Glutamate- and GABA-mediated neuron–satellite cell interaction in nodose ganglia as revealed by intracellular calcium imaging

Abstract

In the sensory ganglia, neurons are devoid of synaptic contacts, and ganglion neurons surrounded by one of glial cells, satellite cells. Recent studies suggest that neurons and satellite cells interact through neurotransmitters. In the present study, intracellular Ca(2+) ([Ca(2+)](i)) dynamics of neurons and satellite cells from one of viscerosensory ganglia, nodose ganglion (NG), were investigated by stimulation with glutamate and its agonist and/or the antagonist of the GABA(A) receptor bicuculline. In the specimens containing neurons with satellite cells, glutamate and a metabotropic glutamate receptor (mGluR) agonist t-ACPD evoked [Ca(2+)](i) increases in both neurons and surrounding satellite cells. Moreover, bicuculline also induced [Ca(2+)](i) increases in neurons and satellite cells. However, in the isolated neurons, bicuculline did not cause an increase in [Ca(2+)](i), suggesting that satellite cells are equipped with the ability to release GABA. In the neurons associated with satellite cells, the delay time until the onset of a response was shorter in the case of glutamate stimulation with bicuculline than that without bicuculline (107.3 +/- 93.4 vs. 231.8 +/- 97.0 s, p < 0.01). Furthermore, immunoreactivities for glutamate transporter, GLAST, and GABA transporter, GAT-3, were observed in both neurons and satellite cells of NG. In conclusion, the levels of [Ca(2+)](i) of NG neurons and surrounding satellite cells are increased by glutamate through at least mGluRs, and endogenous GABA modulates these responses; GABA inhibition is dependent on a close association between neurons and satellite cells. Such neuron-glia interaction in the nodose ganglion may regulate sensory information from visceral organs.

GABA-mediated modulation of ATP-induced intracellular calcium responses in nodose ganglion neurons of the rat

“…The methods of immunohistochemistry have been described previously [18]. The following antibodies were used: polyclonal guinea pig antibody against P2X2 (1:100; GP14106, Neuromics, Edina, MN, USA), and polyclonal rabbit antibody against P2X3 (1:1000; RA10109, Neuromics), P2Y1 (1:100; APR-009, Alomone Labs, Jerusalem, Israel), or P2Y2 (1:100; APR-010, Alomone Labs).…”

“…The methods of intracellular calcium imaging were performed as previously reported [18], with some modifications. To prepare the specimens of NG neurons with satellite cells, NGs were placed in Dulbecco's modified Eagle's medium-F-12 (DMEM/F12; GIBCO, Tokyo) containing 0.4 mg/ml collagenase P (1213857; Roche Applied Science, Mannheim, Germany), and incubated for 25 min at 37 • C. Partially digested ganglia were dropped onto coverslips, and then incubated at 37 • C in a humidified atmosphere of 95% air-5% CO 2 .…”

Histochemistry and cell biology: the annual review 2010

“…It is suggested that the selective depletion of ganglion cells and therefore the loss of a substantial metabolic load is the basic cause of impaired vascular development in AnC retina. Shoji et al (2010) suggested, based on previous studies of expression of neurotransmitters receptors in neurons and satellite cells (SCs) of sensory ganglia (Hanani 2005;Julius and Basbaum 2001) that nodose ganglion (NG) neurons are regulated by surrounding SCs through glutamate and GABA and that such neuron-glia interactions may be involved in regulating viscerosensory informations from visceral organs. The authors found immunoreactivities for GLAST (glutamate transporter) and GAT-3 (GABA-selective transporter) in neurons and SCs.…”

δ-Aminolevulinic acid and its methyl ester induce the formation of Protoporphyrin IX in cultured sensory neurones

“…Borden 1996;Conti et al 1999;Liu et al 1999;Minelli et al 2003), information on their expression in the DRG is rather sparse. Only one report (Shoji et al 2010) showed GAT-3 expression in the rat nodose ganglion by immunohistochemistry.…”