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Effect of intestinal inflammation on capsaicin-sensitive afferents in the ileum of Schistosoma mansoni-infected mice

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Abstract

In the present study, the effect of intestinal schistosomiasis on the extrinsic sensory innervation of the murine ileum was investigated. Immunocytochemical techniques to localize calcitonin gene-related peptide (CGRP), substance P (SP), and vanilloid receptor 1 (VR1) were combined with retrograde tracing techniques and capsaicin treatment. Neurochemical characterization of extrinsic primary afferent neurons (EPANs) in normal and capsaicin-treated mice, revealed that CGRP and VR1, but not SP, were expressed in extrinsic afferents. Immunocytochemical analysis using the above-mentioned antibodies yielded three different populations of neurons in both dorsal root and nodose ganglia, namely CGRP/−-, SP/−-, and CGRP/SP-expressing neurons. Retrograde tracing revealed that only CGRP/−-expressing neurons projected to the ileum. Intestinal schistosomiasis resulted in an upregulation of the number of CGRP-immunoreactive (ir) nerve fibers in the lamina propria of the villi, coinciding with an increase in mucosal mast cells in acutely and chronically infected animals. In infected animals, mucosal mast cells were found closely associated with a dense mucosal CGRP-ir fiber network. Neonatal capsaicin treatment led to a 70% reduction in the number of mucosal mast cells. In conclusion, the present study provides evidence that CGRP is a valid marker for EPANs in the mouse ileum, which are involved in the recruitment of mucosal mast cells. Morphological evidence is provided of a neuroimmune interaction between mucosal mast cells and EPANs in schistosoma-infected mice.

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Acknowledgements

The authors thank the technical staff of all laboratories for their excellent assistance. This study was supported by IUAP project P5/20, an IWT fellowship from the Flemish Government (SB1146) to Frederik De Jonge, and by grants from the Wellcome Trust.

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Authors and Affiliations

  1. Laboratory of Cell Biology and Histology, Department of Biomedical Sciences, University of Antwerp (RUCA), Groenenborgerlaan 171, 2020, Antwerp, Belgium

    Frederik De Jonge, Luc Van Nassauw, Dirk Adriaensen, Frans Van Meir & Jean-Pierre Timmermans

  2. Department of Veterinary Clinical Studies, Royal (Dick) School of Veterinary Studies, Veterinary Field Station, University of Edinburgh, Easter Bush, Roslin, Midlothian, EH5 9RG, UK

    Hugh R. P. Miller

  3. Laboratory of Pathology, Department of Medicine, University of Antwerp, Universiteitsplein 1, 2610, Wilrijk, Belgium

    Eric Van Marck

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  1. Frederik De Jonge
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  2. Luc Van Nassauw
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  7. Jean-Pierre Timmermans
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Correspondence to Jean-Pierre Timmermans.

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De Jonge, F., Van Nassauw, L., Adriaensen, D. et al. Effect of intestinal inflammation on capsaicin-sensitive afferents in the ileum of Schistosoma mansoni-infected mice. Histochem Cell Biol 119, 477–484 (2003). https://doi.org/10.1007/s00418-003-0532-5

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