Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-13T05:12:23.908Z Has data issue: false hasContentIssue false
  • English
  • Français

Phenotypic changes in satellite glial cells in cultured trigeminal ganglia

Published online by Cambridge University Press:  28 October 2011

Vitali Belzer ,
Nathanael Shraer  and
Menachem Hanani
Vitali Belzer
Affiliation:
Laboratory of Experimental Surgery, Hadassah-Hebrew University Medical Center, Mount Scopus, Jerusalem 91240, Israel
Nathanael Shraer
Affiliation:
Laboratory of Experimental Surgery, Hadassah-Hebrew University Medical Center, Mount Scopus, Jerusalem 91240, Israel
Menachem Hanani*
Affiliation:
Laboratory of Experimental Surgery, Hadassah-Hebrew University Medical Center, Mount Scopus, Jerusalem 91240, Israel
*
Correspondence should be addressed to: Menachem Hanani, Ph.D., 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
Get access Rights & Permissions [Opens in a new window]

Abstract

Satellite glial cells (SGCs) are specialized cells that form a tight sheath around neurons in sensory ganglia. In recent years, there is increasing interest in SGCs and they have been studied in both intact ganglia and in tissue culture. Here we studied phenotypic changes in SGCs in cultured trigeminal ganglia from adult mice, containing both neurons and SGCs, using phase optics, immunohistochemistry and time-lapse photography. Cultures were followed for up to 14 days. After isolation virtually every sensory neuron is ensheathed by SGCs, as in the intact ganglia. After one day in culture, SGCs begin to migrate away from their parent neurons, but in most cases the neurons still retain an intact glial cover. At later times in culture, there is a massive migration of SGCs away from the neurons and they undergo clear morphological changes, and at 7 days they become spindle-shaped. At one day in culture SGCs express the glial marker glutamine synthetase, and also the purinergic receptor P2X7. From day 2 in culture the glutamine synthetase expression is greatly diminished, whereas that of P2X7 is largely unchanged. We conclude that SGCs retain most of their characteristics for about 24 h after culturing, but undergo major phenotypic changes at later times.

Keywords

Tissue culturesatellite glial cellstrigeminal ganglionglutamine synthetaseP2X7 receptors
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Issue 4 , November 2010 , pp. 237 - 243
Copyright
Copyright © Cambridge University Press 2011

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

Arora, D.K., Cosgrave, A.S., Howard, M.R., Bubb, V., Quinn, J.P. and Thippeswamy, T. (2007) Evidence of postnatal neurogenesis in dorsal root ganglion: role of nitric oxide and neuronal restrictive silencer transcription factor. Journal of Molecular Neuroscience 32, 97–107.CrossRefGoogle ScholarPubMed
Bradman, M.J., Arora, D.K., Morris, R. and Thippeswamy, T. (2010) How do the satellite glia cells of the dorsal root ganglia respond to stressed neurons?—nitric oxide saga from embryonic development to axonal injury in adulthood. Neuron Glia Biology 6, 11–17.CrossRefGoogle ScholarPubMed
Cameron-Curry, P., Dulac, C. and Le Douarin, N.M. (1993) Negative regulation of Schwann cell myelin protein gene expression by the dorsal root ganglionic microenvironment. European Journal of Neuroscience 5, 594–604.CrossRefGoogle ScholarPubMed
Capuano, A., De Corato, A., Lisi, L., Tringali, G., Navarra, P. and Dello Russo, C. (2009) Proinflammatory-activated trigeminal satellite cells promote neuronal sensitization: relevance for migraine pathology. Molecular Pain 5, 43.CrossRefGoogle ScholarPubMed
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
Chessell, I.P., Hatcher, J.P., Bountra, C., Michel, A.D., Hughes, J.P., Green, P., Egerton, J., Murfin, M., Richardson, J., Peck, W.L., Grahames, C.B., Casula, M.A., Yiangou, Y., Birch, R., Anand, P. and Buell, G.N. (2005) Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114, 386–396.CrossRefGoogle ScholarPubMed
Crain, S.M. (1956) Resting and action potentials of cultured chick embryo spinal ganglion cells. Journal of Comparative Neurology 104, 285–329.CrossRefGoogle ScholarPubMed
Devor, M. (1999) Unexplained peculiarities of the dorsal root ganglion. Pain Suppl 6, S27–35.CrossRefGoogle ScholarPubMed
Fex Svenningsen, A., Colman, D.R. and Pedraza, L. (2004) Satellite cells of dorsal root ganglia are multipotential glial precursors. Neuron Glia Biology 1, 85–93.CrossRefGoogle ScholarPubMed
Gu, Y., Chen, Y., Zhang, X., Li, G.W., Wang, C. and Huang, L.Y. (2010) Neuronal soma-satellite glial cell interactions in sensory ganglia and the participation of purinergic receptors. Neuron Glia Biology 6, 53–62.CrossRefGoogle 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., Xia, Y. and Wood, J.D. (1994) Myenteric ganglia from the adult guinea-pig small intestine in tissue culture. Neurogastroenterology and Motility 6, 103–118.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.CrossRefGoogle ScholarPubMed
Jasmin, L., Vit, J.P., Bhargava, A. and Ohara, P.T. (2010) Can satellite glial cells be therapeutic targets for pain control?. Neuron Glia Biology 6, 63–71.CrossRefGoogle ScholarPubMed
Jessen, K.R. and Mirsky, R. (1983) Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. Journal of Neuroscience 3, 2206–2218.CrossRefGoogle ScholarPubMed
Jessen, K.R., Morgan, L., Stewart, H.J. and Mirsky, R. (1990) Three markers of adult non-myelin-forming Schwann cells, 217c(Ran-1), A5E3 and GFAP: development and regulation by neuron-Schwann cell interactions. Development 109, 91–103.CrossRefGoogle ScholarPubMed
Julius, D. and Basbaum, A.I. (2001) Molecular mechanisms of nociception. Nature 413, 203–210.CrossRefGoogle ScholarPubMed
Kobayashi, K., Fukuoka, T., Yamanaka, H., Dai, Y., Obata, K., Tokunaga, A. and Noguchi, K. (2005) Differential expression patterns of mRNAs for P2X receptor subunits in neurochemically characterized dorsal root ganglion neurons in the rat. Journal of Comparative Neurology 481, 377–390.CrossRefGoogle ScholarPubMed
Kushnir, R., Cherkas, P.S. and Hanani, M. (2011) Peripheral inflammation upregulates P2X receptor expression in satellite glial cells of mouse trigeminal ganglia: a calcium imaging study. Neuropharmacology 61, 739–746.CrossRefGoogle ScholarPubMed
Lawson, S.N., Biscoe, T.J. and Headley, P.M. (1976) The effect of electrophoretically applied GABA on cultured dissociated spinal cord and sensory ganglion neurones of the rat. Brain Research 117, 493–497.CrossRefGoogle ScholarPubMed
Li, H.Y., Say, E.H. and Zhou, X.F. (2007) Isolation and characterization of neural crest progenitors from adult dorsal root ganglia. Stem Cells 25, 2053–2065.CrossRefGoogle ScholarPubMed
Li, R.H., Sliwkowski, M.X., Lo, J. and Mather, J.P. (1996) Establishment of Schwann cell lines from normal adult and embryonic rat dorsal root ganglia. Journal of Neuroscience Methods 67, 57–69.CrossRefGoogle ScholarPubMed
Ng, K.Y., Wong, Y.H. and Wise, H. (2010) The role of glial cells in influencing neurite extension by dorsal root ganglion cells. Neuron Glia Biology 6, 19–29.CrossRefGoogle ScholarPubMed
Ninomiya, T., Barakat-Walter, I. and Droz, B. (1994) Neuronal phenotypes in mouse dorsal root ganglion cell cultures: enrichment of substance P and calbindin D-28k expressing neurons in a defined medium. International Journal of Developmental Neuroscience 12, 99–106.CrossRefGoogle Scholar
Norenberg, M.D. and Martinez-Hernandez, A. (1979) Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Research 161, 303–310.CrossRefGoogle ScholarPubMed
Pannese, E. (1981) The satellite cells of the sensory ganglia. Advances in Anatomy Embryology and Cell Biology 65, 1–111.CrossRefGoogle ScholarPubMed
Pannese, E. (2010) The structure of the perineuronal sheath of satellite glial cells (SGCs) in sensory ganglia. Neuron Glia Biology 6, 3–10.CrossRefGoogle ScholarPubMed
Rugiero, F., Drew, L.J. and Wood, J.N. (2010) Kinetic properties of mechanically activated currents in spinal sensory neurons. Journal of Physiology 588, 301–314.CrossRefGoogle ScholarPubMed
Shoji, Y., Yamaguchi-Yamada, M. and Yamamoto, Y. (2010) Glutamate- and GABA-mediated neuron-satellite cell interaction in nodose ganglia as revealed by intracellular calcium imaging. Histochemistry and Cell Biology 134, 13–22.CrossRefGoogle ScholarPubMed
Suadicani, S.O., Cherkas, P.S., Zuckerman, J., Smith, D.N., Spray, D.C. and Hanani, M. (2010) Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia. Neuron Glia Biology 6, 43–51.CrossRefGoogle ScholarPubMed
Thippeswamy, T. and Morris, R. (2001) Evidence that nitric oxide-induced synthesis of cGMP occurs in a paracrine but not an autocrine fashion and that the site of its release can be regulated: studies in dorsal root ganglia in vivo and in vitro. Nitric Oxide 5, 105–115.CrossRefGoogle Scholar
Weick, M., Cherkas, P.S., Härtig, W., Pannicke, T., Uckermann, O., Bringman, A., Tal, M., Reichenbach, A. and Hanani, M. (2003) P2 Receptors in satellite glial cells in trigeminal ganglia of mice. Neuroscience 120, 969–977.CrossRefGoogle ScholarPubMed
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