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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

Published online by Cambridge University Press:  01 February 2010

Matthew J.G. Bradman ,
Daleep K. Arora ,
Richard Morris  and
Thimmasettappa Thippeswamy
Matthew J.G. Bradman
Affiliation:
Department of Animal Health and Welfare, School of Veterinary Science, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UK
Daleep K. Arora
Affiliation:
Department of Animal Health and Welfare, School of Veterinary Science, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UK
Richard Morris
Affiliation:
Department of Animal Health and Welfare, School of Veterinary Science, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UK
Thimmasettappa Thippeswamy*
Affiliation:
Department of Animal Health and Welfare, School of Veterinary Science, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UK
*
Correspondence should be addressed to: Thimmasettappa Thippeswamy, Department of Animal Health and Welfare, School of Veterinary Science, Faculty of Health and Life Sciences, University of Liverpool, Crown Street, Liverpool L69 7ZJ, UK phone: 00 44 151 794 4242 fax: 0044 151 794 4243 email: [email protected]
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Abstract

Dorsal root ganglia (DRG) respond to peripheral nerve injury by up-regulating nitric oxide (NO) production by neurons and glia in addition to local fibroblasts, endothelium and macrophages. We hypothesise that NO produced from these cells has specific roles. We have shown that when neuronal NO synthase (nNOS) is blocked in axotomised DRG, neurons undergo degenerative changes (Thippeswamy et al., 2001, 2007a). Further, we demonstrated that increased neuronal NO production, in response to axotomy/growth factor-deprivation in vitro, signals glial cells to produce trophic factors to support neuronal survival (Thippeswamy et al., 2005a). Recently, we found that treating satellite glia–neuron co-cultures with nNOS inhibitor, 7-nitroindazole (7NI), decreases the number of nestin+ cells that show neuron-like morphology. Cultured/axotomised DRG also upregulate inducible NOS (iNOS) in non-neuronal cells. Therefore, it is plausible that degenerative changes following nNOS inhibition are also due to iNOS-mediated excessive NO production by non-neuronal cells, which indeed is cytotoxic. NG-nitro-l-arginine methylester (L-NAME), the pan NOS inhibitor did not significantly change nNOS+ neuron number in axotomised DRG compared to 7NI suggesting that iNOS-mediated NO contributes to the degenerative process. In this paper, these findings from our and others' past work on NO-mediated neuron–glia signalling in axotomised DRG are discussed.

Keywords

Neuroprotectionneuron–glia communicationaxotomyneurotrophic factorDRG
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Special Issue 1: Satellite Glial Cells , February 2010 , pp. 11 - 17
Copyright
Copyright © Cambridge University Press 2010

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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
Bacon, A., Kerr, N.C., Holmes, F.E., Gaston, K. and Wynick, D. (2007) Characterization of an enhancer region of the galanin gene that directs expression to the dorsal root ganglion and confers responsiveness to axotomy. Journal of Neuroscience 27, 6573–6580.Google Scholar
Ballas, N., Grunseich, C., Lu, D.D., Speh, J.C. and Mandel, G. (2005) REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121, 645–657.CrossRefGoogle ScholarPubMed
Boer, R., Ulrich, W.R., Klein, T., Mirau, B., Haas, S. and Baur, I. (2000) The inhibitory potency and selectivity of arginine substrate site nitric-oxide synthase inhibitors is solely determined by their affinity toward the different isoenzymes. Molecular Pharmacology 58, 1026–1034.Google Scholar
Bredt, D.S. and Snyder, S.H. (1994) Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia, and olfactory epithelium. Neuron 13, 301–313.CrossRefGoogle ScholarPubMed
Elliott-Hunt, C.R., Marsh, B., Bacon, A., Pope, R., Vanderplank, P. and Wynick, D. (2004) Galanin acts as a neuroprotective factor to the hippocampus. Proceedings of the National Academy of Sciences of the U.S.A. 101, 5105–5110.CrossRefGoogle ScholarPubMed
Ernsberger, U. (2009) Role of neurotrophin signalling in the differentiation of neurons from dorsal root ganglia and sympathetic ganglia. Cell Tissue Research 336, 349–384.Google Scholar
Garthwaite, J. (2008) Concepts of neural nitric oxide-mediated transmission. European Journal of Neuroscience 27, 2783–2802.CrossRefGoogle ScholarPubMed
Gouge, R.C., Marshburn, P., Gordon, B.E., Nunley, W. and Huet-Hudson, Y.M. (1998) Nitric oxide as a regulator of embryonic development. Biology of Reproduction 58, 875–879.CrossRefGoogle ScholarPubMed
Gutièrrez-Mecinas, M., Crespo, C., Blasco-Ibáñez, J.M., Nácher, J., Varea, E. and Martínez-Guijarro, F.J. (2007) Migrating neuroblasts of the rostral migratory stream are putative targets for the action of nitric oxide. European Journal of Neuroscience, 26, 392–402.Google Scholar
Halpern, M.E., Thisse, C., Ho, R.K., Thisse, B., Riggleman, B., Trevarrow, B. et al. (1995) Cell-autonomous shift from axial to paraxial mesodermal development in zebrafish floating head mutants. Development 121, 4257–4264.Google Scholar
Hu, P. and McLachlan, E.M. (2003) Selective reactions of cutaneous and muscle afferent neurons to peripheral nerve transection in rats. Journal of Neuroscience 23, 10559–10567.CrossRefGoogle ScholarPubMed
Kalcheim, C. and Teillet, M.A. (1989) Consequences of somite manipulation on the pattern of dorsal root ganglion development. Development 106, 85–93.CrossRefGoogle ScholarPubMed
Koesling, D., Russwurm, M., Mergia, E., Mullershausen, F. and Friebe, A. (2004) Nitric oxide-sensitive guanylyl cyclase: structure and regulation. Neurochemistry International 45, 813–819.Google Scholar
Lewin, G.R. and Barde, Y.A. (1996) Physiology of the neurotrophins. Annual Review of Neuroscience 19, 289–317.CrossRefGoogle ScholarPubMed
Liuzzi, F.J. and Tedeschi, B. (1991) Peripheral nerve regeneration. Neurosurgery Clinics of North America 2, 31–42.CrossRefGoogle ScholarPubMed
Ma, Q., Fode, C., Guillemot, F. and Anderson, D.J. (1999) Neurogenin1 and neurogenin2 control two distinct waves of neurogenesis in developing dorsal root ganglia. Genes Development 13, 1717–1728.Google Scholar
Memberg, S.P. and Hall, A.K. (1995) Proliferation, differentiation, and survival of rat sensory neuron precursors in vitro require specific trophic factors. Molecular and Cellular Neuroscience 6, 323–335.Google Scholar
Moreno-Lopez, B., Noval, J.A., González-Bonet, L.G. and Estrada, C. (2000) Morphological bases for a role of nitric oxide in adult neurogenesis. Brain Research 869, 244–250.Google ScholarPubMed
Nott, A., Watson, P.M., Robinson, J.D., Crepaldi, L. and Riccio, A. (2008) S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455, 411–415.Google Scholar
Packer, M.A., Stasiv, Y., Benraiss, A., Chmielnicki, E., Grinberg, A., Westphal, H. et al. (2003) Nitric oxide negatively regulates mammalian adult neurogenesis. Proceedings of the National Academy of Sciences of the U.S.A. 100, 9566–9571.CrossRefGoogle ScholarPubMed
Palm, K., Belluardo, N., Metsis, M. and Timmusk, T. (1998) Neuronal expression of zinc finger transcription factor REST/NRSF/XBR gene. Journal of Neuroscience 18, 1280–1296.Google Scholar
Pannese, E. (ed.) (1981) The Satellite Cells of the Sensory Ganglia. Berlin: Springer-Verlag.Google Scholar
Perez, S.E., Rebelo, S. and Anderson, D.J. (1999) Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development 126, 1715–1728.CrossRefGoogle ScholarPubMed
Pirondi, S., Fernandez, M., Schmidt, R., Hokfelt, T., Giardino, L. and Calza, L. (2005) The galanin-R2 agonist AR-M1896 reduces glutamate toxicity in primary neural hippocampal cells. Journal of Neurochemistry 95, 821–833.CrossRefGoogle ScholarPubMed
Romero-Grimaldi, C., Moreno-López, B. and Estrada, C. (2008) Age-dependent effect of nitric oxide on subventricular zone and olfactory bulb neural precursor proliferation. Journal of Comparative Neurology 506, 339–346.Google Scholar
Roy, B., Halvey, E.J. and Garthwaite, J. (2008) An enzyme-linked receptor mechanism for nitric oxide-activated guanylyl cyclase. Journal of Biological Chemistry 283, 18841–18851.CrossRefGoogle ScholarPubMed
Russwurm, M. and Koesling, D. (2004) NO activation of guanylyl cyclase. EMBO Journal 23, 4443–4450.CrossRefGoogle ScholarPubMed
Schäfers, M., Geis, C., Brors, D., Yaksh, T.L. and Sommer, C. (2002) Anterograde transport of tumor necrosis factor-alpha in the intact and injured rat sciatic nerve. Journal of Neuroscience 22, 536–545.CrossRefGoogle ScholarPubMed
Talbot, W.S., Trevarrow, B., Halpern, M.E., Melby, A.E., Farr, G., Postlethwait, J.H. et al. (1995) A homeobox gene essential for zebrafish notochord development. Nature 378, 150–157.CrossRefGoogle ScholarPubMed
Thippeswamy, T., Haddley, K., Corness, J.D., Howard, M.R., McKay, J.S., Beaucourt, S.M. et al. (2007a) NO-cGMP mediated galanin expression in NGF-deprived or axotomized sensory neurons. Journal of Neurochemistry 100, 790–801.CrossRefGoogle ScholarPubMed
Thippeswamy, T., Howard, M.R., Cosgrave, A.S., Arora, D.K., McKay, J.S. and Quinn, J.P. (2007b) Nitric oxide-NGF mediated PPTA/SP, ADNP, and VIP expression in the peripheral nervous system. Journal of Molecular Neuroscience 33, 268–277.Google Scholar
Thippeswamy, T., Jain, R.K., Mumtaz, N. and Morris, R. (2001) Inhibition of neuronal nitric oxide synthase results in neurodegenerative changes in the axotomised dorsal root ganglion neurons: evidence for a neuroprotective role of nitric oxide in vivo. Neuroscience Research 40, 37–44.Google Scholar
Thippeswamy, T., McKay, J.S., Quinn, J. and Morris, R. (2005a) Either nitric oxide or nerve growth factor is required for dorsal root ganglion neurons to survive during embryonic and neonatal development. Brain Research Development. Brain Research 154, 153–164.CrossRefGoogle ScholarPubMed
Thippeswamy, T., McKay, J.S., Morris, R., Quinn, J., Wong, L.F. and Murphy, D. (2005b) Glial-mediated neuroprotection: Evidence for the protective role of the NO–cGMP pathway via neuron–glial communication in the peripheral nervous system. Glia 49, 197–210.Google Scholar
Thippeswamy, T. and Morris, R. (1997a) Nerve growth factor inhibits the expression of nitric oxide synthase in neurones in dissociated cultures of rat dorsal root ganglia. Neuroscience Letters 230, 9–12.CrossRefGoogle ScholarPubMed
Thippeswamy, T. and Morris, R. (1997b) Cyclic guanosine 3′,5′-monophosphate-mediated neuroprotection by nitric oxide in dissociated cultures of rat dorsal root ganglion neurones. Brain Research 774, 116–122.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.Google Scholar
Tong, J.X., Eichler, M.E. and Rich, K.M. (1996) Intracellular calcium levels influence apoptosis in mature sensory neurons after trophic factor deprivation. Experimental Neurology 138, 45–52.Google Scholar
Tran, E.H., Hardin-Pouzet, H., Verge, G. and Owens, T. (1997) Astrocytes and microglia express inducible nitric oxide synthase in mice with experimental allergic encephalomyelitis. Journal of Neuroimmunology 74, 121–129.Google Scholar
Ungos, J.M., Karlstrom, R.O. and Raible, D.W. (2003) Hedgehog signaling is directly required for the development of zebrafish dorsal root ganglia neurons. Development 130, 5351–5362.CrossRefGoogle ScholarPubMed
Verge, V.M., Xu, Z., Xu, X.J., Wiesenfeld, H.Z. and Hokfelt, T. (1992) Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies. Proceedings of the National Academy of Sciences of the U.S.A. 89, 11617–11621.Google Scholar
Zhang, X., Aman, K. and Hökfelt, T. (1995) Secretory pathways of neuropeptides in rat lumbar dorsal root ganglion neurons and effects of peripheral axotomy. Journal of Comparative Neurology 352, 481–500.Google Scholar
Zhang, X., Verge, V.M., Wiesenfeld, H.Z., Ju, G., Bredt, D., Synder, S.H. et al. (1993) Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. Journal of Comparative Neurology 335, 563–575.Google Scholar