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  4. CSF-contacting neurons respond to Streptococcus pneumoniae and promote host survival during central nervous system infection
 
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research article

CSF-contacting neurons respond to Streptococcus pneumoniae and promote host survival during central nervous system infection

Prendergast, Andrew E.
•
Jim, Kin Ki
•
Marnas, Hugo
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March 13, 2023
Current Biology

The pathogenic bacterium Streptococcus pneumoniae (S. pneumoniae) can invade the cerebrospinal fluid (CSF) and cause meningitis with devastating consequences. Whether and how sensory cells in the central nervous system (CNS) become activated during bacterial infection, as recently reported for the peripheral nervous system, is not known. We find that CSF infection by S. pneumoniae in larval zebrafish leads to changes in posture and behavior that are reminiscent of pneumococcal meningitis, including dorsal arching and epileptic-like seizures. We show that during infection, invasion of the CSF by S. pneumoniae massively activates in vivo sensory neurons contacting the CSF, referred to as "CSF-cNs"and previously shown to detect spinal curvature and to control posture, locomotion, and spine morphogenesis. We find that CSF-cNs express orphan bitter taste receptors and respond in vitro to bacterial supernatant and metabolites via massive calcium transients, similar to the ones observed in vivo during infection. Upon infection, CSF-cNs also upregulate the expression of numerous cytokines and complement components involved in innate immunity. Accordingly, we demonstrate, using cell-specific ablation and blockade of neurotransmission, that CSF-cN neurosecretion enhances survival of the host during S. pneumoniae infection. Finally, we show that CSF-cNs respond to various pathogenic bacteria causing meningitis in humans, as well as to the supernatant of cells infected by a neurotropic virus. Altogether, our work uncovers that central sensory neurons in the spinal cord, previously involved in postural control and morphogenesis, contribute as well to host survival by responding to the invasion of the CSF by pathogenic bacteria during meningitis.

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Type
research article
DOI
10.1016/j.cub.2023.01.039
Web of Science ID

WOS:000956333800001

Author(s)
Prendergast, Andrew E.
•
Jim, Kin Ki
•
Marnas, Hugo
•
Desban, Laura
•
Quan, Feng B.
•
Djenoune, Lydia
•
Laghi, Valerio
•
Hocquemiller, Agnes
•
Lunsford, Elias T.
•
Roussel, Julian
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Date Issued

2023-03-13

Publisher

CELL PRESS

Published in
Current Biology
Volume

33

Issue

5

Start page

940

End page

956.e10

Subjects

Biochemistry & Molecular Biology

•

Biology

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Cell Biology

•

Life Sciences & Biomedicine - Other Topics

•

in-situ hybridization

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substance inducing transformation

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solitary chemosensory cells

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cerebrospinal-fluid

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sensory neurons

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volatile metabolites

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pneumococcal types

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gene-expression

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chemical nature

•

zebrafish

Peer reviewed

REVIEWED

Written at

EPFL

EPFL units
LFMI  
Available on Infoscience
April 10, 2023
Use this identifier to reference this record
https://infoscience.epfl.ch/handle/20.500.14299/196887
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