B. Sztein

    (University of Maryland School of Medicine
    University of Maryland School of Medicine
    University of Maryland School of Medicine)

  • Marcela F. Pasetti

    (University of Maryland School of Medicine
    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
    Janssen Research and Development)

  • Laura Santambrogio

    (Albert Einstein College of Medicine
    Weill Cornell Medicine)

  • Joao H. F. Pedra

    (University of Maryland School of Medicine)

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.

Suggested Citation

  • 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 B, 2021. "Tick extracellular vesicles enable arthropod feeding and promote distinct outcomes of bacterial infection," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-23900-8
    DOI: 10.1038/s41467-021-23900-8
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    Cited by:

    1. Agustin Rolandelli & Hanna J. Laukaitis-Yousey & Haikel N. Bogale & Nisha Singh & Sourabh Samaddar & Anya J. O’Neal & Camila R. Ferraz & Matthew Butnaru & Enzo Mameli & Baolong Xia & M. Tays Mendes & , 2024. "Tick hemocytes have a pleiotropic role in microbial infection and arthropod fitness," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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