Trophic factors attenuate nitric oxide mediated neuronal and axonal injury in vitro: Roles and interactions of mitogen-activated protein kinase signalling pathways

Journal of Neurochemistry

Volumn 92, Issue 6, 2005, Pages 1487-1496

  Wilkins, Alastair ^a   Compston, Alastair ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Axon; Inflammation; Mitogen activated protein kinase; Neurone; Neuroprotection; Trophic

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUROPROTECTIVE AGENT; NITRIC OXIDE; OLIGODENDROCYTE CONDITIONED MEDIUM; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN CELL; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; NERVE INJURY; NEUROPATHY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; CYTOPROTECTION; DEMYELINATING DISEASES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENCEPHALITIS; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; INSULIN-LIKE GROWTH FACTOR I; MAP KINASE SIGNALING SYSTEM; MODELS, NEUROLOGICAL; NERVE GROWTH FACTORS; NEURONS; NITRIC OXIDE; NITRIC OXIDE DONORS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS; WALLERIAN DEGENERATION;

EID: 15144362148     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02981.x     Document Type: Article

References (50)

1. Bagasra O., Michaels F. H., Zheng Y. M., Bobroski L. E., Spitsin S. V., Fu Z. F., Tawadros R. and Koprowski H. (1995) Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proc. Natl Acad. Sci. USA 92, 12 041-12 045.
2. Bal-Price A. and Brown G. C. (2001) Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J. Neurosci. 21, 6480-6491.
3. Bauer J., Rauschka H. and Lassmann H. (2001) Inflammation in the nervous system: the human perspective. Glia 36, 235-243.
4. Bossy-Wetzel E., Talantova M. V., Lee W. D. et al. (2004) Crosstalk between nitric oxide and zinc pathways to neuronal cell death involving mitochondrial dysfunction and p38-activated K+ channels. Neuron 41, 351-365.
5. Brady S. T., Wirt A. S., Kirkpatrick L. L., de Waegh S. M., Readhead C., Tu P. H. and Lee V. M. (1999) Formation of compact myelin is required for maturation of the axonal cytoskeleton. J. Neurosci. 19, 7278-7288.
6. Brown G. C. and Borutaite V. (2002) Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Radic. Biol. Med. 33, 1440-1450.
7. Byravan S., Foster L. M., Phan T., Verity A. N. and Campagnoni A. T. (1994) Murine oligodendroglial cells express nerve growth factor. Proc. Natl Acad. Sci. USA 91, 8812-8816.
8. Canoll P. D., Musacchio J. M., Hardy R., Reynolds R., Marchionni M. A. and Salzer J. L. (1996) GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 17, 229-243.
9. Cao L., Liu L., Chen Z. Y., Wang L. M., Ye J. L., Qiu H. Y., Lu C. L. and He C. (2004) Olfactory ensheathing cells genetically modified to secrete GDNF to promote spinal cord repair. Brain 127, 535-549.
10. Carden M. J., Trojanowski J. Q., Schlaepfer W. W. and Lee V. M. (1987) Two-stage expression of neurofilament polypeptides during rat neurogenesis with early establishment of adult phosphorylation patterns. J. Neurosci. 7, 3489-3504.
11. Colello R. J., Pott U. and Schwab M. E. (1994) The role of oligodendrocytes and myelin on axon maturation in the developing rat retinofugal pathway. J. Neurosci. 14, 2594-2605.
12. Creedon D. J., Johnson E. M. and Lawrence J. C. (1996) Mitogen-activated protein kinase-independent pathways mediate the effects of nerve growth factor and cAMP on neuronal survival. J. Biol. Chem. 271, 20 713-20 718.
13. Davie C. A. G. J., Barker S., Webb P. S., Tofts A. J., Thompson A. J., Harding A. E., McDonald W. I. and Miller D. H. (1995) Persistent functional deficit in multiple sclerosis and autosomal dominant cerebellar ataxia is associated with axon loss. Brain 118, 1583-1592.
14. Dudek H., Datta S. R., Franke T. F., Birnbaum M. J., Yao R., Cooper G. M., Segal R. A., Kaplan D. R. and Greenberg M. E. (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275, 661-665.
15. Estevez A. G., Spear N., Manuel S. M., Radi R., Henderson C. E., Barbeito L. and Beckman J. S. (1998) Nitric oxide and superoxide contribute to motor neuron apoptosis induced by trophic factor deprivation. J. Neurosci. 18, 923-931.
16. Finn J. T., Weil M., Archer F., Siman R., Srinivasan A. and Raff M. C. (2000) Evidence that Wallerian degeneration and localized axon degeneration induced by local neurotrophin deprivation do not involve caspases. J. Neurosci. 20, 1333-1341.
17. Garthwaite G., Goodwin D. A., Batchelor A. M., Leeming K. and Garthwaite J. (2002) Nitric oxide toxicity in CNS white matter: an in vitro study using rat optic nerve. Neuroscience 109, 145-155.
18. Ghatan S., Larner S., Kinoshita Y., Hetman M., Patel L., Xia Z., Youle R. J. and Morrison R. S. (2000) p38 MAP kinase mediates bax translocation in nitric oxide-induced apoptosis in neurons. J. Cell Biol. 150, 335-347.
19. Golde S., Chandran S., Brown G. C. and Compston A. (2002) Different pathways for iNOS-mediated toxicity in vitro dependent on neuronal maturation and NMDA receptor expression. J. Neurochem. 82, 269-282.
20. Ishikawa Y., Kusaka E., Enokido Y., Ikeuchi T. and Hatanaka H. (2003) Regulation of Bax translocation through phosphorylation at Ser-70 of Bcl-2 by MAP kinase in NO-induced neuronal apoptosis. Mol. Cell. Neurosci. 24, 451-459.
21. Kaplan M. R., Meyer-Franke A., Lambert S., Bennett V., Duncan I. D., Levinson S. R. and Barres B. A. (1997) Induction of sodium channel clustering by oligodendrocytes. Nature 386, 724-728.
22. Kapoor R., Davies M., Blaker P. A., Hall S. M. and Smith K. J. (2003) Blockers of sodium and calcium entry protect axons from nitric oxide-mediated degeneration. Ann. Neurol. 53, 174-180.
23. Kerschensteiner M., Stadelmann C., Dechant G., Wekerle H. and Hohlfeld R. (2003) Neurotrophic cross-talk between the nervous and immune systems: implications for neurological diseases. Ann. Neurol. 53, 292-304.
24. Komoly S., Hudson L. D., Webster H. D. and Bondy C. A. (1992) Insulin-like growth factor I gene expression is induced in astrocytes during experimental demyelination. Proc. Natl Acad. Sci. USA 89, 1894-1898.
25. Koprowski H., Zheng Y. M., Heber-Katz E., Fraser N., Rorke L., Fu Z. F., Hanlon C. and Dietzschold B. (1993) In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases. Proc. Natl Acad. Sci. USA 90, 3024-3027.
26. Komek B. and Lassmann H. (2003) Neuropathology of multiple sclerosis-new concepts. Brain Res. Bull. 61, 321-326.
27. Komek B., Storch M. K., Weissert R., Wallstroem E., Stefferl A., Olsson T., Linington C., Schmidbauer M. and Lassmann H. (2000) Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive and remyelinated lesions. Am. J. Pathol. 157, 267-276.
28. Lee V. M., Carden M. J., Schlaepfer W. W. and Trojanowski J. Q. (1987) Monoclonal antibodies distinguish several differentially phosphorylated states of the two largest rat neurofilament subuntts (NF-H and NF-M) and demonstrate their existence in the normal nervous system of adult rats. J. Neurosci. 7, 3474-3488.
29. Li B. S., Veeranna J., Gu P., Grant and Pant H. C. (1999) Activation of mitogen-acttvated protein kinases (Erk1 and Erk2) cascade results in phosphorylation of NF-M tail domains in transfected NIH 3T3 cells. Eur. J. Biochem. 262, 211-217.
30. Li S. P., Junttila M. R., Han J., Kahari V. M. and Westermarck J. (2003) p38 Mitogen-activated protein kinase pathway suppresses cell survival by inducing dephosphorylation of mitogen-activated protein/extracellular signal-regulated kinase kinase 1,2. Cancer Res. 63, 3473-3477.
31. Lin L. F., Doherty D. H., Lile J. D., Bektesh S. and Collins F. (1993) GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260, 1130-1132.
32. Lin S., Zhang Y., Dodel R., Farlow M. R., Paul S. M., and Du Y. (2001) Minocycline blocks nitric oxide-induced neurotoxicity by inhibition p38 MAP kinase in rat cerebellar granule neurons. Neurosci. Lett. 315, 61-64.
33. Lindholm D., Carroll P., Tzimagiogis G. and Thoenen H. (1996) Autocrine-paracrine regulation of hippocampal neuron survival by IGF-1 and the neurotrophins BDNF, NT-3 and NT-4. Eur. J. Neurosci. 8, 1452-1460.
34. Matsuzaki H., Tamatani M., Mitsuda N., Namikawa K., Kiyama H., Miyake S. and Tohyama M. (1999) Activation of Akt kinase inhibits apoptosis and changes in Bcl-2 and Bax expression induced by nitric oxide in primary hippocampal neurons. J. Neurochem. 73, 2037-2046.
35. McCarthy K. D. and de Vellis J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902.
36. Meyer-Franke A., Kaplan M. R., Pfrieger F. W. and Barres B. A. (1995) Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 15, 805-819.
37. Nicole O., Docagne F., Plawinski L., Mackenzie E. T., Vivien D. and Buisson A. (2001) Neuroprotection mediated by glial cell line-derived neurotrophic factor: involvement of a reduction of NMDA-induced calcium influx by the mitogen-activated protein kinase pathway. J. Neurosci. 21, 3024-3033.
38. Redford E. J., Kapoor R. and Smith K. J. (1997) Nitric oxide donors reversibly block axonal conduction: demyelinated axons are especially susceptible. Brain 120, 2149-2157.
39. Sanchez I., Hassinger L., Paskevich P. A., Shine H. D. and Nixon R. A. (1996) Oligodendroglia regulate the regional expansion of axon caliber and local accumulation of neurofilaments during development independently of myelin formation. J. Neurosci. 16, 5095-5105.
40. Smith K. J. and Lassmann H. (2002) The role of nitric oxide in multiple sclerosis. Lancet Neuril. 1, 232-241.
41. Smith K. J., Kapoor R., Hall S. M. and Davies M. (2001) Electrically active axons degenerate when exposed to nitric oxide. Ann. Neurol. 49, 470-476.
42. Strelau J. and Unsicker K. (1999) GDNF family members and their receptors: expression and functions in two oligodendroglial cell lines representing distinct stages of oligodendroglial development. Glia 26, 291-301.
43. Trapp B. D., Peterson J., Ransohoff R. M., Rudick R., Mork S. and Bo L. (1998) Axonal transecrion in the lesions of multiple sclerosis. N. Engl. J. Med. 338, 278-285.
44. Veeranna N. D., Amin N. G., Ahn H., Jaffe C. A., Winters P., Grant and Pant H. C. (1998) Mitogen-activated protein kinases (Erk1,2) phosphorylate Lys-Ser-Pro (KSP) repeats in neurofilament proteins NF-H and NF-M. J. Neurosci. 18, 4008-4021.
45. Wang L. J., Lu Y. Y., Muramatsu S. et al. (2002) Neuroprotective effects of glial cell line-derived neurotrophic factor mediated by an adeno-associated virus vector in a transgenic animal model of amyotrophic lateral sclerosis. J. Neurosci. 22, 6920-6928.
46. Wang J. Y., Shum A. Y., Ho Y. J. and Wang J. Y. (2003) Oxidative neurotoxicity in rat cerebral cortex neurons: synergistic effects of H2O2 and NO on apoptosis involving activation of p38 mitogen-activated protein kinase and caspase-3. J. Neurosci. Res. 72, 508-519.
47. Waxman S. G. (2003) Nitric oxide and the axonal death cascade. Ann. Neurol. 53, 150-153.
48. Wilkins A., Chandran S. and Compston A. (2001) A role for oligodendrocyte-derived IGF-1 in trophic support of cortical neurons. Glia 36, 48-57.
49. Wilkins A., Majed H., Layfield R., Compston A. and Chandran S. (2003) Oligodendrocytes promote neuronal survival and axonal length by distinct intracellular mechanisms: a novel role for oligodendrocyte-derived glial cell line-derived neurotrophic factor. J. Neurosci. 23, 4967-4974.
50. Yamagishi S., Matsumoto T., Yokomaku D., Hatanaka H., Shimoke K., Yamada M. and Ikeuchi T. (2003) Comparison of inhibitory effects of brain-derived neurotrophic factor and insulin-like growth factor on low potassium-induced apoptosis and activation of p38 MAPK and C-Jun in cultured cerebellar granule neurons. Brain Res. Mol. Brain Res. 119, 184-191.