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Peripheral inflammation augments gap junction-mediated coupling among satellite glial cells in mouse sympathetic ganglia

  • Menachem Hanani (a1), Anna Caspi (a1) and Vitali Belzer (a1)

Intercellular coupling by gap junctions is one of the main features of glial cells, but very little is known about this aspect of satellite glial cells (SGCs) in sympathetic ganglia. We used the dye coupling method to address this question in both a prevertebral ganglion (superior mesenteric) and a paravertebral ganglion (superior cervical) of mice. We found that in control ganglia, the incidence of dye coupling among SGCs that form the envelope around a given neuron was 10–20%, and coupling between SGCs around different envelopes was rare (1.5–3%). The dye injections also provided novel information on the structure of SGCs. Following peripheral inflammation, both types of coupling were increased, but most striking was the augmentation of coupling between SGCs forming envelopes around different neurons, which rose by 8–14.6-fold. This effect appeared to be non-systemic, and was blocked by the gap junction blocker carbenoxolone. These changes in SGCs may affect signal transmission and processing in sympathetic ganglia.

Corresponding author
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:
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Brázda, V., Klusáková, I., Svízenská, I., Veselková, Z. and Dubový, P. (2009) Bilateral changes in IL-6 protein, but not in its receptor gp130, in rat dorsal root ganglia following sciatic nerve ligature. Cellular and Molecular Neurobiology 29, 10531062.
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, 290298.
De Stefano, M.E., Leone, L., Moriconi, C., Del Signore, A., Petrucci, T.C. and Paggi, P. (2007) Involvement of the plasminogen enzymatic cascade in the reaction to axotomy of rat sympathetic neurons. Molecular and Cellular Neuroscience 36, 174184.
Elfvin, L.G., Björklund, H., Dahl, D. and Seiger, A. (1987) Neurofilament-like and glial fibrillary acidic protein-like immunoreactivities in rat and guinea-pig sympathetic, ganglia in situ and after perturbation. Cell and Tissue Research 250, 7986.
Elfvin, L.G. and Forsman, C. (1978) The ultrastructure of junctions between satellite cells in mammalian sympathetic ganglia as revealed by freeze-etching. Journal of Ultrastructure Research 163, 261274.
Fasano, C. and Niel, J.P. (2009) The mammalian sympathetic prevertebral ganglia: models for the study of neuronal networks and basic neuronal properties. Autonomic Neuroscience 150, 820.
Gabella, G. (1972) Fine structure of the myenteric plexus in the guinea-pig ileum. Journal of Anatomy 111, 6997.
Hanani, M. (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Research Brain Research Reviews 48, 457476.
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, 279283.
Hanani, M., Maudlej, N. and Härtig, W. (1999) Morphology and intercellular communication in glial cells of the intrinsic ganglia of the guinea-pig urinary bladder. Journal of the Autonomic Nervous System 76, 6267.
Hanani, M., Zamir, O. and Baluk, P. (1989) Glial cells in the guinea pig myenteric plexus are dye coupled. Brain Research 497, 245249.
Herr, J.C. (1976) Reflexive gap junctions. Gap junctions between processing arising from the same ovarian decidual cell. Journal of Cell Biology 69, 495501.
Huang, T.Y., Belzer, V. and Hanani, M. (2010) Gap junctions in dorsal root ganglia: possible contribution to visceral pain. European Journal of Pain 14, 4957.
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, 4249.
Klimaschewski, L., Kummer, W. and Heym, C. (1996) Localization, regulation and functions of neurotransmitters and neuromodulators in cervical sympathetic ganglia. Microscopy Research and Technique 35, 4468.
Komuro, T., Baluk, P. and Burnstock, G. (1982) An ultrastructural study of neurons and non-neuronal cells in the myenteric plexus of the rabbit colon. Neuroscience 7, 17971806.
Li, C. and Horn, J.P. (2006) Physiological classification of sympathetic neurons in the rat superior cervical ganglion. Journal of Neurophysiology 95, 187195.
Matthews, M.R. and Nelson, V.H. (1975) Detachment of structurally intact nerve endings from chromatolytic neurones of rat superior cervical ganglion during the depression of synaptic transmission induced by post-ganglionic axotomy. Journal of Physiology 245, 91135.
McLachlan, E.M. (2003) Transmission of signals through sympathetic ganglia – modulation, integration or simply distribution? Acta Physiologica Scandinavica 177, 227235.
Miller, R.J., Jung, H., Bhangoo, S.K. and White, F.A. (2009) Cytokine and chemokine regulation of sensory neuron function. Handbook of Experimental Pharmacology 194, 417449.
Ohara, P.T., Vit, J.P., Bhargava, A. and Jasmin, L. (2008) Evidence for a role of connexin 43 in trigeminal pain using RNA interference in vivo. Journal of Neurophysiology 100, 30643073.
Ohara, P.T., Vit, J.P., Bhargava, A., Romero, M., Sundberg, C., Charles, A.C. et al. (2009) Gliopathic pain: when satellite glial cells go bad. Neuroscientist 15, 450463.
Pekny, M. and Nilsson, M. (2005) Astrocyte activation and reactive gliosis. Glia 50, 427434.
Raivich, G., Bohatsche, M., Kloss, C.U., Werner, A., Jones, L.L. and Kreutzberg, G.W. (1999) Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Research Brain Research Reviews 30, 77105.
Rouach, N., Avignone, E., Même, W., Koulakoff, A., Venance, L., Blomstrand, F. et al. (2002) Gap junctions and connexin expression in the normal and pathological central nervous system. Biology of the Cell 94, 457475.
Shadiack, A.M., Sun, Y. and Zigmond, R.E. (2001) Nerve growth factor antiserum induces axotomy-like changes in neuropeptide expression in intact sympathetic and sensory neurons. Journal of Neuroscience 21, 363371.
Stephenson, J.L. and Byers, M.R. (1995) GFAP immunoreactivity in trigeminal ganglion satellite cells after tooth injury in rats. Experimental Neurology 131, 1122.
Szurszewski, J.H. and Miller, S.M. (2006) Physiology of prevetebral ganglia. In Johnson, L.R. (ed.) Physiology of the Gastrointestinal Tract (4th edn.), New York: Raven, pp. 603628.
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, 10081023.
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Neuron Glia Biology
  • ISSN: 1740-925X
  • EISSN: 1741-0533
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