Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T19:48:30.302Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of glial cells in influencing neurite extension by dorsal root ganglion cells

Published online by Cambridge University Press:  22 December 2009

Kai-Yu Ng ,
Yung H. Wong  and
Helen Wise
Kai-Yu Ng
Affiliation:
School of Biomedical Sciences, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong SAR, China
Yung H. Wong
Affiliation:
Department of Biochemistry, Hong Kong University of Science and Technology, Hong Kong SAR, China
Helen Wise*
Affiliation:
School of Biomedical Sciences, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong SAR, China
*
Correspondence should be addressed to: Helen Wise, School of Biomedical Sciences, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong SAR, China phone: +852 2603 6849 fax: +852 2603 5139 email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

When pretreated with pertussis toxin (PTX), the neurites of adult rat dorsal root ganglion (DRG) cells in mixed cell cultures retract over a period of 2 h following the initial stimulus of removal from the cell culture incubator for brief periods of observation. The purpose of this investigation was to determine whether this PTX-dependent response was specific to any one of the three subpopulations of DRG neurons. However, no neurite retraction response was observed in neuron-enriched populations of cells, or in cultures enriched in isolectin B4 (IB4)-positive neurons or in IB4-negative neurons. But, the addition of non-neuronal cells, and/or medium conditioned by non-neuronal cells, was sufficient to restore the PTX-dependent neurite retraction response, but only in large diameter IB4-negative neurons. In conclusion, we have identified a regulatory response, mediated by Gi/o-proteins, which prevents retraction of neurites in large diameter IB4-negative cells of adult rat DRG. The non-neuronal cells of adult rat DRG constitutively release factor/s that can stimulate neurite retraction of a subset of isolated DRG neurons, but this property of non-neuronal cells is only observed when the Gi/o-proteins of large diameter IB4-negative cells are inhibited.

Keywords

Neurite retractionGi/o proteins
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Special Issue 1: Satellite Glial Cells , February 2010 , pp. 19 - 29
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

Bennett, D.L., Michael, G.J., Ramachandran, N., Munson, J.B., Averill, S., Yan, Q. et al. (1998) A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. Journal of Neuroscience 18, 3059–3072.CrossRefGoogle ScholarPubMed
Campana, W.M. (2007) Schwann cells: activated peripheral glia and their role in neuropathic pain. Brain Behavior and Immunity 21, 522–527.CrossRefGoogle ScholarPubMed
Clarke, G.A. and Moss, D.J. (1997) GP55 inhibits both cell adhesion and growth of neurons, but not non-neuronal cells, via a G-protein-coupled receptor. European Journal of Neuroscience 9, 334–341.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Fang, X., Djouhri, L., McMullan, S., Berry, C., Waxman, S.G., Okuse, K. et al. (2006) Intense isolectin-B4 binding in rat dorsal root ganglion neurons distinguishes C-fiber nociceptors with broad action potentials and high Nav1.9 expression. Journal of Neuroscience 26, 7281–7292.CrossRefGoogle ScholarPubMed
Fields, R.D. and Stevens-Graham, B. (2002) New insights into neuron–glia communication. Science 298, 556–562.CrossRefGoogle ScholarPubMed
Filippo, M.D., Sarchielli, P., Picconi, B. and Calabresi, P. (2008) Neuroinflammation and synaptic plasticity: theorectical basis for a novel, immune-centred, therapeutic approach to neurological disorders. Trends in Pharmacological Sciences 29, 402–412.CrossRefGoogle Scholar
Franklin, S.L., Davies, A.M. and Wyatt, S. (2009) Macrophage stimulating protein is a neurotrophic factor for a sub-population of nociceptive sensory neurons. Molecular and Cellular Neuroscience 41, 175–185CrossRefGoogle ScholarPubMed
Gavazzi, I., Kumar, R.D.C., McMahon, S.B. and Cohen, J. (1999) Growth responses of different subpopulations of adult sensory neurons to neurotrophic factors in vitro. European Journal of Neuroscience 11, 3405–3414.CrossRefGoogle ScholarPubMed
Guseva, D. and Chelyshev, Y. (2006) The platicity of the DRG neurons belonging to different subpopulations after dorsal rhizotomy. Cellular and Molecular Neurobiology 26, 1225–1234.CrossRefGoogle Scholar
Hanani, M. (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Research Reviews 48, 457–476.CrossRefGoogle ScholarPubMed
He, J.C.J., Gomes, I., Nguyen, T., Jayaram, G., Ram, P.T., Devi, L.A. et al. (2005) The Gαo/i-coupled cannabinoid receptor-mediated neurite outgrowth involves rap regulation of Src and Stat3. Journal of Biological Chemistry 280, 33426–33434.CrossRefGoogle Scholar
He, J.C.J., Neves, S.R., Jordan, J.D. and Iyengar, R. (2006) Role of the Go/i signaling network in the regulation of neurite outgrowth. Canadian Journal of Physiology and Pharmacology 84, 687–694.CrossRefGoogle ScholarPubMed
Heblich, F., England, S. and Docherty, R.J. (2001) Indirect actions of bradykinin on neonatal rat dorsal root ganglion neurones: a role for non-neuronal cells as nociceptors. Journal of Physiology 536, 111–121.CrossRefGoogle ScholarPubMed
Igarashi, M., Strittmatter, S.M., Vartanian, T. and Fishman, M.C. (1993) Mediation by G proteins of signals that cause collapse of growth cones. Science 259, 77–79.CrossRefGoogle ScholarPubMed
Julius, D. and Basbaum, A.I. (2001) Molecular mechanisms of nociception. Nature 413, 203–210.CrossRefGoogle ScholarPubMed
Kimpinski, K. and Mearow, K. (2001) Neurite growth promotion by nerve growth factor and insulin-like growth factor-1 in cultured adult sensory neurons: role of phosphoinositide 3-kinase and mitogen activated protein kinase. Journal of Neuroscience 63, 486–499.Google ScholarPubMed
Kindt, R.M. and Lander, A.D. (1995) Pertussis toxin specifically inhibits growth cone guidance by a mechanism independent of direct G protein inactivation. Neuron 15, 79–88.CrossRefGoogle ScholarPubMed
Leclere, P.G., Norman, E., Groutsi, F., Coffin, R., Mayer, U., Pizzey, J. et al. (2007) Impaired axonal regeneration by isolectin B4-binding dorsal root ganglion neurons in vitro. Journal of Neuroscience 27, 1190–1199.CrossRefGoogle ScholarPubMed
Lindsay, R.M. (1988) Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurons. Journal of Neuroscience 8, 2394–2405.CrossRefGoogle Scholar
Lotto, B., Upton, L., Price, D.J. and Gaspar, P. (1999) Serotonin receptor activation enhances neurite outgrowth of thalamic neurones in rodents. Neuroscience Letters 269, 87–90.CrossRefGoogle ScholarPubMed
Lu, X. and Richardson, P.M. (1991) Inflammation near the nerve cell body enhances axonal regeneration. Journal of Neuroscience 11, 972–978.CrossRefGoogle ScholarPubMed
Molliver, D.C., Wright, D.E., Leitner, M.L., Parsadanian, A.S., Doster, K., Wen, D. et al. (1997) IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19, 849–861.CrossRefGoogle ScholarPubMed
Nascimento, R.S., Santiago, M.F., Marques, S.A., Allodi, S. and Martinez, A.M.B. (2008) Diversity among satellite glial cells in dorsal root ganglia of the rat. Brazilian Journal of Medical Biology Research 41, 1011–1017.CrossRefGoogle ScholarPubMed
Nave, K.A. and Trapp, B.D. (2008) Axon–glial signaling and the glial support of axon function. Annual Review of Neuroscience 31, 535–561.CrossRefGoogle ScholarPubMed
Priestley, J.V., Michael, G.J., Averill, S., Liu, M. and Willmott, N. (2002) Regulation of nociceptive neurons by nerve growth factor and glial cell line derived neurotrophic factor. Canadian Journal of Physiology and Pharmacology 80, 495–505.CrossRefGoogle ScholarPubMed
Raye, W.S., Tochon-Danguy, N., Pouton, C.W. and Haynes, J.M. (2007) Heterogeneous population of dopaminergic neurons derived from mouse embryonic stem cells: preliminary phenotyping based on receptor expression and function. European Journal of Neuroscience 25, 1961–1970.CrossRefGoogle ScholarPubMed
Rowlands, D.K., Kao, C.L. and Wise, H. (2001) Regulation of prostacyclin and prostaglandin E2 receptor mediated responses in adult rat dorsal root ganglion cells, in vitro. British Journal of Pharmacology 133, 13–22.CrossRefGoogle ScholarPubMed
Snider, W.D. and McMahon, S.B. (1998) Tackling pain at the source: new ideas about nociceptors. Neuron 20, 629–632.CrossRefGoogle ScholarPubMed
Strittmatter, S.M., Fishman, M.C. and Zhu, X.-P. (1994) Activated mutants of the α subunit of Go promote an increased number of neurites per cell. Journal of Neuroscience 14, 2327–2338.CrossRefGoogle ScholarPubMed
Stucky, C.L. and Lewin, G.R. (1999) Isolectin B4-positive and -negative nociceptors are functionally distinct. Journal of Neuroscience 19, 6497–6505.CrossRefGoogle Scholar
Swarzenski, B.C., O'Malley, K.L. and Todd, R.D. (1996) PTX-sensitive regulation of neurite outgrowth by the dopamine D3 receptor. NeuroReport 7, 573–576.CrossRefGoogle ScholarPubMed
Tamura, M., Nogimori, K., Murai, S., Yajima, M., Ito, K., Katada, T. et al. (1982) Subunit structure of islet-activating protein, pertussis toxin, in comformity with the A-B model. Biochemistry 21, 5516–5522.CrossRefGoogle Scholar
Tang, H.B., Li, Y.S. and Nakata, Y. (2007) The release of substance P from cultured dorsal root ganglion neurons requires the non-neuronal cells around these neurons. Journal of Pharmacological Sciences 105, 264–271.CrossRefGoogle ScholarPubMed
Tucker, B.A., Rahimtula, M. and Mearow, K.M. (2005) A procedure for selecting and culturing subpopulations of neurons from rat dorsal root ganglia using magnetic beads. Brain Research Protocols 16, 50–57.CrossRefGoogle ScholarPubMed
Tucker, B.A., Rahimtula, M. and Mearow, K.M. (2006) Laminin and growth factor receptor activation stimulates differential growth responses in subpopulations of adult DRG neurons. European Journal of Neuroscience 24, 676–690.CrossRefGoogle ScholarPubMed
Vesce, S., Bezzi, P. and Volterra, A. (2001) Synaptic transmission with the glia. News Physiological Sciences 16, 178–184.Google ScholarPubMed
Watkins, L.R., Hutchinson, M.R., Milligan, E.D. and Maier, S.F. (2007) “Listening” and “talking” to neurons: implications of immune activation for pain control and increasing the efficacy of opioids. Brain Research Reviews 56, 148–169.CrossRefGoogle ScholarPubMed
Wewetzer, K., Lausch, M. and Christ, B. (1999) Macrowell cultures identify a subpopulation of neonatal rat dorsal root ganglionic neurons displaying nerve growth factor independent survival. Neuroscience Letters 276, 9–12.CrossRefGoogle ScholarPubMed
Wise, H. (2006) Lack of interaction between prostaglandin E2 receptor subtypes in regulating adenylyl cyclase activity in cultured rat dorsal root ganglion cells. European Journal of Pharmacology 535, 69–77.CrossRefGoogle ScholarPubMed
Wong, W.S.F. and Rosoff, P.M. (1996) Pharmacology of pertussis toxin B-oligomer. Canadian Journal of Physiology and Pharmacology 74, 559–564.CrossRefGoogle ScholarPubMed
Wu, D., Zhang, Y., Bo, X., Huang, W., Xiao, F., Zhang, X. et al. (2007) Actions of neuropoietic cytokines and cyclic AMP in regenerative conditioning of rat primary sensory neurons. Experimental Neurology 204, 66–76.CrossRefGoogle ScholarPubMed
Zhang, X., Chen, Y., Wang, C. and Huang, L.-Y.M. (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.CrossRefGoogle ScholarPubMed