Neuroprotective effect of nitric oxide donor isosorbide-dinitrate against oxidative stress induced by ethidium bromide in rat brain

EXCLI Journal

Volumn 11, Issue , 2012, Pages 125-141

  Abdel Salam, Omar M E ^a   Khadrawy, Yasser Ashry ^a   Mohammed, Nadia A ^a  

^a NATIONAL RESEARCH CENTRE   (Egypt)

Author keywords

Ethidium bromide; Isosorbide dinitrate; Rat brain; Toxic demyelination

Indexed keywords

ACETYLCHOLINESTERASE; ARYLDIALKYLPHOSPHATASE; DOPAMINE; ETHIDIUM BROMIDE; GLUTATHIONE; ISOSORBIDE DINITRATE; MALONALDEHYDE; NITRIC OXIDE; NORADRENALIN; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DEMYELINATING DISEASE; DOPAMINE BRAIN LEVEL; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; LIPID PEROXIDATION; MALE; NEUROPROTECTION; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; NORADRENALIN BRAIN LEVEL; OXIDATIVE STRESS; RAT; SEROTONIN BRAIN LEVEL; SYSTEMIC THERAPY;

EID: 84867596642     PISSN: None     EISSN: 16112156     Source Type: Journal    
DOI: None     Document Type: Article

References (97)

1. Abdel-Salam OME, Khadrawy YA, Salem NA, Sleem AA. Oxidative stress in a model of toxic demyelination in rat brain: the effect of piracetam and vinpocetine. Neurochem Res 2011;36:1062-72.
2. Amengual-Cladera E, Nadal-Casellas A, Gómez-Pérez Y, Gomila I, Prieto RM, Proenza AM, Lladó I. Phytotherapy in a rat model of hyperoxaluria: the antioxidant effects of quercetin involve serum paraoxonase 1 activation. Exp Biol Med 2011;236:1133-8.
3. Arnelle DR, Stamler JS. NO1, NO, NO2 do-nation by S-nitrosothiols: implications for regulation of physiological functions by S-nitrosylation and acceleration of disulfide formation. Arch Biochem Biophys 1995;318: 279-85.
4. Bagasra O, Michaels FH, Zheng YM, Bobro-ski LE, Spitsin SV, Fu ZF et al. Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proc Natl Acad Sci USA 1995;92:12041-5.
5. Barkhatova VP, Zavalishin IA, Askarova LSh, Shavratskii VKh, Demina EG. Changes in neurotransmitters in multiple sclerosis. Neurosci Behav Physiol 1998;28:341-4.
6. Bhat R, Axtell R, Mitra A, Miranda M, Lock C, Tsien RW et al. Inhibitory role for GABA in autoimmune inflammation. Proc Natl Acad Sci USA 2010;107:2580-5.
7. Bredt DS. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic Res 1999;31:577-96.
8. Brüne B, von Knethen A, Sandau KB. Nitric oxide and its role in apoptosis. Eur J Pharma-col 1998;351:261-72.
9. Choi IY, Lee SP, Denney DR, Lynch SG. Lower levels of glutathione in the brains of secondary progressive multiple sclerosis pa-tients measured by 1H magnetic resonance chemical shift imaging at 3 T. Mult Scler 2011;17:289-96.
10. Darvesh S, Leblanc AM, Macdonald IR, Reid GA, Bhan V, Macaulay RJ et al. Butyrylcho-linesterase activity in multiple sclerosis neu-ropathology. Chem Biol Interact 2010;187: 425-31.
11. de Groot CJ, Ruuls SR, Theeuwes JW, Dijks-tra CD, van der Valk P. Immunocytochemical characterization of the expression of induci-ble and constitutive isoforms of nitric oxide synthase in demyelinating multiple sclerosis lesions. J Neuropathol Exp Neurol 1997;56: 10-20.
12. de Vries HE, Schreibelt G, van Horssen G. Oxidative stress in multiple sclerosis pathol-ogy and therapeutic potential of Nrf2 activa-tion. In: Armstrong D (ed.). Oxidative stress in applied basic research and clinical practice (pp 65-77). New York: Springer, 2011
13. di Matteo V, Pierucci M, Benigno A, Crescimanno G, Esposito E, Di Giovanni G. Involvement of nitric oxide in nigrostriatal dopaminergic system degeneration: a neuro-chemical study. Ann N Y Acad Sci 2009; 1155:309-15.
14. Ellman GL. Tissue sulfhydryl groups. Arch Biochem 1959;82:70-7.
15. Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM. A new and rapid colori-metric determination of acetylcholinesterase activity. Biochem Pharm 1961;7:88-95.
16. Garthwaite G, Goodwin DA, Batchelor AM, Leeming K, Garthwaite J. Nitric oxide toxici-ty in CNS white matter: an in vitro study us-ing rat optic nerve. Neuroscience 2002;109: 145-55.
17. Giovannoni G, Heales SJ, Land JM, Thomp-son EJ. The potential role of nitric oxide in multiple sclerosis. Mult Scler 1998;4:212-6.
18. Glabinski A, Tawsek NS, Bartosz G. In-creased generation of superoxide radicals in the blood of MS patients. Acta Neurol Scand 1993;88:174-7.
19. Gorun V, Proinov I, Baltescu V, Balaban G, Barzu O. Modified Ellman procedure for as-say of cholinesterases in crude enzymatic preparation. Anal Biochem 1978;86:324-6.
20. Graça DL, Bondan EF, Pereira LA, Fernan-des CG, Maiorka PC. Behaviour of oligoden-drocytes and Schwann cells in an experi-mental model of toxic demyelination of the central nervous system. Arq Neuropsiquiatr 2001;59(2-B):358-61.
21. Gulati K, Chakraborti A, Ray A. Modulation of stress-induced neurobehavioral changes and brain oxidative injury by nitric oxide (NO) mimetics in rats. Behav Brain Res 2007;183:226-30.
22. Gutteridge JMC. Lipid peroxidation and anti-oxidants as biomarkers of tissue damage. Clin Chem 1995;41:1819-28.
23. Haider L, Fischer MT, Frischer JM, Bauer J, Höftberger R, Botond G et al. Oxidative damage in multiple sclerosis lesions. Brain 2011;134:1914-24.
24. Higashino K, Takahashi Y, Yamamura Y. Release of phenyl acetate esterase from liver microsomes by carbon tetrachloride. Clin Chim Acta 1972;41:313-20.
25. Honmou O, Felts PA, Waxman SG, Kocsis JD. Restoration of normal conduction proper-ties in demyelinated spinal cord axons in the adult rat by transplantation of exogenous Schwann cells. J Neurosci 1996;16:3199-208.
26. Hu W, Lucchinetti CF. The pathological spectrum of CNS inflammatory demyelinat-ing diseases. Semin Immunopathol 2009;31: 439-53.
27. Hummel SG, Fischer AJ, Martin SM, Schafer FQ, Buetner GR. Nitric oxide as a cellular antioxidant: a little goes a long way. Free Rad Biol Med 2006;40:501-6.
28. Iadecola C. Bright and dark sides of nitric oxide in ischemic brain injury. Trends Neuro-sci 1997;20:132-9.
29. Ibragic S, Sofic E, Suljic E, Avdagic N, Ba-jraktarevic A, Tahirovic I. Serum nitric oxide concentrations in patients with multiple scle-rosis and patients with epilepsy. J Neural Transm 2012;119:7-11.
30. Jamroz-Wisniewska A, Beltowski J, Stel-masiak Z, Bartosik-Psujek H. Paraoxonase 1 activity in different types of multiple sclero-sis. Mult Scler 2009;15:399-402.
31. Jeffery ND, Blakemore WF. Locomotor defi-cits induced by experimental spinal cord de-myelination are abolished by spontaneous remyelination. Brain 1997;120:27-37.
32. Jiang HB, Yoneyama H, Furukawa A, Hamamoto T, Takahara J, Ichikawa Y. Effect of isosorbide dinitrate on nitric oxide syn-thase under hypoxia. Pharmacology 2001;62: 10-6.
33. Kapoor R, Blaker PA, Hall SM, Davies M, Smith KJ. Protection of axons from degen-eration resulting from exposure to nitric ox-ide. Rev Neurol (Paris) 2000;156(Suppl. 3): S67.
34. Karg E, Klivényi P, Németh I, Bencsik K, Pintér S, Vécsei L. Nonenzymatic antioxi-dants of blood in multiple sclerosis. J Neurol 1999;246:533-9.
35. Kim YM, Talanian RV, Billiar TR. Nitric oxide inhibits apoptosis by preventing in-creases in caspase-3-like activity via two dis-tinct mechanisms. J Biol Chem 1997;272: 31138-48.
36. Kirchner SM, Bonan CD, Battastini AM, Sarkis JJ. Effect of nitric oxide donors on ex-tracellular ATP, ADP, and AMP catabolism in rat hippocampal synaptosomes. Brain Res Bull 2001;55:469-73.
37. Kiriyama Y, Hiruma H, Kobayashi H, To-mita T, Kawakami T. Inhibitory effects of nitric oxide (NO) on fast axonal transport in cultured rat hippocampal neurons. Kitasato Med 2002;32:203-9.
38. Koch M, Mostert J, Arutjunyan A, Stepanov M, Teelken A, Heersema D et al. Peripheral blood leukocyte NO production and oxidative stress in multiple sclerosis. Mult Scler 2008; 14:159-65.
39. Kotur-Stevuljevic J, Spasic S, Jelic-Ivanovic Z, Spasojevic-Kalimanovska V, Stefanovic A, Vujovic A et al. PON1 status is influenced by oxidative stress and inflammation in coro-nary heart disease patients. Clin Biochem 2008;41:1067-73.
40. Kurauchi Y, Hisatsune A, Isohama Y, Katsu-ki H. Nitric oxide-cyclic GMP signaling pathway limits inflammatory degeneration of midbrain dopaminergic neurons: cell type-specific regulation of heme oxygenase-1 ex-pression. Neuroscience 2009;158:856-66.
41. Kwak HJ, Pae HO, Oh GS, Choi BM, Jang SI, Jung S et al. Molsidomine ameliorates experimental allergic encephalomyelitis in Lewis rats. Immunopharmacol Immunotoxi-col 2003;25:41-52.
42. La Du BN. Human serum paraoxonase/aryl-esterase. In: Kalow W (ed.). Pharmacogenet-ics of drug metabolism (pp 51-91). New York: Pergamon Elmford, 1992.
43. Laroux FS, Pavlick KP, Hines IN, Kawachi S, Harada H, Bharwani S et al. Role of nitric oxide in inflammation. Acta Physiol Scand 2001;173:113-8.
44. Lassmann H. Classification of demyelinating diseases at the interface between etiology and pathogenesis. Curr Opin Neurol 2001;14: 253-8.
45. Lassmann H, Brück W, Lucchinetti CF. The immunopathology of multiple sclerosis: an overview. Brain Pathol 2007;17:210-8.
46. Lee M, Schwab C, McGeer PL. Astrocytes are GABAergic cells that modulate microgli-al activity. Glia 2011;59:152-65.
47. Li S, Vana AC, Ribeiro R, Zhang Y. Distinct role of nitric oxide and peroxynitrite in medi-ating oligodendrocyte toxicity in culture and in experimental autoimmune encephalomyeli-tis. Neuroscience 2011;184:107-19.
48. Liu JS, Zhao ML, Brosnan CF, Lee SC. Ex-pression of inducible nitric oxide synthase and nitrotyrosine in multiple sclerosis lesions. Am J Pathol 2001;158:2057-66.
49. Ljubisavljevic S, Stojanovic I, Pavlovic D, Sokolovic D, Stevanovic I. Aminoguanidine and N-acetyl-cysteine supress oxidative and nitrosative stress in EAE rat brains. Redox Rep 2011;16:166-72.
50. Love S. Demyelinating diseases. J Clin Pathol 2006;59:1151-9.
51. Mackness B, Quarck R, Verreth W, Mack-ness M, Holvoet P. Human paraoxonase-1 overexpression inhibits atherosclerosis in a mouse model of metabolic syndrome. Arteri-oscler Thromb Vasc Biol 2006;26:1545-50.
52. Maletić SD, Dragicević LM, Zikić RV, Stajn AS, Kostić MM. Effects of nitric oxide do-nor, isosorbide dinitrate, on energy metabo-lism of rat reticulocytes. Physiol Res 1999;48:417-27.
53. Maletic SD, Dragicevic-Djokovic LM, Zikic RV, Stajn AS, Milenkovic P, Kostic MM. Effects of nitric oxide donors on energy me-tabolism of rat erythrocytes. J Environ Pathol Toxicol Oncol 2000;19:383-90.
54. Marsillach J, Camps J, Ferré N, Beltran R, Rull A, Mackness B et al. Paraoxonase-1 is related to inflammation, fibrosis and PPAR delta in experimental liver disease. BMC Gastroenterol 2009;9:3.
55. Masood A, Banerjee BD, Vijayan VK, Ray A. Modulation of stress induced neurobehav-ioral changes by nitric oxide in rats. Eur J Pharmacol 2003;458:138-9.
56. Mazzanti CM, Spanevello RM, Pereira LB, Gonçalves JF, Kaizer R, Corrêa M et al. Ace-tylcholinesterase activity in rats experimen-tally demyelinated with ethidium bromide and treated with interferon beta. Neurochem Res 2006;31:1027-34.
57. Medina JH, Izquierdo I. Retrograde messen-gers, long-term potentiation and memory. Brain Res Rev 1995;21:185-94.
58. Mirshafiey A, Mohsenzadegan M. Antioxi-dant therapy in multiple sclerosis. Immuno-pharmacol Immunotoxicol 2009;31:13-29.
59. Mitosek-Szewczyk K, Gordon-Krajcer W, Walendzik P, Stelmasiak Z. Free radical pe-roxidation products in cerebrospinal fluid and serum of patients with multiple sclerosis after glucocorticoid therapy. Fol Neuropathol 2010;48:116-22.
60. Moncada S, Bolaños JP. Nitric oxide, cell bioenergetics and neurodegeneration. J Neu-rochem 2006;97:1676-89.
61. Moshage H, Kok B, Huizenga JR. Nitrite and nitrate determination in plasma: a critical evaluation. Clin Chem 1995;41:892-6.
62. Murphy S. Production of nitric oxide by glial cells: regulation and potential roles in the CNS. Glia 2000;29:1-13.
63. Musgrave TM, Tenorio G, Rauw G, Baker GB, Kerr BJ. Tissue concentration changes of amino acids and biogenic amines in the cen-tral nervous system of mice with experi-mental autoimmune encephalomyelitis (EAE). Neurochem Int 2011;59:28-38.
64. Nunes C, Almeida L, Laranjinha J. 3,4-Dihydroxyphenylacetic acid (DOPAC) mod-ulates the toxicity induced by nitric oxide in PC-12 cells via mitochondrial dysfunctioning and ATP depletion. Neurotoxicology 2008;29:998-1007.
65. Olearczyk JJ, Ellsworth ML, Stephenson AH, Lonigro AJ, Sprague RS. Nitric oxide inhibits ATP release from erythrocytes. J Pharmacol Exp Ther 2004;309:1079-84.
66. Oleszak EL, Zaczynska E, Bhattacharjee M, Butunoi C, Legido A, Katsetos CD. Inducible nitric oxide synthase and nitrotyrosine are found in monocytes/macrophages and/or as-trocytes in acute, but not in chronic, multiple sclerosis. Clin Diagn Lab Immunol 1998;5: 438-45.
67. Paget GE, Barnes JM. Toxicity tests. In: Lau-rence DR, Bacharach AL (eds.). Evaluation of drug activities. Pharmacometrics (p 161). London: Academic Press.
68. Permpongpaiboon T, Nagila A, Pidetcha P, Tuangmungsakulchai K, Tantrarongroj S, Porntadavity S. Decreased paraoxonase 1 ac-tivity and increased oxidative stress in low lead-exposed workers. Hum Exp Toxicol 2011;30:1196-1203.
69. Primo-Parmo SL, Sorenson RC, Teiber J, La Du BN. The human serum paraoxonase/aryl-esterase gene (PON1) is one member of a multigene family. Genomics 1996;33:498-507.
70. Rajkovic MG, Rumora L, Barisic K. The paraoxonase 1, 2 and 3 in humans. Biochem Med (Zagreb) 2011;21:122-30.
71. Ramos-Zúñiga R, Velázquez-Santana H, Mercado-Pimentel R, Cerda-Camacho F. Neuroprotection in selective focal ischemia in rats by nitrates, an alternative redox manipu-lation of nitric oxide: experimental model. Minim Invasive Neurosurg 1998;41:152-60.
72. Rauhala P, Lin AM, Chiueh CC. Neuropro-tection by S-nitrosoglutathione of brain do-pamine neurons from oxidative stress. FASEB J 1998;12:165-73.
73. Redford EJ, Kapoor R, Smith KJ. Nitric ox-ide donors reversibly block axonal conduc-tion: demyelinated axons are especially sus-ceptible. Brain 1997;120:2149-57.
74. Rodrigo L, Hernández AF, López-Caballero JJ, Gil F, Pla A. Immunohistochemical evi-dence for the expression and induction of paraoxonase in rat liver, kidney, lung and brain tissue: implications for its physiological role. Chem Biol Interact 2001;137:123-37.
75. Ruberg M, Villageois A, Bonnet AM, Pillon B, Rieger F, Agid Y. Acetylcholinesterase and butyrylcholinesterase activity in the cere-brospinal fluid of patients with neurodegen-erative diseases involving cholinergic sys-tems. J Neurol Neurosurg Psych 1987;50: 538-43.
76. Ruiz-Larrea MB, Leal AM, Liza M, Lacort M, de Groot H. Antioxidant effects of estra-diol and 2-hydroxyestradiol on iron-induced lipid peroxidation of rat liver microsomes. Steroids 1994;59:383-8.
77. Salom JB, Ortí M, Centeno JM, Torregrosa G, Alborch E. Reduction of infarct size by the NO donors sodium nitroprusside and spermine/NO after transient focal cerebral ischemia in rats. Brain Res 2000;865:149-56.
78. Serrano J, Fernández AP, Martínez-Murillo R, Alonso D, Rodrigo J, Salas E et al. The nitric oxide donor LA 419 decreases ischemic brain damage. Int J Mol Med 2007;19:229-36.
79. Shuman EM, Madison DV. Nitric oxide and synaptic function Annu Rev Neurosci 1994; 17:153-83.
80. Simonini MV, Polak PE, Sharp A, McGuire S, Galea E, Feinstein DL. Increasing CNS noradrenaline reduces EAE severity. J Neuro-immune Pharmacol 2010;5:252-9.
81. Smith KJ. Newly lesioned tissue in multiple sclerosis-a role for oxidative damage? Brain 2011;134:1877-81.
82. Srinivasan R, Ratiney H, Hammond-Rosen-bluth KE, Pelletier D, Nelson SJ. MR spec-troscopic imaging of glutathione in the white and gray matter at 7 T with an application to multiple sclerosis. Magn Reson Imaging 2010;28:163-70.
83. Szabo C. Physiological and pathophysiologi-cal roles of nitric oxide in the central nervous system. Brain Res Bull 1996;41:131-41.
84. Taler M, Gil-Ad I, Korob I, Weizman A. The immunomodulatory effect of the antidepres-sant sertraline in an experimental autoim-mune encephalomyelitis mouse model of multiple sclerosis. Neuroimmunomodulation 2010;18:117-22.
85. Tsoi VL, Hill KE, Carlson NG, Warner JE, Rose JW. Immunohistochemical evidence of inducible nitric oxide synthase and nitrotyro-sine in a case of clinically isolated optic neu-ritis. J Neuroophthalmol 2006;26:87-94.
86. van der Veen RC, Roberts LJ. Contrasting roles for nitric oxide and peroxynitrite in the peroxidation of myelin lipids. J Neuroimmu-nol 1999;95:1-7.
87. Vana AC, Li S, Ribeiro R, Tchantchou F, Zhang Y. Arachidonyl trifluoromethyl ketone ameliorates experimental autoimmune en-cephalomyelitis via blocking peroxynitrite formation in mouse spinal cord white matter. Exp Neurol 2011;231:45-55.
88. Verrecchia C, Boulu RG, Plotkine M. Neuro-protective and deleterious effects of nitric oxide on focal cerebral ischemia-induced neurone death. Adv Neuroimmunol 1995;5: 359-78.
89. Vollmar P, Nessler S, Kalluri SR, Hartung HP, Hemmer B. The antidepressant venlafax-ine ameliorates murine experimental auto-immune encephalomyelitis by suppression of pro-inflammatory cytokines. Int J Neuropsy-chopharmacol 2009;12:525-36.
90. Wang W, Ballatori N. Endogenous glutathi-one conjugates: occurrence and biological functions. Pharmacol Rev 1998;50:335-56.
91. Wang Y, Feng D, Liu G, Luo Q, Xu Y, Lin S et al. Gamma-aminobutyric acid transporter 1 negatively regulates T cell-mediated immune responses and ameliorates autoimmune in-flammation in the CNS. J Immunol 2008; 181:8226-36.
92. Watson AD, Berliner JA, Hama SY, La Du BN, Faull KF, Fogelman AM et al. Protective effect of high density lipoprotein associated paraoxonase: inhibition of the biological ac-tivity of minimally oxidized low density lip-oprotein. J Clin Invest 1995;96:2882-91.
93. Willmot MR, Bath PMW. The potential of nitric oxide therapeutics in stroke. Expert Opin Investig Drugs 2003;12:455-70.
94. Xu LY, Yang JS, Link H, Xiao BG. SIN-1, a nitric oxide donor, ameliorates experimental allergic encephalomyelitis in Lewis rats in the incipient phase: the importance of the time window. J Immunol 2001;166:5810-6.
95. Yajima K, Suzuki K. Demyelination and re-myelination in the rat central nervous system following ethidium bromide injection. Lab Invest 1979;41:385-92.
96. Yao SY, Ljunggren-Rose A, Chandramohan N, Whetsell WO Jr, Sriram S. In vitro and in vivo induction and activation of nNOS by LPS in oligodendrocytes. J Neuroimmunol 2010;229:146-56.
97. Yun H-Y, Dawson VL, Dawson TM. Nitric oxide in health and disease of the nervous system. Mol Psychiatry 1997;2:300-10.