Functional relationships between sensory nerve fibers and mast cells of dura mater in normal and inflammatory conditions

In this study, we have characterized the phenotype of mast cells in rat dura mater and their topological and functional relationships with C-fibers in normal and inflammatory conditions. Three mast cell populations with different size, morphology and localization were characterized by their content...

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Bibliographic Details
Published in:Neuroscience 1997-04, Vol.77 (3), p.829-839
Main Authors: Dimitriadou, V, Rouleau, A, Trung Tuong, M.D, Newlands, G.J.F, Miller, H.R.P, Luffau, G, Schwartz, J.-C, Garbarg, M
Format: Article
Language:English
Subjects:
Animals
Animals, Newborn
Biological and medical sciences
Capsaicin
Cerebral circulation. Blood-brain barrier. Choroid plexus. Cerebrospinal fluid. Circumventricular organ. Meninges
Cerebral Cortex - immunology
Cerebral Cortex - physiology
Cerebral Cortex - physiopathology
Chymases
Denervation
dura mater
Dura Mater - physiology
Dura Mater - physiopathology
Enzyme-Linked Immunosorbent Assay
Fundamental and applied biological sciences. Psychology
Histamine - biosynthesis
Histamine Antagonists - pharmacology
histamine H 3 receptors
inflammation
Inflammation - blood
Inflammation - physiopathology
Male
mast cells
Mast Cells - drug effects
Mast Cells - physiology
Methylhistamines - pharmacology
Nerve Fibers - drug effects
Nerve Fibers - physiology
Neurons, Afferent - drug effects
Neurons, Afferent - physiology
neuropeptides
Nippostrongylus
Piperidines - pharmacology
proteases
Rats
Rats, Wistar
Reference Values
Sensitivity and Specificity
Serine Endopeptidases - blood
Serine Endopeptidases - metabolism
Strongylida Infections - blood
Strongylida Infections - physiopathology
Vertebrates: nervous system and sense organs
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Summary:In this study, we have characterized the phenotype of mast cells in rat dura mater and their topological and functional relationships with C-fibers in normal and inflammatory conditions. Three mast cell populations with different size, morphology and localization were characterized by their content of specific neutral serine proteases. They showed immunoreactivity corresponding to rat mast cell protease I, rat mast cell protease II, or both proteases. Using confocal microscopy, all three mast cell types were observed in close apposition (distance less than 100 nm) to calcitonin gene-related peptide- and substance P-immunoreactive nerve fibers in both controls and rats infected with the nematode Nippostrongylus brasiliensis. After nematode infection or neonatal treatment with capsaicin, a large increase in the number of rat mast cell protease II-immunoreactive mast cells was found within dura mater segments (+1478% and +596%, respectively), without concomitant changes of rat mast cell protease I- or rat mast cell protease I/II-immunoreactive mast cells. Under both these conditions, the increase in mast cell number was accompanied by a significant increase in rat mast cell protease II level within tissue extracts (+281% after nematode infection and +36% after capsaicin treatment). The functional interaction of mast cells with sensory nerve fibers in the dura mater was assessed by evaluating [ 3H]histamine synthesis after administration of l-[ 3H]histidine, an index of mast cell activity. The H 3 receptor agonist ( R)- α-methylhistamine (15 mg/kg, i.p.) had no effect, but administration of the H 3 receptor antagonist, thioperamide (10 mg/kg, i.p.), resulted in a significant increase of [ 3H]histamine synthesis (+62%). This effect was reduced in neonatal capsaicin-treated rats, but not completely suppressed (+35%), very likely because of partial denervation, as assessed by monitoring calcitonin gene-related peptide immunoreactivity. It is concluded that, in the dura mater, as in peripheral tissues, sensory nerve fibers and mast cells actively synthesizing and releasing histamine form a short inhibitory feedback loop involving prejunctional H 3 receptors that could regulate the release of pro-inflammatory mediators, thus limiting the extent of inflammatory reactions.
ISSN:0306-4522
1873-7544
DOI:10.1016/S0306-4522(96)00488-5