Mast cells in the guinea pig superior cervical ganglion: a functional and histological assessment

Bradley J. Undem, Walter C. Hubbard, Edward P. Christian, Daniel Weinreich

Research output: Contribution to journalArticlepeer-review

Abstract

We have previously found that antigenic stimulation of mast cells in the guinea pig superior cervical ganglion leads to membrane depolarization of principal neurons and a long-term increase in the efficacy of ganglionic transmission. In this study experiments were conducted to discern the histological, immunological and pharmacological characteristics of the mast cells within the superior cervical ganglion. Mast cells within the superior cervical ganglion could be stained with toluidine blue or berberine sulfate, the latter indicating that heparin-like molecules were present in the granules. Stainable mast cells were distributed throughout the ganglion with no gross evidence of regional localization. The number of mast cells stained with toluidine blue was reduced significantly (P < 0.01) in contralateral ganglia that had been exposed to the sensitizing antigen (ovalbumin), indicating antigen-induced degranulation. The superior cervical ganglion contained 208 ± 6 picomole of histamine (mean ± SEM, n = 66). Ovalbumin evoked the release of histamine from the superior cervical ganglion in a concentration-dependent fashion. At maximally effective concentrations, ovalbumin released 33 ± 2% of the total histamine stores (mean ± SEM, n = 61). Similar values were obtained with antigen-challenged stellate ganglia. A temperature of 37°C and an extracellular calcium concentration of 1 mM was required to elicit optimal antigen-induced responses. In addition to releasing histamine, antigenic stimulation of the ganglion resulted in a 3- to 5-fold increase in the synthesis and release of arachidonic acid metabolites including peptidoleukotriene, thromboxane B2, prostaglandins (PG) E2, F2α, D2, the PGD2 metabolite 9α 11β-PGF2, and the prostacyclin metabolite 6-keto PGF1α. Various putative mast cell secretagogues were examined for their ability to activate the superior cervical ganglion mast cell, as indicated by evoked histamine release. In contrast to rat peritoneal mast cells, high concentrations of substance P, compound 48/80, and nerve growth factor failed to stimulate the ganglion mast cells. Preganglionic nerve stimulation, electrical field stimulation of axons and cell bodies, or depolarizing concentrations of potassium chloride also failed to activate the superior cervical ganglion mast cells. These results suggest that substances released by membrane depolarization do not influence the function of the resident mast cells. The results demonstrate that the mast cells within sympathetic ganglia can be actively sensitized to respond to specific antigen. These mast cells are similar to lung parenchymal mast cells with respect to histological, immunological and pharmacological characteristics. Finally, the data are consistent with a hypothesis that the antigen-induced effects on superior cervical ganglion neurons occur secondary to the synthesis and release of a variety of bioactive substances, including biogenic amines, heparin-like molecules, and cyclooxygenase and lipoxygenase products of arachidonic acid.

Original languageEnglish (US)
Pages (from-to)75-87
Number of pages13
JournalJournal of the Autonomic Nervous System
Volume30
Issue number1
DOIs
StatePublished - Apr 1990

Keywords

  • Autacoid
  • Eicosanoid
  • Histamine
  • Mast cell
  • Neuroimmunology
  • Prostaglandin
  • Sympathetic ganglia

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology
  • Clinical Neurology

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