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Streptococcus pneumoniae rapidly translocates from the nasopharynx through the cribriform plate to invade and inflame the dura

Teerawit Audshasai, Jonathan A. Coles, Stavros Panagiotou, Shadia Khandaker, Hannah E. Scales, Morten Kjos, Murielle Baltazar, Julie Vignau, James M. Brewer, Aras Kadioglu, Marie Yang
doi: https://doi.org/10.1101/2021.09.28.462246
Teerawit Audshasai
1Institute of Infection and Global Health, University of Liverpool, 8 West Derby Street, Liverpool L69 7BE, United Kingdom
2Faculty of Pharmacy, Mahidol University, 447 Sri-Ayuthaya Road, Rajathevi, Bangkok 10400, Thailand
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Jonathan A. Coles
3Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow G12 8TA, United Kingdom
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Stavros Panagiotou
1Institute of Infection and Global Health, University of Liverpool, 8 West Derby Street, Liverpool L69 7BE, United Kingdom
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Shadia Khandaker
1Institute of Infection and Global Health, University of Liverpool, 8 West Derby Street, Liverpool L69 7BE, United Kingdom
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Hannah E. Scales
3Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow G12 8TA, United Kingdom
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Morten Kjos
4Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Christian Magnus Falsensvei 18, 1433 Ås, Norway
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Murielle Baltazar
1Institute of Infection and Global Health, University of Liverpool, 8 West Derby Street, Liverpool L69 7BE, United Kingdom
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Julie Vignau
5Centre de Recherche en Cancérologie et Immunologie Nantes Angers, Université de Nantes, 8 quai Moncousu, 44007 Nantes, France
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James M. Brewer
3Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow G12 8TA, United Kingdom
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Aras Kadioglu
1Institute of Infection and Global Health, University of Liverpool, 8 West Derby Street, Liverpool L69 7BE, United Kingdom
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  • For correspondence: a.kadioglu@liverpool.ac.uk marie.yang@liverpool.ac.uk
Marie Yang
1Institute of Infection and Global Health, University of Liverpool, 8 West Derby Street, Liverpool L69 7BE, United Kingdom
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  • For correspondence: a.kadioglu@liverpool.ac.uk marie.yang@liverpool.ac.uk
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Abstract

The entry routes and translocation mechanisms of bacterial pathogens into the central nervous system remain obscure. We report here that Streptococcus pneumoniae (Sp) or polystyrene microspheres, applied to the nose of a mouse, appeared in the meninges of the dorsal cortex within minutes. Recovery of viable bacteria from dissected tissue and fluorescence microscopy showed that up to at least 72h, Sp and microspheres were predominantly in the outer of the two meninges, the pachymeninx. No Sp were found in blood or cerebrospinal fluid. Evidence that this was not an artifact of the method of administration is that in mice infected by horizontal transmission, Sp were also predominantly in the meninges and absent from blood. Intravital imaging through the skull, and flow cytometry showed recruitment and activation of LysM+ cells in the dorsal pachymeninx at 5h and 10h following intranasal infection. Imaging of the cribriform plate suggested that both Sp and microspheres entered through its foramina via an inward flow of fluid connecting the nose to the pachymeninx. Our findings bring further insight into the invasion mechanisms of bacterial pathogens such as Sp into the central nervous system, but are also pertinent to the delivery of drugs to the brain, and the entry of air-borne particles into the cranium.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵* Co-senior authors.

  • Abbreviations

    BHI
    Brain Heart Infusion
    CSF
    Cerebrospinal Fluid
    CSFE
    CarboxyFluorescein Succinimidyl Ester
    CNS
    Central Nervous System
    DC
    Dendritic Cell
    CFU
    Colony Forming Unit
    GFP
    Green Fluorescent Protein
    FCS
    Fetal Calf Serum
    IAV
    Influenza A Virus
    LSM
    Laser Scanning Microscope
    N.A.
    Numerical Aperture
    PBS
    phosphate buffered saline
    PFA
    paraformaldehyde
    SHG
    Second Harmonic Generation
    Sp
    Streptococcus pneumoniae
  • Copyright 
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    Streptococcus pneumoniae rapidly translocates from the nasopharynx through the cribriform plate to invade and inflame the dura
    Teerawit Audshasai, Jonathan A. Coles, Stavros Panagiotou, Shadia Khandaker, Hannah E. Scales, Morten Kjos, Murielle Baltazar, Julie Vignau, James M. Brewer, Aras Kadioglu, Marie Yang
    bioRxiv 2021.09.28.462246; doi: https://doi.org/10.1101/2021.09.28.462246
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    Streptococcus pneumoniae rapidly translocates from the nasopharynx through the cribriform plate to invade and inflame the dura
    Teerawit Audshasai, Jonathan A. Coles, Stavros Panagiotou, Shadia Khandaker, Hannah E. Scales, Morten Kjos, Murielle Baltazar, Julie Vignau, James M. Brewer, Aras Kadioglu, Marie Yang
    bioRxiv 2021.09.28.462246; doi: https://doi.org/10.1101/2021.09.28.462246

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