Journal Article

DZNE-2025-01417

http://join2-wiki.gsi.de/foswiki/pub/Main/Artwork/join2_logo100x88.png Basophils activate splenic B cells and dendritic cells via IL-13 signaling in acute traumatic brain injury.

Olde Heuvel, F. ; Zhang, J. ; Sun, F. ; Krishnamurthy, S. S. ; Yartas, G.Extern* ; Özkan, B. ; Pagliarini, M. ; Voehringer, D. ; O'Meara, C. C. ; Schäfer, M. K. E. ; Huber-Lang, M. ; Roselli, F. (Last author)DZNE*

2025
BioMed Central London

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Please use a persistent id in citations: doi:10.1186/s12974-025-03621-1

Abstract: Peripheral consequences following traumatic brain injury (TBI) are characterized by both systemic inflammatory responses and autonomic dysregulation. One of the main immune regulatory organs, the spleen, shows high interaction with the brain which is controlled by both circulating mediators as well as autonomic fibers targeting splenic immune cells. The brain-spleen axis does not function as a one-way street, it also shows reciprocal effects where the spleen affects neuroinflammatory and cognitive functions post injury. To date, systemic and splenic inflammatory responses are measured by cells or mediators located in circulation. Nevertheless, most of the signaling and inflammation post injury takes place in the organs.We set out to investigate the early (3 h) signaling landscape in the spleen following a moderate severity closed head injury model to wild-type animals aged p60-90. Using phospho-proteomic signaling approaches, immunofluorescence stainings, Enzyme-Linked Immunosorbent Assay (ELISA), super-resolution microscopy and single mRNA in situ hybridization we investigated novel molecular and cellular players in the spleen involved in immune modulation after a head injury.Based on the signaling signature, we found a rapid influx of basophil granulocytes towards the spleen, via a recruitment mechanism that includes CXCL1 expressed by B-cells and dendritic cells (DCs). The basophils in turn seem to activate B cells and dendritic cells via the IL-13/IL-13Ra1 signaling pathway and enhance protein translation through the long non-coding RNA NORAD. The early recruitment of basophils and subsequent activation of B cells and DCs, is short lived and sets at 3dpi. Interestingly, the rapid recruitment of basophils is inhibited by ethanol intoxication in TBI, with a subsequent prevention of IL-13Ra phosphorylation and NORAD increase in B-cells and DCs.Basophils recruitment to the spleen may serve as an early mediator of systemic inflammatory responses to TBI with potential implications for research on biomarkers and therapeutic targets.

Keyword(s): Animals (MeSH) ; Brain Injuries, Traumatic: immunology (MeSH) ; Brain Injuries, Traumatic: metabolism (MeSH) ; Brain Injuries, Traumatic: pathology (MeSH) ; Mice (MeSH) ; Spleen: immunology (MeSH) ; Spleen: metabolism (MeSH) ; Spleen: pathology (MeSH) ; Signal Transduction: physiology (MeSH) ; B-Lymphocytes: metabolism (MeSH) ; B-Lymphocytes: immunology (MeSH) ; Interleukin-13: metabolism (MeSH) ; Interleukin-13: immunology (MeSH) ; Basophils: metabolism (MeSH) ; Basophils: immunology (MeSH) ; Mice, Inbred C57BL (MeSH) ; Dendritic Cells: metabolism (MeSH) ; Dendritic Cells: immunology (MeSH) ; Male (MeSH) ; B-cell ; Basophil ; Dendritic cell ; IL-13 ; Spleen ; Traumatic brain injury ; Interleukin-13

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Contributing Institute(s):

1. Metabolic Changes in Neurodegeneration (AG Roselli)

Research Program(s):

1. 352 - Disease Mechanisms (POF4-352) (POF4-352)

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