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.Mc Clure 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; Joao H.F. Pedra

doi:10.1038/s41467-021-23900-8

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.Mc Clure 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. ScolesEileen 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, Joao H.F. Pedra

School of Medicine

Research output: Contribution to journal › Article › peer-review

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.

Original language	English (US)
Article number	3696
Journal	Nature communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-23900-8
State	Published - Dec 1 2021

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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Oliva Chávez, A. S., Wang, X., Marnin, L., Archer, N. K., Hammond, H. L., Carroll, E. E. M. C., Shaw, D. K., Tully, B. G., Buskirk, A. D., Ford, S. L., Butler, L. R., Shahi, P., Morozova, K., Clement, C. C., Lawres, L., Neal, A. J. O., Mamoun, C. B., Mason, K. L., Hobbs, B. E., ... Pedra, J. H. F. (2021). Tick extracellular vesicles enable arthropod feeding and promote distinct outcomes of bacterial infection. Nature communications, 12(1), Article 3696. https://doi.org/10.1038/s41467-021-23900-8

Oliva Chávez, AS, Wang, X, Marnin, L, Archer, NK, Hammond, HL, Carroll, EEMC, Shaw, DK, Tully, BG, Buskirk, AD, Ford, SL, Butler, LR, Shahi, P, Morozova, K, Clement, CC, Lawres, L, Neal, AJO, Mamoun, CB, Mason, KL, Hobbs, BE, Scoles, GA, Barry, EM, Sonenshine, DE, Pal, U, Valenzuela, JG, Sztein, MB, Pasetti, MF, Levin, ML, Kotsyfakis, M, Jay, SM, Huntley, JF, Miller, LS, Santambrogio, L & Pedra, JHF 2021, 'Tick extracellular vesicles enable arthropod feeding and promote distinct outcomes of bacterial infection', Nature communications, vol. 12, no. 1, 3696. https://doi.org/10.1038/s41467-021-23900-8

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title = "Tick extracellular vesicles enable arthropod feeding and promote distinct outcomes of bacterial infection",

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.",

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

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AU - Oliva Chávez, Adela S.

AU - Wang, Xiaowei

AU - Marnin, Liron

AU - Archer, Nathan K.

AU - Hammond, Holly L.

AU - Carroll, Erin E.Mc Clure

AU - Shaw, Dana K.

AU - Tully, Brenden G.

AU - Buskirk, Amanda D.

AU - Ford, Shelby L.

AU - Butler, L. Rainer

AU - Shahi, Preeti

AU - Morozova, Kateryna

AU - Clement, Cristina C.

AU - Lawres, Lauren

AU - Neal, Anya J.O’

AU - Mamoun, Choukri Ben

AU - Mason, Kathleen L.

AU - Hobbs, Brandi E.

AU - Scoles, Glen A.

AU - Barry, Eileen M.

AU - Sonenshine, Daniel E.

AU - Pal, Utpal

AU - Valenzuela, Jesus G.

AU - Sztein, Marcelo B.

AU - Pasetti, Marcela F.

AU - Levin, Michael L.

AU - Kotsyfakis, Michail

AU - Jay, Steven M.

AU - Huntley, Jason F.

AU - Miller, Lloyd S.

AU - Santambrogio, Laura

AU - Pedra, Joao H.F.

PY - 2021/12/1

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N2 - 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.

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

Abstract

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