Hostname: page-component-745bb68f8f-cphqk Total loading time: 0 Render date: 2025-02-05T05:56:47.157Z Has data issue: false hasContentIssue false
  • English
  • Français

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: [email protected]
Get access Rights & Permissions [Opens in a new window]

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

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ceruti, S., Fumagalli, M., Villa, G., Verderio, C. and Abbracchio, M.P. (2008) Purinoceptor-mediated calcium signaling in primary neuron–glia trigeminal cultures. Cell Calcium 43, 576–590.CrossRefGoogle ScholarPubMed
Charles, A.C., Merrill, J.E., Dirksen, E.R. and Sanderson, M.J. (1991) Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron 6, 983–992.Google Scholar
Cherkas, P.S., Huang, T.Y., Pannicke, T., Tal, M., Reichenbach, A. and Hanani, M. (2004) The effects of axotomy on neurons and satellite glial cells in mouse trigeminal ganglion. Pain 110, 290–298.Google Scholar
Cornell-Bell, A.H., Finkbeiner, S.M., Cooper, M.S. and Smith, S.J. (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470–473.CrossRefGoogle ScholarPubMed
Devor, M. (2006) Responses of nerves to injury in relations to neuropathic pain. In McMahon, S.B. and Koltzenburg, M. (eds) Wall and Melzack's Textbook of Pain, 5th edition. Dover: Elsevier Churchill Livingstone, pp. 905–928.Google Scholar
Dublin, P. and Hanani, M. (2007) Satellite glial cells in sensory ganglia: their possible contribution to inflammatory pain. Brain Behavior and Immunity 21, 592–598.Google Scholar
Froes, M.M., Correia, A.H., Garcia-Abreu, J., Spray, D.C., Campos de Carvalho, A.C. and Neto, M.V. (1999) Gap-junctional coupling between neurons and astrocytes in primary central nervous system cultures. Proceedings of the National Academy of Sciences of the U.S.A. 96, 7541–7546.CrossRefGoogle ScholarPubMed
Grynkiewicz, G., Poenie, M. and Tsien, R.Y. (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. Journal of Biological Chemistry 260, 3440–3450.Google Scholar
Gulbransen, B.D. and Sharkey, K.A. (2009) Purinergic neuron-to-glia signaling in the enteric nervous system. Gastroenterology 136, 1349–1358.CrossRefGoogle ScholarPubMed
Hanani, M. (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Research Brain Research Reviews 48, 457–476.Google Scholar
Hanani, M., Huang, T.Y., Cherkas, P.S., Ledda, M. and Pannese, E. (2002) Glial cell plasticity in sensory ganglia induced by nerve damage. Neuroscience 114, 279–283.Google Scholar
Hanani, M., Kushnir, R. and Cherkas, P.S. (2007) Nerve damage or inflammation augment purinergic signaling in satellite glial cells in mouse sensory ganglia. Neuron Glia Biology 3, S108.Google Scholar
Haydon, P.G. and Carmignoto, G. (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiological Reviews 86, 1009–1031.Google Scholar
Huang, T.Y., Belzer, V. and Hanani, M. (2009) Gap junctions in dorsal root ganglia: possible contribution to visceral pain. European Journal of Pain (in press).Google ScholarPubMed
Huang, T.Y., Cherkas, P.S., Rosenthal, D.W. and Hanani, M. (2005) Dye coupling among satellite glial cells in mammalian dorsal root ganglia. Brain Research 1036, 42–49.Google Scholar
Montana, V., Malarkey, E.B., Verderio, C., Matteoli, M. and Parpura, V. (2006) Vesicular transmitter release from astrocytes. Glia 54, 700–715.CrossRefGoogle ScholarPubMed
Nedergaard, M., Ransom, B. and Goldman, S.A. (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends in Neuroscience 26, 523–530.CrossRefGoogle ScholarPubMed
Pannese, E. (1981) The satellite cells of the sensory ganglia. Advances in Anatomy Embryology and Cell Biology 65, 1–111.Google Scholar
Parpura, V., Scemes, E. and Spray, D.C. (2004) Mechanisms of glutamate release from astrocytes: gap junction “hemichannels”, purinergic receptors and exocytotic release. Neurochemistry International 45, 259–264.Google Scholar
Rozental, R., Andrade-Rozental, A.F., Zheng, X., Urban, M., Spray, D.C. and Chiu, F.C. (2001) Gap junction-mediated bidirectional signaling between human fetal hippocampal neurons and astrocytes. Develomental Neuroscience 23, 420–431.Google Scholar
Scemes, E. and Giaume, C. (2006) Astrocyte calcium waves: what they are and what they do. Glia 54, 716–725.Google Scholar
Scemes, E. and Spray, D.C. (2008) Connexin expression (gap junctions and hemichannels) in astrocytes. In Parpura, V. and Haydon, P.G. (eds) Astrocytes in Pathophysiology of the Nervous System. Springer, Berlin, pp. 107–150.Google Scholar
Spataro, L.E., Sloane, E.M., Milligan, E.D., Wieseler-Frank, J., Schoeniger, D., Jekich, B.M. et al. (2004) Spinal gap junctions: potential involvement in pain facilitation. Journal of Pain 5, 392–405.CrossRefGoogle ScholarPubMed
Stephenson, J.L. and Byers, M.R. (1995) GFAP immunoreactivity in trigeminal ganglion satellite cells after tooth injury in rats. Experimental Neurology 131, 11–22.Google Scholar
Suadicani, S.O., Brosnan, C.F. and Scemes, E. (2006) P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. Journal of Neuroscience 26, 1378–1385.Google Scholar
Suadicani, S.O., Flores, C.E., Urban-Maldonado, M., Beelitz, M. and Scemes, E. (2004) Gap junction channels coordinate the propagation of intercellular Ca2+ signals generated by P2Y receptor activation. Glia 48, 217–229.CrossRefGoogle ScholarPubMed
Takeda, M., Tanimoto, T., Kadoi, J., Nasu, M., Takahashi, M., Kitagawa, J. et al. (2007) Enhanced excitability of nociceptive trigeminal ganglion neurons by satellite glial cytokine following peripheral inflammation. Pain 129, 155–166.Google Scholar
Thalakoti, S., Patil, V.V., Damodaram, S., Vause, C.V., Langford, L.E., Freeman, S.E. et al. (2007) Neuron–glia signaling in trigeminal ganglion: implications for migraine pathology. Headache 47, 1008–1023.CrossRefGoogle ScholarPubMed
Weick, M., Cherkas, P.S., Hartig, W., Pannicke, T., Uckermann, O., Bringmann, A. et al. (2003) P2 receptors in satellite glial cells in trigeminal ganglia of mice. Neuroscience 120, 969–977.Google Scholar
Zhang, W., Segura, B.J., Lin, T.R., Hu, Y. and Mulholland, M.W. (2003) Intercellular calcium waves in cultured enteric glia from neonatal guinea pig. Glia 42, 252–262.Google Scholar
Zhang, X., Chen, Y., Wang, C. and Huang, L.Y. (2007) Neuronal somatic ATP release triggers neuron–satellite glial cell communication in dorsal root ganglia. Proceedings of the National Academy of Sciences of the U.S.A. 104, 9864–9869.Google Scholar
Zhang, X.F., Han, P., Faltynek, C.R., Jarvis, M.F. and Shieh, C.C. (2005) Functional expression of P2X7 receptors in non-neuronal cells of rat dorsal root ganglia. Brain Research 1052, 63–70.CrossRefGoogle ScholarPubMed