Nicotine attenuates oxidative stress, activation of redox-regulated transcription factors and induction of proinflammatory genes in compressive spinal cord trauma

Molecular Brain Research

Volumn 124, Issue 2, 2004, Pages 188-198

  Ravikumar, R ^a   Flora, Govinder ^a   Geddes, James W ^b   Hennig, Bernhard ^b   Toborek, Michal ^a,c  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

Chemokines; CREB; Cytokines; NF B, AP 1; Nicotine; Oxidative stress; Signal transduction: gene expression; Trauma, spinal cord and brainstem

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MECAMYLAMINE; MESSENGER RNA; NICOTINE; NICOTINIC RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL MODEL; ARTICLE; ATTENUATION; BINDING AFFINITY; CONTROLLED STUDY; DNA BINDING; DRUG EFFECT; LUMBAR SPINAL CORD; LUMBAR SPINE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD INJURY; THORAX;

ANIMALS; BINDING, COMPETITIVE; CHEMOKINE CCL2; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; NF-KAPPA B; NICOTINE; NICOTINIC ANTAGONISTS; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; RATS, LONG-EVANS; RECEPTORS, NICOTINIC; RNA, MESSENGER; SPINAL CORD COMPRESSION; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS; TREATMENT OUTCOME; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 2342516047     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbrainres.2004.02.018     Document Type: Article

References (61)

1. Aksenova M., Butterfield D.A., Zhang X.S., Underwood M., Geddes J.W. Increased protein oxidation and decreased creatine kinase BB expression and activity after spinal cord contusion injury. J. Neurotrauma. 19:2002;491-502
2. Azbill R.D., Mu X., Bruce-Keller A.J., Mattson M.P., Springer J.E. Impaired mitochondrial function, oxidative stress and altered antioxidant enzyme activities following traumatic spinal cord injury. Brain Res. 765:1997;283-290
3. Baldwin S.A., Broderick R., Osbourne D., Waeg G., Blades D.A., Scheff S.W. The presence of 4-hydroxynonenal/protein complex as an indicator of oxidative stress after experimental spinal cord contusion in a rat model. J. Neurosurg. 88:1998;874-883
4. Basso D.M., Beattie M.S., Bresnahan J.C., Anderson D.K., Faden A.I., Gruner J.A., Holford T.R., Hsu C.Y., Noble L.J., Nockels R., Perot P.L., Salzman S.K., Young W. MASCIS evaluation of open field locomotor scores: effects of experience and teamwork on reliability. Multicenter animal spinal cord injury study. J. Neurotrauma. 13:1996;343-359
5. Basso D.M., Beattie M.S., Bresnahan J.C. Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp. Neurol. 139:1996;244-256
6. Beattie M.S., Hermann G.E., Rogers R.C., Bresnahan J.C. Cell death in models of spinal cord injury. Prog. Brain Res. 137:2002;37-47
7. Bethea J.R., Castro M., Keane R.W., Lee T.T., Dietrich W.D., Yezierski R.P. Traumatic spinal cord injury induces nuclear factor-kappaB activation. J. Neurosci. 18:1998;3251-3260
8. Bethea J.R., Nagashima H., Acosta M.C., Briceno C., Gomez F., Marcillo A.E., Loor K., Green J., Dietrich W.D. Systemically administered interleukin-10 reduces tumor necrosis factor-alpha production and significantly improves functional recovery following traumatic spinal cord injury in rats. J. Neurotrauma. 16:1999;851-863
9. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254
10. Brandoli C., Shi B., Pflug B., Andrews P., Wrathall J.R., Mocchetti I. Dexamethasone reduces the expression of p75 neurotrophin receptor and apoptosis in contused spinal cord. Mol. Brain Res. 87:2001;61-70
11. Brinkman B.M., Telliez J.B., Schievella A.R., Lin L.L., Goldfeld A.E. Engagement of tumor necrosis factor (TNF) receptor 1 leads to ATF-2-and p38 mitogen-activated protein kinase-dependent TNF-alpha gene expression. J. Biol. Chem. 274:1999;30882-30886
12. Chan C.F., Sun W.Z., Lin J.K., Lin-Shiau S.Y. Activation of transcription factors of nuclear factor kappa B, activator protein-1 and octamer factors in hyperalgesia. Eur. J. Pharmacol. 402:2000;61-68
13. Che X., Ye W., Panga L., Wu D.C., Yang G.Y. Monocyte chemoattractant protein-1 expressed in neurons and astrocytes during focal ischemia in mice. Brain Res. 902:2001;171-177
14. Cogswell J.P., Godlevski M.M., Wisely G.B., Clay W.C., Leesnitzer L.M., Ways J.P., Gray J.G. NF-kappa B regulates IL-1 beta transcription through a consensus NF-kappa B binding site and a nonconsensus CRE-like site. J. Immunol. 153:1994;712-723
15. Costa G., Abin-Carriquiry J.A., Dajas F. Nicotine prevents striatal dopamine loss produced by 6-hydroxydopamine lesion in the substantia nigra. Brain Res. 888:2001;336-342
16. Dajas-Bailador F.A., Lima P.A., Wonnacott S. The alpha7 nicotinic acetylcholine receptor subtype mediates nicotine protection against NMDA excitotoxicity in primary hippocampal cultures through a Ca(2+) dependent mechanism. Neuropharmacology. 39:2000;2799-2807
17. Demediuk P., Daly M.P., Faden A.I. Changes in free fatty acids, phopholipids, and cholesterol following impact to the rat spinal cord. J. Neurosci. Res. 23:1989;95-106
18. Dumont R.J., Okonkwo D.O., Verma S., Hurlbert R.J., Boulos P.T., Ellegala D.B., Dumont A.S. Acute spinal cord injury: Part I. Pathophysiologic mechanisms. Clin. Neuropharmacol. 24:2001;254-264
19. Dumont A.S., Dumont R.J., Oskouian R.J. Will improved understanding of the pathophysiological mechanisms involved in acute spinal cord injury improve the potential for therapeutic intervention? Curr. Opin. Neurol. 15:2002;713-720
20. Farooque M., Hillered L., Holtz A., Olsson Y. Changes of extracellular levels of amino acids after graded compression trauma to the spinal cord: an experimental study in the rat using microdialysis. J. Neurotrauma. 13:1996;537-548
21. Ferchmin P.A., Perez D., Eterovic V.A., De Vellis J. Nicotinic receptors differentially regulate NMDA damage in acute hippocampal slices. J. Pharmacol. Exp. Ther. 305:2003;1071-1078
22. Fratiglioni L., Wang H.-X. Smoking and Parkinson's and Alzheimer's disease: review of the epidemiological studies. Behav. Brain Res. 113:2000;117-120
23. Garrido R., Malecki A., Hennig B., Toborek M. Nicotine attenuates arachidonic acid-induced neurotoxicity in cultured spinal cord neurons. Brain Res. 861:2000;59-68
24. Garrido R., Mattson M.P., Hennig B., Toborek M. Nicotine protects against arachidonic-acid-induced caspase activation, cytochrome c release and apoptosis of cultured spinal cord neurons. J. Neurochem. 76:2001;1395-1403
25. Ghirnikar R.S., Lee Y.L., Eng L.F. Chemokine antagonist infusion promotes axonal sparing after spinal cord contusion injury in rat. J. Neurosci. Res. 64:2001;582-589
26. Gruner J.A. A monitored contusion model of spinal cord injury in the rat. J. Neurotrauma. 9:1992;123-128
27. Guan Z.Z., Yu W.F., Nordberg A. Dual effects of nicotine on oxidative stress and neuroprotection in PC12 cells. Neurochem. Int. 43:2003;243-249
28. Jackson M.J., Papa S., Bolanos J., Bruckdorfer R., Carlsen H., Elliott R.M., Flier J., Griffiths H.R., Heales S., Holst B., Lorusso M., Lund E., Oivind Moskaug J., Moser U., Di Paola M., Polidori M.C., Signorile A., Stahl W., Vina-Ribes J., Astley S.B. Antioxidants, reactive oxygen and nitrogen species, gene induction and mitochondrial function. Mol. Aspects Med. 23:2002;209-285
29. Kamencic H., Griebel R.W., Lyon A.W., Paterson P.G., Juurlink B.H. Promoting glutathione synthesis after spinal cord trauma decreases secondary damage and promotes retention of function. FASEB J. 15:2001;243-250
30. Kaneko S., Maeda T., Kume T., Kochiyama H., Akaike A., Shimohama S., Kimura J. Nicotine protects cultured cortical neurons against glutamate-induced cytotoxicity via alpha7-neuronal receptors and neuronal CNS receptors. Brain Res. 765:1997;135-140
31. Kim G.M., Xu J., Xu J., Song S.K., Yan P., Ku G., Xu X.M., Hsu C.Y. Tumor necrosis factor receptor deletion reduces nuclear factor-kappaB activation, cellular inhibitor of apoptosis protein 2 expression, and functional recovery after traumatic spinal cord injury. J. Neurosci. 21:2001;6617-6625
32. Lee Y.W., Son K.W., Flora G., Hennig B., Nath A., Toborek M. Methamphetamine activates DNA binding of specific redox-responsive transcription factors in mouse brain. J. Neurosci. Res. 70:2002;82-89
33. Lee Y.W., Park H.J., Son K.W., Hennig B., Robertson L.W., Toborek M. 2, 2′, 4, 6, 6′-Pentachlorobiphenyl (PCB104) induces apoptosis of human microvascular endothelial cells through the caspase-dependent activation of CREB. Toxicol. Appl. Pharmacol. 189:2003;1-10
34. Liu X.Z., Xu X.M., Hu R., Du C., Zhang S.X., McDonald J.W., Dong H.X., Wu Y.J., Fan G.S., Jacquin M.F., Hsu C.Y., Choi D.W. Neuronal and glial apoptosis after traumatic spinal cord injury. J. Neurosci. 17:1997;5395-5406
35. Nanri M., Kasahara N., Yamamoto J., Miyake H., Watanabe H. GTS-21, a nicotinic agonist, protects against neocortical neuronal cell loss induced by the nucleus basalis magnocellularis lesion in rats. Jpn. J. Pharmacol. 74:1997;285-289
36. Nanri M., Yamamoto J., Miyake H., Watanabe H. Protective effect of GTS-21, a novel nicotinic receptor agonist, on delayed neuronal death induced by ischemia in gerbils. Jpn. J. Pharmacol. 76:1998;23-29
37. Ma M., Wei T., Boring L., Charo I.F., Ransohoff R.M., Jakeman L.B. Monocyte recruitment and myelin removal are delayed following spinal cord injury in mice with CCR2 chemokine receptor deletion. J. Neurosci. Res. 68:2002;691-702
38. Martin L.J., Liu Z. Injury-induced spinal motor neuron apoptosis is preceded by DNA single-strand breaks and is p53- and Bax-dependent. J. Neurobiol. 50:2002;181-197
39. Martin E.J., Panickar K.S., King M.A., Deyrup M., Hunter B.E., Wang G., Meyer E.M. Cytoprotective action of 2, 4, -dimethoxybenzylidene anabaseine in differentiated PC12 cells and septal cholinergic neurons. Drug Dev. Res. 31:1994;135-141
40. Messi M.L., Renganathan M., Grigorenko E., Delbono O. Activation of alpha7 nicotinic acetylcholine receptor promotes survival of spinal cord motoneurons. FEBS Lett. 411:1997;32-38
41. Moriya T., Hassan A.Z., Young W., Chesler M. Dynamics of extracellular calcium activity following contusion of the rat spinal cord. J. Neurotrauma. 11:1994;255-263
42. Negre-Salvayre A., Auge N., Duval C., Robbesyn F., Thiers J.C., Nazzal D., Benoist H., Salvayre R. Detection of intracellular reactive oxygen species in cultured cells using fluorescent probes. Methods Enzymol. 352:2002;62-71
43. Obata T., Aomine M., Inada M., Kinemuchi H. Nicotine suppresses 1-methyl-4-phenylpyridinium ion-induced hydroxyl radical generation in rat striatum. Neurosci. Lett. 330:2002;122-124
44. Obinu M.C., Reibaud M., Miquet J.M., Pasquet M., Rooney T. Brain-selective stimulation of nicotinic receptors by TC-1734 enhances ACh transmission from frontoparietal cortex and memory in rodents. Prog. Neuro-Psychopharmacol. Biol. Psychiatry. 26:2002;913-918
45. Oudega M., Vargas C.G., Weber A.B., Kleitman N., Bunge M.B. Long-term effects of methylprednisolone following transection of adult rat spinal cord. Eur. J. Neurosci. 11:1999;2453-2464
46. Popovich P.G., Jones T.B. Manipulating neuroinflammatory reactions in the injured spinal cord: back to basics. Trends Pharmacol. Sci. 24:2003;13-17
47. Pu H., Tian J., Flora G., Lee Y.W., Nath A., Hennig B., Toborek M. HIV-1 Tat protein upregulates inflammatory mediators and induces monocyte invasion into the brain. Mol. Cell. Neurosci. 24:2003;224-237
48. Quik M., Kulak J.M. Nicotine and nicotinic receptors: relevance to Parkinson's disease. Neurotoxicology. 23:2002;581-594
49. Reusch J.E., Klemm D.J. Inhibition of CREB activity decreases protein kinase B/Akt expression in 3T3-L1 adipocytes and induces apoptosis. J. Biol. Chem. 277:2002;1426-1432
50. Roebuck K.A., Carpenter L.R., Lakshminarayanan V., Page S.M., Moy J.N., Thomas L.L. Stimulus-specific regulation of chemokine expression involves differential activation of the redox-responsive transcription factors AP-1 and NF-kappaB. J. Leukoc. Biol. 65:1999;291-298
51. Ryan R.E., Ross S.A., Drago J., Loiacono R.E. Dose-related neuroprotective effects of chronic nicotine in 6-hydroxydopamine treated rats, and loss of neuroprotection in alpha4 nicotinic receptor subunit knockout mice. Br. J. Pharmacol. 132:2001;1650-1656
52. Shimohama S., Akaike A., Kimura J. Nicotine-induced protection against glutamate cytotoxicity. Nicotinic cholinergic receptor-mediated inhibition of nitric oxide formation. Ann. N.Y. Acad. Sci. 777:1996;356-361
53. Socci D.J., Bjugstad K.B., Jones H.C., Pattisapu J.V., Arendash G.W. Evidence that oxidative stress is associated with the pathophysiology of inherited hydrocephalus in the H-Tx rat model. Exp. Neurol. 155:1999;109-117
54. Song G., Cechvala C., Resnick D.K., Dempsey R.J., Rao V.L. GeneChip analysis after acute spinal cord injury in rat. J. Neurochem. 79:2001;804-815
55. Soto-Otero R., Mendez-Alvarez E., Hermida-Ameijeiras A., Lopez-Real A.M., Labandeira-Garcia J.L. Effects of (-)-nicotine and (-)-cotinine on 6-hydroxydopamine-induced oxidative stress and neurotoxicity: relevance for Parkinson's disease. Biochem. Pharmacol. 64:2002;125-135
56. Springer J.E., Azbill R.D., Mark R.J., Begley J.G., Waeg G., Mattson M.P. 4-Hydroxynonenal, a lipid peroxidation product, rapidly accumulates following traumatic spinal cord injury and inhibits glutamate uptake. J. Neurochem. 68:1997;2469-2476
57. Streit W.J., Semple-Rowland S.L., Hurley S.D., Miller R.C., Popovich P.G., Stokes B.T. Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp. Neurol. 152:1998;74-87
58. Sugawara T., Lewen A., Gasche Y., Yu F., Chan P.H. Overexpression of SOD1 protects vulnerable motor neurons after spinal cord injury by attenuating mitochondrial cytochrome c release. FASEB. 16:2002;1997-1999
59. Toborek M., Garrido R., Malecki A., Kaiser S., Mattson M.P., Hennig B., Young B. Nicotine attenuates arachidonic acid-induced overexpression of nitric oxide synthase in cultured spinal cord neurons. Exp. Neurol. 161:2000;609-620
60. Xu J., Fan G., Chen S., Wu Y., Xu X.M., Hsu C.Y. Methylprednisolone inhibition of TNF-alpha expression and NF-kB activation after spinal cord injury in rats. Mol. Brain Res. 59:1998;135-142
61. Xu J., Kim G.M., Ahmed S.H., Xu J., Yan P., Xu X.M., Hsu C.Y. Glucocorticoid receptor-mediated suppression of activator protein-1 activation and matrix metalloproteinase expression after spinal cord injury. J. Neurosci. 21:2001;92-97