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

Sylvia O. Suadicani, Pavel S. Cherkas, Jonathan Zuckerman, David N. Smith, David C. Spray, Menachem Hanani

Research output: Contribution to journalArticle

75 Citations (Scopus)

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 (50M) 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 P 2 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.

Original languageEnglish (US)
Pages (from-to)43-51
Number of pages9
JournalNeuron Glia Biology
Volume6
Issue number1
DOIs
StatePublished - Feb 2010

Fingerprint

Trigeminal Ganglion
Calcium Signaling
Neuroglia
Neurons
Sensory Ganglia
Carbenoxolone
Calcium
Suramin
Gap Junctions
Sensory Receptor Cells
Astrocytes
Freund's Adjuvant

Keywords

  • Gap junctions
  • neuron-glial communication
  • orofacial hypersensitivity
  • purinergic receptors

ASJC Scopus subject areas

  • Cell Biology
  • Cellular and Molecular Neuroscience

Cite this

Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia. / Suadicani, Sylvia O.; Cherkas, Pavel S.; Zuckerman, Jonathan; Smith, David N.; Spray, David C.; Hanani, Menachem.

In: Neuron Glia Biology, Vol. 6, No. 1, 02.2010, p. 43-51.

Research output: Contribution to journalArticle

Suadicani, Sylvia O. ; Cherkas, Pavel S. ; Zuckerman, Jonathan ; Smith, David N. ; Spray, David C. ; Hanani, Menachem. / Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia. In: Neuron Glia Biology. 2010 ; Vol. 6, No. 1. pp. 43-51.
@article{02b4dde2960147a6b567615bd547b810,
title = "Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia",
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 (50M) 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 P 2 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 junctions, neuron-glial communication, orofacial hypersensitivity, purinergic receptors",
author = "Suadicani, {Sylvia O.} and Cherkas, {Pavel S.} and Jonathan Zuckerman and Smith, {David N.} and Spray, {David C.} and Menachem Hanani",
year = "2010",
month = "2",
doi = "10.1017/S1740925X09990408",
language = "English (US)",
volume = "6",
pages = "43--51",
journal = "Neuron Glia Biology",
issn = "1740-925X",
publisher = "Cambridge University Press",
number = "1",

}

TY - JOUR

T1 - Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia

AU - Suadicani, Sylvia O.

AU - Cherkas, Pavel S.

AU - Zuckerman, Jonathan

AU - Smith, David N.

AU - Spray, David C.

AU - Hanani, Menachem

PY - 2010/2

Y1 - 2010/2

N2 - 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 (50M) 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 P 2 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.

AB - 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 (50M) 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 P 2 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.

KW - Gap junctions

KW - neuron-glial communication

KW - orofacial hypersensitivity

KW - purinergic receptors

UR - http://www.scopus.com/inward/record.url?scp=77956338290&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77956338290&partnerID=8YFLogxK

U2 - 10.1017/S1740925X09990408

DO - 10.1017/S1740925X09990408

M3 - Article

C2 - 19891813

AN - SCOPUS:77956338290

VL - 6

SP - 43

EP - 51

JO - Neuron Glia Biology

JF - Neuron Glia Biology

SN - 1740-925X

IS - 1

ER -