Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-08T00:20:33.415Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  05 March 2010

Menachem Hanani ,
Anna Caspi  and
Vitali Belzer
Menachem Hanani*
Affiliation:
Laboratory of Experimental Surgery, Hadassah-Hebrew University Medical Center, Jerusalem, Israel
Anna Caspi
Affiliation:
Laboratory of Experimental Surgery, Hadassah-Hebrew University Medical Center, Jerusalem, Israel
Vitali Belzer
Affiliation:
Laboratory of Experimental Surgery, Hadassah-Hebrew University Medical Center, 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

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.

Keywords

Gliainflammationdye couplingsuperior mesenteric ganglionsuperior cervical ganglion
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Special Issue 1: Satellite Glial Cells , February 2010 , pp. 85 - 89
Copyright
Copyright © Cambridge University Press 2010

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

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, 1053–1062.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.CrossRefGoogle ScholarPubMed
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, 174–184.Google Scholar
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, 79–86.Google Scholar
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, 261–274.CrossRefGoogle Scholar
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, 8–20.Google Scholar
Gabella, G. (1972) Fine structure of the myenteric plexus in the guinea-pig ileum. Journal of Anatomy 111, 69–97.Google ScholarPubMed
Hanani, M. (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Research Brain Research Reviews 48, 457–476.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 62–67.CrossRefGoogle Scholar
Hanani, M., Zamir, O. and Baluk, P. (1989) Glial cells in the guinea pig myenteric plexus are dye coupled. Brain Research 497, 245–249.CrossRefGoogle ScholarPubMed
Herr, J.C. (1976) Reflexive gap junctions. Gap junctions between processing arising from the same ovarian decidual cell. Journal of Cell Biology 69, 495–501.CrossRefGoogle ScholarPubMed
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, 49–57.Google Scholar
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.CrossRefGoogle ScholarPubMed
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, 44–68.Google Scholar
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, 1797–1806.CrossRefGoogle ScholarPubMed
Li, C. and Horn, J.P. (2006) Physiological classification of sympathetic neurons in the rat superior cervical ganglion. Journal of Neurophysiology 95, 187–195.CrossRefGoogle ScholarPubMed
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, 91–135.Google Scholar
McLachlan, E.M. (2003) Transmission of signals through sympathetic ganglia – modulation, integration or simply distribution? Acta Physiologica Scandinavica 177, 227–235.Google Scholar
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, 417–449.Google Scholar
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, 3064–3073.CrossRefGoogle ScholarPubMed
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, 450–463.CrossRefGoogle ScholarPubMed
Pekny, M. and Nilsson, M. (2005) Astrocyte activation and reactive gliosis. Glia 50, 427–434.Google Scholar
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, 77–105.CrossRefGoogle ScholarPubMed
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, 457–475.Google Scholar
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, 363–371.Google Scholar
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
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. 603–628.CrossRefGoogle 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.Google Scholar