Tumor necrosis factor alpha and interferon gamma cooperatively induce oxidative stress and motoneuron death in rat spinal cord embryonic explants

Neuroscience

Volumn 162, Issue 4, 2009, Pages 959-971

  Mir, M ^a   Asensio, V J ^a   Tolosa, L ^a   Gou Fabregas, M ^b   Soler, R M ^b   Llado J ^a   Olmos, G ^a  

^a Grup de Neurobiologia Cellular   (Spain)

^b Facultat de Medicina   (Spain)

Author keywords

amyotrophic lateral sclerosis; microglia; neuroinflammation; nitric oxide; proinflammatory cytokines

Indexed keywords

3 NITROTYROSINE; CASPASE 3; CYCLOOXYGENASE 2; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOCORTIN 5; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TUMOR NECROSIS FACTOR ALPHA;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL VIABILITY; CHRONIC INFLAMMATION; CONTROLLED STUDY; CULTURE TECHNIQUE; EMBRYO; EXPLANT; GLIA CELL; IMMUNOREACTIVITY; MICROGLIA; MONOLAYER CULTURE; MOTONEURON; MOUSE; NERVE CELL NECROSIS; NITRATION; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD;

ANIMALS; APOPTOSIS; CELL MOVEMENT; CELL SURVIVAL; CULTURE MEDIA; EMBRYO, MAMMALIAN; INTERFERON-GAMMA; MICROGLIA; MOTOR NEURONS; NITRIC OXIDE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TISSUE CULTURE TECHNIQUES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 67949100439     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.05.049     Document Type: Article

References (71)

1. Almer G., Vukosavic S., Romero N., and Przedborski S. Inducible nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 72 (1999) 2415-2425
2. Arce V., Garces A., de Bovis B., Filippi P., Henderson C., and Pettmann B deLapeyriere O. Cardiotrophin-1 requires LIFRbeta to promote survival of mouse motoneurons purified by a novel technique. J Neurosci Res 55 (1999) 119-126
3. Babu G.N., Kumar A., Chandra R., Puri S.K., Kalita J., and Misra U.K. Elevated inflammatory markers in a group of amyotrophic lateral sclerosis patients from northern India. Neurochem Res 33 (2008) 1145-1149
4. Banerjee R., Mosley R.L., Reynolds A.D., Dhar A., Jackson-Lewis V., Gordon P.H., Przedborski S., and Gendelman H.E. Adaptive immune neuroprotection in G93A-SOD1 amyotrophic lateral sclerosis mice. PLoS ONE 3 (2008) e2740
5. Bao F., and Liu D. Peroxynitrite generated in the rat spinal cord induces apoptotic cell death and activates caspase-3. Neuroscience 116 (2003) 59-70
6. Bar-Peled O., Knudson M., Korsmeyer S.J., and Rothstein J.D. Motor neuron degeneration is attenuated in bax-deficient neurons in vitro. J Neurosci Res 55 (1999) 542-556
7. Beal M.F., Ferrante R.J., Browne S.E., Matthews R.T., Kowall N.W., and Brown Jr. R.H. Increased 3-nitrotyrosine in both sporadic and familial amyotrophic lateral sclerosis. Ann Neurol 42 (1997) 644-654
8. Bentz B.G., Simmons R.L., Haines III G.K., and Radosevich J.A. The yin and yang of nitric oxide: reflections on the physiology and pathophysiology of NO. Head Neck 22 (2000) 71-83
9. Boillee S., Vande Velde C., and Cleveland D.W. ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52 (2006) 39-59
10. Cha C.I., Chung Y.H., Shin C.M., Shin D.H., Kim Y.S., Gurney M.E., and Lee K.W. Immunocytochemical study on the distribution of nitrotyrosine in the brain of the transgenic mice expressing a human Cu/Zn SOD mutation. Brain Res 853 (2000) 156-161
11. Consilvio C., Vincent A.M., and Feldman E.L. Neuroinflammation, COX-2, and ALS-a dual role?. Exp Neurol 187 (2004) 1-10
12. Cookson M.R., Menzies F.M., Manning P., Eggett C.J., Figlewicz D.A., McNeil C.J., and Shaw P.J. Cu/Zn superoxide dismutase (SOD1) mutations associated with familial amyotrophic lateral sclerosis (ALS) affect cellular free radical release in the presence of oxidative stress. Amyotroph Lateral Scler Other Motor Neuron Disord 3 (2002) 75-85
13. Dawson V.L., and Dawson T.M. Nitric oxide in neurodegeneration. Prog Brain Res 118 (1998) 215-229
14. De Paola M., Diana V., Bigini P., and Mennini T. Morphological features and responses to AMPA receptor-mediated excitotoxicity of mouse motor neurons: comparison in purified, mixed anterior horn or motor neuron/glia cocultures. J Neurosci Methods 170 (2008) 85-95
15. Elliott J.L. Cytokine upregulation in a murine model of familial amyotrophic lateral sclerosis. Brain Res Mol Brain Res 95 (2001) 172-178
16. Emerit J., Edeas M., and Bricaire F. Neurodegenerative diseases and oxidative stress. Biomed Pharmacother 58 (2004) 39-46
17. Ferri A., Nencini M., Cozzolino M., Carrara P., Moreno S., and Carri M.T. Inflammatory cytokines increase mitochondrial damage in motoneuronal cells expressing mutant SOD1. Neurobiol Dis 32 (2008) 454-460
18. Francisco-Morcillo J., Hidalgo-Sanchez M., and Martin-Partido G. Spatial and temporal patterns of proliferation and differentiation in the developing turtle eye. Brain Res 1103 (2006) 32-48
19. Gauss K.A., Nelson-Overton L.K., Siemsen D.W., Gao Y., DeLeo F.R., and Quinn M.T. Role of NF-kappaB in transcriptional regulation of the phagocyte NADPH oxidase by tumor necrosis factor-alpha. J Leukoc Biol 82 (2007) 729-741
20. Ghezzi P., and Mennini T. Tumor necrosis factor and motoneuronal degeneration: an open problem. Neuroimmunomodulation 9 (2001) 178-182
21. Gibbons H.M., and Dragunow M. Microglia induce neural cell death via a proximity-dependent mechanism involving nitric oxide. Brain Res 1084 (2006) 1-15
22. Gowing G., Dequen F., Soucy G., and Julien J.P. Absence of tumor necrosis factor-alpha does not affect motor neuron disease caused by superoxide dismutase 1 mutations. J Neurosci 26 (2006) 11397-11402
23. Graves M.C., Fiala M., Dinglasan L.A., Liu N.Q., Sayre J., Chiappelli F., van Kooten C., and Vinters H.V. Inflammation in amyotrophic lateral sclerosis spinal cord and brain is mediated by activated macrophages, mast cells and T cells. Amyotroph Lateral Scler Other Motor Neuron Disord 5 (2004) 213-219
24. 15N]nitrate in biological fluids. Anal Biochem 126 (1982) 131-138
25. Hall E.D., Oostveen J.A., and Gurney M.E. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23 (1998) 249-256
26. Hanisch U.K. Microglia as a source and target of cytokines. Glia 40 (2002) 140-155
27. Hartig W., Stieler J., Boerema A.S., Wolf J., Schmidt U., Weissfuss J., Bullmann T., Strijkstra A.M., and Arendt T. Hibernation model of tau phosphorylation in hamsters: selective vulnerability of cholinergic basal forebrain neurons-implications for Alzheimer's disease. Eur J Neurosci 25 (2007) 69-80
28. He B.P., Wen W., and Strong M.J. Activated microglia (BV-2) facilitation of TNF-alpha-mediated motor neuron death in vitro. J Neuroimmunol 128 (2002) 31-38
29. Henkel J.S., Beers D.R., Siklos L., and Appel S.H. The chemokine MCP-1 and the dendritic and myeloid cells it attracts are increased in the mSOD1 mouse model of ALS. Mol Cell Neurosci 31 (2006) 427-437
30. Henkel J.S., Engelhardt J.I., Siklos L., Simpson E.P., Kim S.H., Pan T., Goodman J.C., Siddique T., Beers D.R., and Appel S.H. Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann Neurol 55 (2004) 221-235
31. Hensley K., Fedynyshyn J., Ferrell S., Floyd R.A., Gordon B., Grammas P., Hamdheydari L., Mhatre M., Mou S., Pye Q.N., Stewart C., West M., West S., and Williamson K.S. Message and protein-level elevation of tumor necrosis factor alpha (TNF alpha) and TNF alpha-modulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol Dis 14 (2003) 74-80
32. Holmoy T. T cells in amyotrophic lateral sclerosis. Eur J Neurol 15 (2008) 360-366
33. Ilieva E.V., Ayala V., Jove M., Dalfo E., Cacabelos D., Povedano M., Bellmunt M.J., Ferrer I., Pamplona R., and Portero-Otin M. Oxidative and endoplasmic reticulum stress interplay in sporadic amyotrophic lateral sclerosis. Brain 130 (2007) 3111-3123
34. Kawamata T., Akiyama H., Yamada T., and McGeer P.L. Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Am J Pathol 140 (1992) 691-707
35. Koopman G., Reutelingsperger C.P., Kuijten G.A., Keehnen R.M., Pals S.T., and van Oers M.H. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84 (1994) 1415-1420
36. Kuno R., Wang J., Kawanokuchi J., Takeuchi H., Mizuno T., and Suzumura A. Autocrine activation of microglia by tumor necrosis factor-alpha. J Neuroimmunol 162 (2005) 89-96
37. Lambeth J.D. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4 (2004) 181-189
38. Levine R.L., Williams J.A., Stadtman E.R., and Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233 (1994) 346-357
39. Li B., Guo Y.S., Sun M.M., Dong H., Wu S.Y., Wu D.X., and Li C.Y. The NADPH oxidase is involved in lipopolysaccharide-mediated motor neuron injury. Brain Res 1226 (2008) 199-208
40. Liu D., Bao F., Wen J., and Liu J. Mutation of superoxide dismutase elevates reactive species: comparison of nitration and oxidation of proteins in different brain regions of transgenic mice with amyotrophic lateral sclerosis. Neuroscience 146 (2007) 255-264
41. Mander P., and Brown G.C. Activation of microglial NADPH oxidase is synergistic with glial iNOS expression in inducing neuronal death: a dual-key mechanism of inflammatory neurodegeneration. J Neuroinflammation 2 (2005) 20
42. Marden J.J., Harraz M.M., Williams A.J., Nelson K., Luo M., Paulson H., and Engelhardt J.F. Redox modifier genes in amyotrophic lateral sclerosis in mice. J Clin Invest 117 (2007) 2913-2919
43. Martin L.J. Neuronal death in amyotrophic lateral sclerosis is apoptosis: possible contribution of a programmed cell death mechanism. J Neuropathol Exp Neurol 58 (1999) 459-471
44. McGeer P.L., and McGeer E.G. Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 26 (2002) 459-470
45. Mhatre M., Floyd R.A., and Hensley K. Oxidative stress and neuroinflammation in Alzheimer's disease and amyotrophic lateral sclerosis: common links and potential therapeutic targets. J Alzheimers Dis 6 (2004) 147-157
46. Mir M., Tolosa L., Asensio V.J., Llado J., and Olmos G. Complementary roles of tumor necrosis factor alpha and interferon gamma in inducible microglial nitric oxide generation. J Neuroimmunol 204 (2008) 101-109
47. 2 release is mediated by the activation of cyclooxygenase-2 (COX-2) transcription via NFkappaB in human gingival fibroblasts. Mol Cell Biochem 238 (2002) 11-18
48. Pasinelli P., Houseweart M.K., Brown Jr. R.H., and Cleveland D.W. Caspase-1 and -3 are sequentially activated in motor neuron death in Cu,Zn superoxide dismutase-mediated familial amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A 97 (2000) 13901-13906
49. Peluffo H., Shacka J.J., Ricart K., Bisig C.G., Martinez-Palma L., Pritsch O., Kamaid A., Eiserich J.P., Crow J.P., Barbeito L., and Estevez A.G. Induction of motor neuron apoptosis by free 3-nitro-L-tyrosine. J Neurochem 89 (2004) 602-612
50. Poloni M., Facchetti D., Mai R., Micheli A., Agnoletti L., Francolini G., Mora G., Camana C., Mazzini L., and Bachetti T. Circulating levels of tumour necrosis factor-alpha and its soluble receptors are increased in the blood of patients with amyotrophic lateral sclerosis. Neurosci Lett 287 (2000) 211-214
51. Rothstein J.D., Jin L., Dykes-Hoberg M., and Kuncl R.W. Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc Natl Acad Sci U S A 90 (1993) 6591-6595
52. Sargsyan S.A., Monk P.N., and Shaw P.J. Microglia as potential contributors to motor neuron injury in amyotrophic lateral sclerosis. Glia 51 (2005) 241-253
53. Sasaki S., Shibata N., Komori T., and Iwata M. iNOS and nitrotyrosine immunoreactivity in amyotrophic lateral sclerosis. Neurosci Lett 291 (2000) 44-48
54. Sathasivam S., and Shaw P.J. Apoptosis in amyotrophic lateral sclerosis-what is the evidence?. Lancet Neurol 4 (2005) 500-509
55. Sedel F., Bechade C., Vyas S., and Triller A. Macrophage-derived tumor necrosis factor alpha, an early developmental signal for motoneuron death. J Neurosci 24 (2004) 2236-2246
56. Shaw P.J. Molecular and cellular pathways of neurodegeneration in motor neurone disease. J Neurol Neurosurg Psychiatry 76 (2005) 1046-1057
57. Soler R.M., Egea J., Mintenig G.M., Sanz-Rodriguez C., Iglesias M., and Comella J.X. Calmodulin is involved in membrane depolarization-mediated survival of motoneurons by phosphatidylinositol-3 kinase- and MAPK-independent pathways. J Neurosci 18 (1998) 1230-1239
58. Stommel E.W., van Hoff R.M., Graber D.J., Bercury K.K., Langford G.M., and Harris B.T. Tumor necrosis factor-alpha induces changes in mitochondrial cellular distribution in motor neurons. Neuroscience 146 (2007) 1013-1019
59. Tolosa L., Mir M., Asensio V.J., Olmos G., and Llado J. Vascular endothelial growth factor protects spinal cord motoneurons against glutamate-induced excitotoxicity via phosphatidylinositol 3-kinase. J Neurochem 105 (2008) 1080-1090
60. Troost D., van den Oord J.J., de Jong J.M., and Swaab D.F. Lymphocytic infiltration in the spinal cord of patients with amyotrophic lateral sclerosis. Clin Neuropathol 8 (1989) 289-294
61. Tsuchida T., Ensini M., Morton S.B., Baldassare M., Edlund T., Jessell T.M., and Pfaff S.L. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79 (1994) 957-970
62. 11C] (R)-PK11195 positron emission tomography study. Neurobiol Dis 15 (2004) 601-609
63. Vermeren M., Maro G.S., Bron R., McGonnell I.M., Charnay P., Topilko P., and Cohen J. Integrity of developing spinal motor columns is regulated by neural crest derivatives at motor exit points. Neuron 37 (2003) 403-415
64. Wen W., Sanelli T., Ge W., Strong W., and Strong M.J. Activated microglial supernatant induced motor neuron cytotoxicity is associated with upregulation of the TNFR1 receptor. Neurosci Res 55 (2006) 87-95
65. Wengenack T.M., Holasek S.S., Montano C.M., Gregor D., Curran G.L., and Poduslo J.F. Activation of programmed cell death markers in ventral horn motor neurons during early presymptomatic stages of amyotrophic lateral sclerosis in a transgenic mouse model. Brain Res 1027 (2004) 73-86
66. Wetts R., and Vaughn J.E. Development of cholinergic terminals around rat spinal motor neurons and their potential relationship to developmental cell death. J Comp Neurol 435 (2001) 171-183
67. Weydt P., and Moller T. Neuroinflammation in the pathogenesis of amyotrophic lateral sclerosis. Neuroreport 16 (2005) 527-531
68. Wilkinson B.L., and Landreth G.E. The microglial NADPH oxidase complex as a source of oxidative stress in Alzheimer's disease. J Neuroinflammation 3 (2006) 30
69. Yamada T., Pfaff S.L., Edlund T., and Jessell T.M. Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from notochord and floor plate. Cell 73 (1993) 673-686
70. Zhang R., Gascon R., Miller R.G., Gelinas D.F., Mass J., Hadlock K., Jin X., Reis J., Narvaez A., and McGrath M.S. Evidence for systemic immune system alterations in sporadic amyotrophic lateral sclerosis (sALS). J Neuroimmunol 159 (2005) 215-224
71. Zhao W., Xie W., Le W., Beers D.R., He Y., Henkel J.S., Simpson E.P., Yen A.A., Xiao Q., and Appel S.H. Activated microglia initiate motor neuron injury by a nitric oxide and glutamate-mediated mechanism. J Neuropathol Exp Neurol 63 (2004) 964-977