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Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia

Published online by Cambridge University Press:  06 November 2009

Sylvia O. Suadicani ,
Pavel S. Cherkas ,
Jonathan Zuckerman ,
David N. Smith ,
David C. Spray  and
Menachem Hanani
Sylvia O. Suadicani
Affiliation:
Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY, USA Department of Urology, Albert Einstein College of Medicine, Bronx, NY, USA
Pavel S. Cherkas
Affiliation:
Laboratory of Experimental Surgery, Hebrew University-Hadassah Medical School, Mount Scopus, Jerusalem, Israel
Jonathan Zuckerman
Affiliation:
Laboratory of Experimental Surgery, Hebrew University-Hadassah Medical School, Mount Scopus, Jerusalem, Israel
David N. Smith
Affiliation:
Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY, USA
David C. Spray
Affiliation:
Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY, USA
Menachem Hanani*
Affiliation:
Laboratory of Experimental Surgery, Hebrew University-Hadassah Medical School, Mount Scopus, Jerusalem, Israel
*
Correspondence should be addressed to: Menachem Hanani, Laboratory of Experimental Surgery, Hadassah University Hospital, Mount Scopus, Jerusalem 91240, Israel phone: 972-2-5844721 fax: 972-2-5823515 email: hananim@cc.huji.ac.il
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Abstract

Astrocytes communicate with neurons, endothelial and other glial cells through transmission of intercellular calcium signals. Satellite glial cells (SGCs) in sensory ganglia share several properties with astrocytes, but whether this type of communication occurs between SGCs and sensory neurons has not been explored. In the present work we used cultured neurons and SGCs from mouse trigeminal ganglia to address this question. Focal electrical or mechanical stimulation of single neurons in trigeminal ganglion cultures increased intracellular calcium concentration in these cells and triggered calcium elevations in adjacent glial cells. Similar to neurons, SGCs responded to mechanical stimulation with increase in cytosolic calcium that spread to the adjacent neuron and neighboring glial cells. Calcium signaling from SGCs to neurons and among SGCs was diminished in the presence of the broad-spectrum P2 receptor antagonist suramin (50 μM) or in the presence of the gap junction blocker carbenoxolone (100 μM), whereas signaling from neurons to SGCs was reduced by suramin, but not by carbenoxolone. Following induction of submandibular inflammation by Complete Freund's Adjuvant injection, the amplitude of signaling among SGCs and from SGCs to neuron was increased, whereas the amplitude from neuron to SGCs was reduced. These results indicate for the first time the presence of bidirectional calcium signaling between neurons and SGCs in sensory ganglia cultures, which is mediated by the activation of purinergic P2 receptors, and to some extent by gap junctions. Furthermore, the results indicate that not only sensory neurons, but also SGCs release ATP. This form of intercellular calcium signaling likely plays key roles in the modulation of neuronal activity within sensory ganglia in normal and pathological states.

Keywords

Gap junctionsneuron–glial communicationorofacial hypersensitivitypurinergic receptors
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Special Issue 1: Satellite Glial Cells , February 2010 , pp. 43 - 51
Copyright
Copyright © Cambridge University Press 2009

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