Increased oxidative stress is associated with chronic intermittent hypoxia-mediated brain cortical neuronal cell apoptosis in a mouse model of sleep apnea

Neuroscience

Volumn 126, Issue 2, 2004, Pages 313-323

  Xu, W ^a   Chi, L ^a   Row, B W ^a   Xu, R ^a   Ke, Y ^a   Xu, B ^a   Luo, C ^a   Kheirandish, L ^a   Gozal, D ^a   Liu, R ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

2,4 dinitropenylhydrazine; analysis of variance; ANOVA; chronic intermittent hypoxia; CIH; DCF; dicholorfluorescein; DNPH; HEt; hydroethidine; malondialdehyde; MDA; NeuN; neuronal nuclear antigen; normoxic control mice normoxia; NOX; PBS; phosphate buffered saline

Indexed keywords

BETA GALACTOSIDASE; CASPASE 3; COPPER ZINC SUPEROXIDE DISMUTASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPID; MOLECULAR MARKER; NUCLEIC ACID; PROTEIN C FOS; PROTEIN C JUN; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ASSAY; HYPOXIA; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; LONG TERM EXPOSURE; MALE; MOLECULAR MECHANICS; MOUSE; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SLEEP APNEA SYNDROME; STEADY STATE;

ANIMALS; APOPTOSIS; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; HYPOXIA, BRAIN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; OXIDATIVE STRESS; SLEEP APNEA SYNDROMES; SUPEROXIDE DISMUTASE;

EID: 2942668297     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.03.055     Document Type: Article

References (54)

1. Ahn B., Rhee S.G., Stadtman E.R. Use of fluorescein hydrazide and fluorescein thiosemicarbazide reagents for the fluorometric determination of protein carbonyl groups and for the detection of oxidized protein on polyacrylamide gels. Anal Biochem. 161:1987;245-257
2. Annunziato L., Amoroso S., Pannaccione A., Cataldi M., Pignataro G., D'Alessio A., Sirabella R., Secondo A., Sibaud L., Di Renzo G.F. Apoptosis induced in neuronal cells by oxidative stress Role played by caspases and intracellular calcium ions. Toxicol Lett. 139:2003;125-133
3. Baker T.L., Fuller D.D., Zabka A.G., Mitchell G.S. Respiratory plasticity Differential actions of continuous and episodic hypoxia and hypercapnia. Respir Physiol. 129:2001;25-35
4. Balfors E.M., Franklin K.A. Impairment of cerebral perfusion during obstructive sleep apneas. Am J Respir Crit Care Med. 150:1994;1587-1591
5. Beebe D.W., Gozal D. Obstructive sleep apnea and the prefrontal cortex Towards a comprehensive model linking nocturnal upper airway obstruction to daytime cognitive and behavioral deficits. J Sleep Res. 11:2002;1-16
6. Benjelloun N., Joly L.M., Palmier B., Plotkine M., Charriaut-Marlangue C. Apoptotic mitochondrial pathway in neurones and astrocytes after neonatal hypoxia-ischaemia in the rat brain. Neuropathol Appl Neurobiol. 29:2003;350-360
7. Carpagnano G.E., Kharitonov S.A., Resta O., Foschino-Barbaro M.P., Gramiccioni E., Barnes P.J. Increased 8-isoprostane and interleukin-6 in breath condensate of obstructive sleep apnea patients. Chest. 122:2002;1162-1167
8. Dei R., Takeda A., Niwa H., Li M., Nakagomi Y., Watanabe M., Inagaki T., Washimi Y., Yasuda Y., Horie K., Miyata T., Sobue G. Lipid peroxidation and advanced glycation end products in the brain in normal aging and in Alzheimer's disease. Acta Neuropathol (Berl). 104:2002;113-122
9. Fletcher E.C. Cardiovascular consequences of obstructive sleep apnea Experimental hypoxia and sympathetic activity. Sleep. 23:(Suppl 4):2000;S127-S131
10. Fletcher E.C. Invited review Physiological consequences of intermittent hypoxia: systemic blood pressure. J Appl Physiol. 90:2001;1600-1605
11. Floyd R.A., Hensley K. Oxidative stress in brain aging Implications for therapeutics of neurodegenerative diseases. Neurobiol Aging. 23:2002;795-807
12. Fujimura M., Morita-Fujimura Y., Noshita N., Sugawara T., Kawase M., Chan P.H. The cytosolic antioxidant copper/zinc-superoxide dismutase prevents the early release of mitochondrial cytochrome c in ischemic brain after transient focal cerebral ischemia in mice. J Neurosci. 20:2000;2817-2824
13. Gerlai R., Clayton N.S. Analysing hippocampal function in transgenic mice An ethological perspective. Trends Neurosci. 22:1999;47-51
14. Gonzalez C., Sanz-Alfayate G., Agapito M.T., Gomez-Nino A., Rocher A., Obeso A. Significance of ROS in oxygen sensing in cell systems with sensitivity to physiological hypoxia. Respir Physiol Neurobiol. 132:2002;17-41
15. Gozal D., Daniel J.M., Dohanich G.P. Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat. J Neurosci. 21:2001;2442-2450
16. Gozal E., Row B.W., Schurr A., Gozal D. Developmental differences in cortical and hippocampal vulnerability to intermittent hypoxia in the rat. Neurosci Lett. 305:2001;197-201
17. + channels. Annu Rev Physiol. 59:1997;23-42
18. + channels. Adv Exp Med Biol. 475:2000;441-452
19. Hall E.D., Smith S.L., Oostveen J.A. Inhibition of lipid peroxidation attenuates axotomy-induced apoptotic degeneration of facial motor neurons in neonatal rats. J Neurosci Res. 44:1996;293-299
20. Han B.H., Xu D., Choi J., Han Y., Xanthoudakis S., Roy S., Tam J., Vaillancourt J., Colucci J., Siman R., Giroux A., Robertson G.S., Zamboni R., Nicholson D.W., Holtzman D.M. Selective, reversible caspase-3 inhibitor is neuroprotective and reveals distinct pathways of cell death after neonatal hypoxic-ischemic brain injury. J Biol Chem. 277:2002;30128-30136
21. Hayakawa T., Terashima M., Kayukawa Y., Ohta T., Okada T. Changes in cerebral oxygenation and hemodynamics during obstructive sleep apneas. Chest. 109:1996;916-921
22. Hodges H. Maze procedures The radial-arm and water maze compared. Brain Res Cogn Brain Res. 3:1996;167-181
23. Kietzmann T., Knabe W., Schmidt-Kastner R. Hypoxia and hypoxia-inducible factor modulated gene expression in brain Involvement in neuroprotection and cell death. Eur Arch Psychiatry Clin Neurosci. 251:2001;170-178
24. Langen R.C., Korn S.H., Wouters E.F. ROS in the local and systemic pathogenesis of COPD. Free Radic Biol Med. 35:2003;226-235
25. Lavie L. Obstructive sleep apnoea syndrome An oxidative stress disorder. Sleep Med Rev. 7:2003;35-51
26. Levine R.L., Wehr N., Williams J.A., Stadtman E.R., Shacter E. Determination of carbonyl groups in oxidized proteins. Methods Mol Biol. 99:2000;15-24
27. Levine R.L., Williams J.A., Stadtman E.R., Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 233:1994;346-357
28. Liu R., Li B., Flanagan S.W., Oberley L.W., Gozal D., Qiu M. Increased mitochondrial antioxidative activity or decreased oxygen free radical propagation prevent mutant SOD1-mediated motor neuron cell death and increase amyotrophic lateral sclerosis-like transgenic mouse survival. J Neurochem. 80:2002;488-500
29. Lopez E., Figueroa S., Oset-Gasque M.J., Gonzalez M.P. Apoptosis and necrosis Two distinct events induced by cadmium in cortical neurons in culture. Br J Pharmacol. 138:2003;901-911
30. Macey P.M., Henderson L.A., Macey K.E., Alger J.R., Frysinger R.C., Woo M.A., Harper R.K., Yan-Go F.L., Harper R.M. Brain morphology associated with obstructive sleep apnea. Am J Respir Crit Care Med. 166:2002;1382-1387
31. Macey P.M., Macey K.E., Henderson L.A., Alger J.R., Frysinger R.C., Woo M.A., Yan-Go F., Harper R.M. Functional magnetic resonance imaging responses to expiratory loading in obstructive sleep apnea. Respir Physiol Neurobiol. 138:2003;275-290
32. Montplaisir J., Bedard M.A., Richer F., Rouleau I. Neurobehavioral manifestations in obstructive sleep apnea syndrome before and after treatment with continuous positive airway pressure. Sleep. 15:1992;S17-S19
33. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods. 11:1984;47-60
34. Oliver C.N., Starke-Reed P.E., Stadtman E.R., Liu G.J., Carney J.M., Floyd R.A. Oxidative damage to brain proteins, loss of glutamine synthetase activity, and production of free radicals during ischemia/reperfusion-induced injury to gerbil brain. Proc Natl Acad Sci USA. 87:1990;5144-5147
35. Oyama Y., Hayashi A., Ueha T., Maekawa K. Characterization of 2′, 7′-dichlorofluorescin fluorescence in dissociated mammalian brain neurons Estimation on intracellular content of hydrogen peroxide. Brain Res. 635:1994;113-117
36. Parikh N.A., Katsetos C.D., Ashraf Q.M., Haider S.H., Legido A., Delivoria-Papadopoulos M., Mishra O.P. Hypoxia-induced caspase-3 activation and DNA fragmentation in cortical neurons of newborn piglets Role of nitric oxide. Neurochem Res. 28:2003;1351-1357
37. Peng Y.J., Prabhakar N.R. Reactive oxygen species in the plasticity of respiratory behavior elicited by chronic intermittent hypoxia. J Appl Physiol. 94:2003;2342-2349
38. Rami A. Ischemic neuronal death in the rat hippocampus The calpain-calpastatin-caspase hypothesis. Neurobiol Dis. 13:2003;75-88
39. Row B.W., Kheirandish L., Neville J.J., Gozal D. Impaired spatial learning and hyperactivity in developing rats exposed to intermittent hypoxia. Pediatr Res. 52:2002;449-453
40. Row B.W., Liu R., Xu W., Kheirandish L., Gozal D. Intermittent hypoxia is associated with oxidative stress and spatial learning deficits in the rat. Am J Respir Crit Care Med. 167:2003;1548-1553
41. Saito A., Hayashi T., Okuno S., Ferrand-Drake M., Chan P.H. Overexpression of copper/zinc superoxide dismutase in transgenic mice protects against neuronal cell death after transient focal ischemia by blocking activation of the Bad cell death signaling pathway. J Neurosci. 23:2003;1710-1718
42. Satoh T., Numakawa T., Abiru Y., Yamagata T., Ishikawa Y., Enokido Y., Hatanaka H. Production of reactive oxygen species and release of L-glutamate during superoxide anion-induced cell death of cerebellar granule neurons. J Neurochem. 70:1998;316-324
43. Schmidt-Ullrich R., Memet S., Lilienbaum A., Feuillard J., Raphael M., Israel A. NF-kappaB activity in transgenic mice Developmental regulation and tissue specificity. Development. 122:1996;2117-2128
44. Silver I., Erecinska M. Oxygen and ion concentrations in normoxic and hypoxic brain cells. Adv Exp Med Biol. 454:1998;7-16
45. Sugawara T., Lewen A., Noshita N., Gasche Y., Chan P.H. Effects of global ischemia duration on neuronal, astroglial, oligodendroglial, and microglial reactions in the vulnerable hippocampal CA1 subregion in rats. J Neurotrauma. 19:2002;85-98
46. Sugawara T., Noshita N., Lewen A., Gasche Y., Ferrand-Drake M., Fujimura M., Morita-Fujimura Y., Chan P.H. Overexpression of copper/zinc superoxide dismutase in transgenic rats protects vulnerable neurons against ischemic damage by blocking the mitochondrial pathway of caspase activation. J Neurosci. 22:2002;209-217
47. Tagaito Y., Polotsky V.Y., Campen M.J., Wilson J.A., Balbir A., Smith P.L., Schwartz A.R., O'Donnell C.P. A model of sleep-disordered breathing in the C57BL/6J mouse. J Appl Physiol. 91:2001;2758-2766
48. Wang J.Y., Shum A.Y., Ho Y.J., Wang J.Y. 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. 72:2003;508-519
49. Wang J.Y., Shum A.Y., Wang J.Y. Hypoxia/reoxygenation induces cell injury via different mechanisms in cultured rat cortical neurons and glial cells. Neurosci Lett. 322:2002;187-191
50. Younes M., Ostrowski M., Thompson W., Leslie C., Shewchuk W. Chemical control stability in patients with obstructive sleep apnea. Am J Respir Crit Care Med. 163:2001;1181-1190
51. Young T., Finn L., Hla K.M., Morgan B., Palta M. Snoring as part of a dose-response relationship between sleep-disordered breathing and blood pressure. Sleep. 19:1996;S202-S205
52. Young T., Peppard P.E., Gottlieb D.J. Epidemiology of obstructive sleep apnea A population health perspective. Am J Respir Crit Care Med. 165:2002;1217-1239
53. Young T., Shahar E., Nieto F.J., Redline S., Newman A.B., Gottlieb D.J., Walsleben J.A., Finn L., Enright P., Samet J.M. Predictors of sleep-disordered breathing in community-dwelling adults The sleep heart health study. Arch Intern Med. 162:2002;893-900
54. Zamzami N., Marchetti P., Castedo M., Decaudin D., Macho A., Hirsch T., Susin S.A., Petit P.X., Mignotte B., Kroemer G. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med. 182:1995;367-377