Reactive oxygen species and the brain in sleep apnea

Respiratory Physiology and Neurobiology

Volumn 174, Issue 3, 2010, Pages 307-316

  Wang, Yang ^a   Zhang, Shelley X L ^a   Gozal, David ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Intermittent hypoxia; Mitochondria; NADPH oxidase; Obstructive sleep apnea; Reactive oxygen species

Indexed keywords

CYTOCHROME P450; LIPOXYGENASE; PHOSPHOLIPASE A2; PROSTAGLANDIN SYNTHASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; XANTHINE OXIDASE;

ANTIOXIDANT ACTIVITY; BRAIN; BRAIN CELL; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME SUBUNIT; HUMAN; HYPOXIA; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NERVE CELL LESION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SLEEP APNEA SYNDROME;

ANIMALS; BRAIN; HUMANS; MITOCHONDRIA; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; SLEEP APNEA SYNDROMES;

EID: 78449285920     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2010.09.001     Document Type: Review

References (136)

1. Abramov A.Y., Canevari L., Duchen M.R. Beta-amyloid peptides induce mitochondrial dysfunction and oxidative stress in astrocytes and death of neurons through activation of NADPH oxidase. J. Neurosci. 2004, 24:565-575.
2. Akki A., Zhang M., Murdoch C., Brewer A., Shah A.M. NADPH oxidase signaling and cardiac myocyte function. J. Mol. Cell. Cardiol. 2009, 47:15-22.
3. Albin R.L., Greenamyre J.T. Alternative excitotoxic hypotheses. Neurology 1992, 42:733-738.
4. Aldieri E., Riganti C., Polimeni M., Gazzano E., Lussiana C., Campia I., Ghigo D. Classical inhibitors of NOX NAD(P)H oxidases are not specific. Curr. Drug Metab. 2008, 9:686-696.
5. Andreyev A.Y., Kushnareva Y.E., Starkov A.A. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc.) 2005, 70:200-214.
6. Angermuller S., Islinger M., Volkl A. Peroxisomes and reactive oxygen species, a lasting challenge. Histochem. Cell Biol. 2009, 131:459-463.
7. Aon M.A., Cortassa S., Marban E., O'Rourke B. Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J. Biol. Chem. 2003, 278:44735-44744.
8. Beal M.F. Aging, energy, and oxidative stress in neurodegenerative diseases. Ann. Neurol. 1995, 38:357-366.
9. Bedard K., Krause K.H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 2007, 87:245-313.
10. Beebe D.W. Neurobehavioral effects of obstructive sleep apnea: an overview and heuristic model. Curr. Opin. Pulm. Med. 2005, 11:494-500.
11. 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. 2002, 11:1-16.
12. Bell E.L., Klimova T.A., Eisenbart J., Moraes C.T., Murphy M.P., Budinger G.R., Chandel N.S. The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J. Cell Biol. 2007, 177:1029-1036.
13. Berg J.M., Tymoczko J.L., Stryer L. Oxidative Phosphorylation, Biochemistry 2002, W. H. Freeman and Company, New York, pp. 491-526. Fifth ed.
14. Berry C.E., Hare J.M. Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms and pathophysiological implications. J. Physiol. 2004, 555:589-606.
15. Bonsignore M.R., Zito A. Metabolic effects of the obstructive sleep apnea syndrome and cardiovascular risk. Arch. Physiol. Biochem. 2008, 114:255-260.
16. Bossy-Wetzel E., Schwarzenbacher R., Lipton S.A. Molecular pathways to neurodegeneration. Nat. Med. 2004, 10(Suppl.):S2-S9.
17. Boveris A., Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem. J. 1973, 134:707-716.
18. Boyer P.D. The ATP synthase-a splendid molecular machine. Annu. Rev. Biochem. 1997, 66:717-749.
19. Brady N.R., Hamacher-Brady A., Westerhoff H.V., Gottlieb R.A. A wave of reactive oxygen species (ROS)-induced ROS release in a sea of excitable mitochondria. Antioxid. Redox Signal. 2006, 8:1651-1665.
20. Brand M.D. The sites and topology of mitochondrial superoxide production. Exp. Gerontol. 2010, 45:466-472.
21. Bredt D.S. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic. Res. 1999, 31:577-596.
22. Burckhardt I.C., Gozal D., Dayyat E., Cheng Y., Li R.C., Goldbart A.D., Row B.W. Green tea catechin polyphenols attenuate behavioral and oxidative responses to intermittent hypoxia. Am. J. Respir. Crit. Care Med. 2008, 177:1135-1141.
23. Butterfield D., Castegna A., Pocernich C., Drake J., Scapagnini G., Calabrese V. Nutritional approaches to combat oxidative stress in Alzheimer's disease. J. Nutr. Biochem. 2002, 13:444.
24. Cape J.L., Bowman M.K., Kramer D.M. A semiquinone intermediate generated at the Qo site of the cytochrome bc1 complex: importance for the Q-cycle and superoxide production. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:7887-7892.
25. Chandel N.S., Maltepe E., Goldwasser E., Mathieu C.E., Simon M.C., Schumacker P.T. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:11715-11720.
26. Chen Q., Vazquez E.J., Moghaddas S., Hoppel C.L., Lesnefsky E.J. Production of reactive oxygen species by mitochondria: central role of complex III. J. Biol. Chem. 2003, 278:36027-36031.
27. Chen Q., Yin G., Stewart S., Hu Y., Lesnefsky E.J. Isolating the segment of the mitochondrial electron transport chain responsible for mitochondrial damage during cardiac ischemia. Biochem. Biophys. Res. Commun. 2010, 397:656-660.
28. Choi S.H., Lee D.Y., Kim S.U., Jin B.K. Thrombin-induced oxidative stress contributes to the death of hippocampal neurons in vivo: role of microglial NADPH oxidase. J. Neurosci. 2005, 25:4082-4090.
29. Clark R.A., Leidal K.G., Pearson D.W., Nauseef W.M. NADPH oxidase of human neutrophils. Subcellular localization and characterization of an arachidonate-activatable superoxide-generating system. J. Biol. Chem. 1987, 262:4065-4074.
30. Daiber A. Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim. Biophys. Acta 2010, 1797:897-906.
31. de Frutos S., Caldwell E., Nitta C.H., Kanagy N.L., Wang J., Wang W., Walker M.K., Gonzalez Bosc L.V. NFATc3 contributes to intermittent hypoxia-induced arterial remodeling in mice. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H356-H363.
32. Dennis K.E., Aschner J.L., Milatovic D., Schmidt J.W., Aschner M., Kaplowitz M.R., Zhang Y., Fike C.D. NADPH oxidases and reactive oxygen species at different stages of chronic hypoxia-induced pulmonary hypertension in newborn piglets. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 297:L596-L607.
33. Desouki M.M., Kulawiec M., Bansal S., Das G.M., Singh K.K. Cross talk between mitochondria and superoxide generating NADPH oxidase in breast and ovarian tumors. Cancer Biol. Ther. 2005, 4:1367-1373.
34. Diebold I., Petry A., Hess J., Gorlach A. The NADPH oxidase subunit NOX4 is a new target gene of the hypoxia-inducible factor-1. Mol. Biol. Cell 2010, 21:2087-2096.
35. Doughan A.K., Harrison D.G., Dikalov S.I. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ. Res. 2008, 102:488-496.
36. Douglas R.M., Ryu J., Kanaan A., Del Carmen Rivero M., Dugan L.L., Haddad G.G., Ali S.S. Neuronal death during combined intermittent hypoxia/hypercapnia is due to mitochondrial dysfunction. Am. J. Physiol. Cell Physiol. 2010, 298:C1594-C1602.
37. Droge W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82:47-95.
38. El-Benna J., Dang P.M., Gougerot-Pocidalo M.A., Marie J.C., Braut-Boucher F. p47phox, the phagocyte NADPH oxidase/NOX2 organizer: structure, phosphorylation and implication in diseases. Exp. Mol. Med. 2009, 41:217-225.
39. Fan C., Iacobas D.A., Zhou D., Chen Q., Lai J.K., Gavrialov O., Haddad G.G. Gene expression and phenotypic characterization of mouse heart after chronic constant or intermittent hypoxia. Physiol. Genomics 2005, 22:292-307.
40. Fedotcheva N.I., Sokolov A.P., Kondrashova M.N. Nonezymatic formation of succinate in mitochondria under oxidative stress. Free Radic. Biol. Med. 2006, 41:56-64.
41. Gao H.M., Liu B., Hong J.S. Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci. 2003, 23:6181-6187.
42. Goldbart A., Row B.W., Kheirandish L., Schurr A., Gozal E., Guo S.Z., Payne R.S., Cheng Z., Brittian K.R., Gozal D. Intermittent hypoxic exposure during light phase induces changes in cAMP response element binding protein activity in the rat CA1 hippocampal region: water maze performance correlates. Neuroscience 2003, 122:585-590.
43. Goldbart A.D., Row B.W., Kheirandish-Gozal L., Cheng Y., Brittian K.R., Gozal D. High fat/refined carbohydrate diet enhances the susceptibility to spatial learning deficits in rats exposed to intermittent hypoxia. Brain Res. 2006, 1090:190-196.
44. Gozal D., Daniel J.M., Dohanich G.P. Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat. J. Neurosci. 2001, 21:2442-2450.
45. Gozal D., Kheirandish-Gozal L. Neurocognitive and behavioral morbidity in children with sleep disorders. Curr. Opin. Pulm. Med. 2007, 13:505-509.
46. Gozal D., Kheirandish-Gozal L. Cardiovascular morbidity in obstructive sleep apnea: oxidative stress, inflammation, and much more. Am. J. Respir. Crit. Care Med. 2008, 177:369-375.
47. Gozal D., Nair D., Goldbart A.D. Physical activity attenuates intermittent hypoxia-induced spatial learning deficits and oxidative stress. Am. J. Respir. Crit. Care Med. 2010, 182:104-112.
48. Gozal D., Row B.W., Gozal E., Kheirandish L., Neville J.J., Brittian K.R., Sachleben L.R., Guo S.Z. Temporal aspects of spatial task performance during intermittent hypoxia in the rat: evidence for neurogenesis. Eur. J. Neurosci. 2003, 18:2335-2342.
49. Gozal D., Row B.W., Kheirandish L., Liu R., Guo S.Z., Qiang F., Brittian K.R. Increased susceptibility to intermittent hypoxia in aging rats: changes in proteasomal activity, neuronal apoptosis and spatial function. J. Neurochem. 2003, 86:1545-1552.
50. Gozal E., Gozal D., Pierce W.M., Thongboonkerd V., Scherzer J.A., Sachleben L.R., Brittian K.R., Guo S.Z., Cai J., Klein J.B. Proteomic analysis of CA1 and CA3 regions of rat hippocampus and differential susceptibility to intermittent hypoxia. J. Neurochem. 2002, 83:331-345.
51. Gozal E., Row B.W., Schurr A., Gozal D. Developmental differences in cortical and hippocampal vulnerability to intermittent hypoxia in the rat. Neurosci. Lett. 2001, 305:197-201.
52. Groemping Y., Rittinger K. Activation and assembly of the NADPH oxidase: a structural perspective. Biochem. J. 2005, 386:401-416.
53. Gupte S.A. Glucose-6-phosphate dehydrogenase: a novel therapeutic target in cardiovascular diseases. Curr. Opin. Investig. Drugs 2008, 9:993-1000.
54. Gutierrez J., Ballinger S.W., Darley-Usmar V.M., Landar A. Free radicals, mitochondria, and oxidized lipids: the emerging role in signal transduction in vascular cells. Circ. Res. 2006, 99:924-932.
55. Guzy R.D., Hoyos B., Robin E., Chen H., Liu L., Mansfield K.D., Simon M.C., Hammerling U., Schumacker P.T. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 2005, 1:401-408.
56. Guzy R.D., Schumacker P.T. Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp. Physiol. 2006, 91:807-819.
57. Gyulkhandanyan A.V., Pennefather P.S. Shift in the localization of sites of hydrogen peroxide production in brain mitochondria by mitochondrial stress. J. Neurochem. 2004, 90:405-421.
58. Halliwell B. Oxidative stress and neurodegeneration: where are we now?. J. Neurochem. 2006, 97:1634-1658.
59. Han D., Antunes F., Canali R., Rettori D., Cadenas E. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J. Biol. Chem. 2003, 278:5557-5563.
60. He L., Liu X., Chen J., Dinger B., Stensaas L., Fidone S. Modulation of chronic hypoxia-induced chemoreceptor hypersensitivity by NADPH oxidase subunits in rat carotid body. J. Appl. Physiol. 2010, 108:1304-1310.
61. Hinkle P.C., Butow R.A., Racker E., Chance B. Partial resolution of the enzymes catalyzing oxidative phosphorylation. XV. Reverse electron transfer in the flavin-cytochrome beta region of the respiratory chain of beef heart submitochondrial particles. J. Biol. Chem. 1967, 242:5169-5173.
62. Hoffman D.L., Salter J.D., Brookes P.S. Response of mitochondrial reactive oxygen species generation to steady-state oxygen tension: implications for hypoxic cell signaling. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H101-H108.
63. Hui-guo L., Kui L., Yan-ning Z., Yong-jian X. Apocynin attenuate spatial learning deficits and oxidative responses to intermittent hypoxia. Sleep Med. 2010, 11:205-212.
64. Ibi M., Katsuyama M., Fan C., Iwata K., Nishinaka T., Yokoyama T., Yabe-Nishimura C. NOX1/NADPH oxidase negatively regulates nerve growth factor-induced neurite outgrowth. Free Radic. Biol. Med. 2006, 40:1785-1795.
65. Johnson J.E., Choksi K., Widger W.R. NADH-Ubiquinone oxidoreductase: substrate-dependent oxygen turnover to superoxide anion as a function of flavin mononucleotide. Mitochondrion 2003, 3:97-110.
66. Joseph J.A., Denisova N., Villalobos-Molina R., Erat S., Strain J. Oxidative stress and age-related neuronal deficits. Mol. Chem. Neuropathol. 1996, 28:35-40.
67. Jun J., Reinke C., Bedja D., Berkowitz D., Bevans-Fonti S., Li J., Barouch L.A., Gabrielson K., Polotsky V.Y. Effect of intermittent hypoxia on atherosclerosis in apolipoprotein E-deficient mice. Atherosclerosis 2010, 209:381-386.
68. Kahles T., Luedike P., Endres M., Galla H.J., Steinmetz H., Busse R., Neumann-Haefelin T., Brandes R.P. NADPH oxidase plays a central role in blood-brain barrier damage in experimental stroke. Stroke 2007, 38:3000-3006.
69. Kamga C.K., Zhang S.X., Wang Y. Dicarboxylate carrier-mediated glutathione transport is essential for reactive oxygen species homeostasis and normal respiration in rat brain mitochondria. Am. J. Physiol. Cell Physiol. 2010, 299:C497-C505.
70. Kamsler A., Segal M. Hydrogen peroxide as a diffusible signal molecule in synaptic plasticity. Mol. Neurobiol. 2004, 29:167-178.
71. Khan S., Nanduri J., Yuan G., Kinsman B., Kumar G.K., Joseph J., Kalyanaraman B., Prabhakar N.R. NOX2 mediates intermittent hypoxia-induced mitochondrial complex i inhibition: relevance to blood pressure changes in rats. Antioxid. Redox Signal. 2010.
72. Kheirandish L., Row B.W., Li R.C., Brittian K.R., Gozal D. Apolipoprotein E-deficient mice exhibit increased vulnerability to intermittent hypoxia-induced spatial learning deficits. Sleep 2005, 28:1412-1417.
73. Kimura S., Zhang G.X., Nishiyama A., Shokoji T., Yao L., Fan Y.Y., Rahman M., Suzuki T., Maeta H., Abe Y. Role of NAD(P)H oxidase- and mitochondria-derived reactive oxygen species in cardioprotection of ischemic reperfusion injury by angiotensin II. Hypertension 2005, 45:860-866.
74. Korshunov S.S., Skulachev V.P., Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 1997, 416:15-18.
75. Kubota C., Torii S., Hou N., Saito N., Yoshimoto Y., Imai H., Takeuchi T. Constitutive reactive oxygen species generation from autophagosome/lysosome in neuronal oxidative toxicity. J. Biol. Chem. 2010, 285:667-674.
76. Kudin A.P., Bimpong-Buta N.Y., Vielhaber S., Elger C.E., Kunz W.S. Characterization of superoxide-producing sites in isolated brain mitochondria. J. Biol. Chem. 2004, 279:4127-4135.
77. Kushnareva Y., Murphy A.N., Andreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem. J. 2002, 368:545-553.
78. Lambeth J.D. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 2004, 4:181-189.
79. Lavie L. Obstructive sleep apnoea syndrome-an oxidative stress disorder. Sleep Med. Rev. 2003, 7:35-51.
80. Lavie L., Dyugovskaya L., Golan-Shany O., Lavie P. Heat-shock protein 70: expression in monocytes of patients with sleep apnoea and association with oxidative stress and tumour necrosis factor-alpha. J. Sleep Res. 2010, 19:139-147.
81. Lavie L., Lavie P. Molecular mechanisms of cardiovascular disease in OSAHS: the oxidative stress link. Eur. Respir. J. 2009, 33:1467-1484.
82. Lavigne M.C., Malech H.L., Holland S.M., Leto T.L. Genetic requirement of p47phox for superoxide production by murine microglia. FASEB J. 2001, 15:285-287.
83. Lee S.B., Bae I.H., Bae Y.S., Um H.D. Link between mitochondria and NADPH oxidase 1 isozyme for the sustained production of reactive oxygen species and cell death. J. Biol. Chem. 2006, 281:36228-36235.
84. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J.A., Robinson J.P. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 2003, 278:8516-8525.
85. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
86. Liu Y., Fiskum G., Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 2002, 80:780-787.
87. Lumeng J.C., Chervin R.D. Epidemiology of pediatric obstructive sleep apnea. Proc. Am. Thorac. Soc. 2008, 5:242-252.
88. 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. 2002, 166:1382-1387.
89. Macey P.M., Kumar R., Woo M.A., Valladares E.M., Yan-Go F.L., Harper R.M. Brain structural changes in obstructive sleep apnea. Sleep 2008, 31:967-977.
90. MacFarlane P.M., Satriotomo I., Windelborn J.A., Mitchell G.S. NADPH oxidase activity is necessary for acute intermittent hypoxia-induced phrenic long-term facilitation. J. Physiol. 2009, 587:1931-1942.
91. Malec V., Gottschald O.R., Li S., Rose F., Seeger W., Hanze J. HIF-1 alpha signaling is augmented during intermittent hypoxia by induction of the Nrf2 pathway in NOX1-expressing adenocarcinoma A549 cells. Free Radic. Biol. Med. 2010, 48:1626-1635.
92. Matsuzaki S., Szweda P.A., Szweda L.I., Humphries K.M. Regulated production of free radicals by the mitochondrial electron transport chain: cardiac ischemic preconditioning. Adv. Drug Deliv. Rev. 2009, 61:1324-1331.
93. Mitchell P. The protonmotive Q cycle: a general formulation. FEBS Lett. 1975, 59:137-139.
94. Muller F.L., Liu Y., Van Remmen H. Complex III releases superoxide to both sides of the inner mitochondrial membrane. J. Biol. Chem. 2004, 279:49064-49073.
95. Muralikrishna Adibhatla R., Hatcher J.F. Phospholipase A2, reactive oxygen species, and lipid peroxidation in cerebral ischemia. Free Radic. Biol. Med. 2006, 40:376-387.
96. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
97. Nakamura K., Bindokas V.P., Kowlessur D., Elas M., Milstien S., Marks J.D., Halpern H.J., Kang U.J. Tetrahydrobiopterin scavenges superoxide in dopaminergic neurons. J. Biol. Chem. 2001, 276:34402-34407.
98. Nisimoto Y., Motalebi S., Han C.H., Lambeth J.D. The p67(phox) activation domain regulates electron flow from NADPH to flavin in flavocytochrome b(558). J. Biol. Chem. 1999, 274:22999-23005.
99. 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. U.S.A. 1990, 87:5144-5147.
100. Page M.M., Robb E.L., Salway K.D., Stuart J.A. Mitochondrial redox metabolism: aging, longevity and dietary effects. Mech. Ageing Dev. 2010, 131:242-252.
101. Park K.W., Baik H.H., Jin B.K. IL-13-induced oxidative stress via microglial NADPH oxidase contributes to death of hippocampal neurons in vivo. J. Immunol. 2009, 183:4666-4674.
102. Peng Y.J., Nanduri J., Yuan G., Wang N., Deneris E., Pendyala S., Natarajan V., Kumar G.K., Prabhakar N.R. NADPH oxidase is required for the sensory plasticity of the carotid body by chronic intermittent hypoxia. J. Neurosci. 2009, 29:4903-4910.
103. Punjabi N.M. The epidemiology of adult obstructive sleep apnea. Proc. Am. Thorac. Soc. 2008, 5:136-143.
104. Qin L., Liu Y., Wang T., Wei S.J., Block M.L., Wilson B., Liu B., Hong J.S. NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J. Biol. Chem. 2004, 279:1415-1421.
105. Rae C., Bartlett D.J., Yang Q., Walton D., Denotti A., Sachinwalla T., Grunstein R.R. Dynamic changes in brain bioenergetics during obstructive sleep apnea. J. Cereb. Blood Flow Metab. 2009, 29:1421-1428.
106. Raha S., McEachern G.E., Myint A.T., Robinson B.H. Superoxides from mitochondrial complex III: the role of manganese superoxide dismutase. Free Radic. Biol. Med. 2000, 29:170-180.
107. Rathore R., Zheng Y.M., Niu C.F., Liu Q.H., Korde A., Ho Y.S., Wang Y.X. Hypoxia activates NADPH oxidase to increase [ROS]i and [Ca2+]i through the mitochondrial ROS-PKCepsilon signaling axis in pulmonary artery smooth muscle cells. Free Radic. Biol. Med. 2008, 45:1223-1231.
108. 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. 2003, 167:1548-1553.
109. Santos C.X., Tanaka L.Y., Wosniak J., Laurindo F.R. Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid. Redox Signal. 2009, 11:2409-2427.
110. Sateia M.J. Neuropsychological impairment and quality of life in obstructive sleep apnea. Clin. Chest Med. 2003, 24:249-259.
111. Schroder K., Kohnen A., Aicher A., Liehn E.A., Buchse T., Stein S., Weber C., Dimmeler S., Brandes R.P. NADPH oxidase Nox2 is required for hypoxia-induced mobilization of endothelial progenitor cells. Circ. Res. 2009, 105:537-544.
112. Schultz B.E., Chan S.I. Structures and proton-pumping strategies of mitochondrial respiratory enzymes. Annu. Rev. Biophys. Biomol. Struct. 2001, 30:23-65.
113. Schulz R., Mahmoudi S., Hattar K., Sibelius U., Olschewski H., Mayer K., Seeger W., Grimminger F. Enhanced release of superoxide from polymorphonuclear neutrophils in obstructive sleep apnea. Impact of continuous positive airway pressure therapy. Am. J. Respir. Crit. Care Med. 2000, 162:566-570.
114. Serrano F., Kolluri N.S., Wientjes F.B., Card J.P., Klann E. NADPH oxidase immunoreactivity in the mouse brain. Brain Res. 2003, 988:193-198.
115. Shan X., Chi L., Ke Y., Luo C., Qian S., Gozal D., Liu R. Manganese superoxide dismutase protects mouse cortical neurons from chronic intermittent hypoxia-mediated oxidative damage. Neurobiol. Dis. 2007, 28:206-215.
116. Sies H., de Groot H. Role of reactive oxygen species in cell toxicity. Toxicol. Lett. 1992, 64-65(Spec No):547-551.
117. St-Pierre J., Buckingham J.A., Roebuck S.J., Brand M.D. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 2002, 277:44784-44790.
118. Stowe D.F., Camara A.K. Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid. Redox Signal. 2009, 11:1373-1414.
119. Tammariello S.P., Quinn M.T., Estus S. NADPH oxidase contributes directly to oxidative stress and apoptosis in nerve growth factor-deprived sympathetic neurons. J. Neurosci. 2000, 20:RC53.
120. Tejada-Simon M.V., Serrano F., Villasana L.E., Kanterewicz B.I., Wu G.Y., Quinn M.T., Klann E. Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol. Cell. Neurosci. 2005, 29:97-106.
121. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552:335-344.
122. Turrens J.F., Alexandre A., Lehninger A.L. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch. Biochem. Biophys. 1985, 237:408-414.
123. 2 release by lung mitochondria and microsomes. Arch. Biochem. Biophys. 1982, 217:411-421.
124. Veasey S.C., Davis C.W., Fenik P., Zhan G., Hsu Y.J., Pratico D., Gow A. Long-term intermittent hypoxia in mice: protracted hypersomnolence with oxidative injury to sleep-wake brain regions. Sleep 2004, 27:194-201.
125. Vijay R., Kaushal N., Gozal D. Sleep fragmentation differentially modifies EEG delta power during slow wave sleep in socially isolated and paired mice. Sleep Sci. 2009, 2:64-75.
126. Votyakova T.V., Reynolds I.J. DeltaPsi(m)-Dependent and -independent production of reactive oxygen species by rat brain mitochondria. J. Neurochem. 2001, 79:266-277.
127. Vrablic A.S., Albright C.D., Craciunescu C.N., Salganik R.I., Zeisel S.H. Altered mitochondrial function and overgeneration of reactive oxygen species precede the induction of apoptosis by 1-O-octadecyl-2-methyl-rac-glycero-3-phosphocholine in p53-defective hepatocytes. FASEB J. 2001, 15:1739-1744.
128. Wali S.O., Bahammam A.S., Massaeli H., Pierce G.N., Iliskovic N., Singal P.K., Kryger M.H. Susceptibility of LDL to oxidative stress in obstructive sleep apnea. Sleep 1998, 21:290-296.
129. Wenzel P., Mollnau H., Oelze M., Schulz E., Wickramanayake J.M., Muller J., Schuhmacher S., Hortmann M., Baldus S., Gori T., Brandes R.P., Munzel T., Daiber A. First evidence for a crosstalk between mitochondrial and NADPH oxidase-derived reactive oxygen species in nitroglycerin-triggered vascular dysfunction. Antioxid. Redox Signal. 2008, 10:1435-1447.
130. Wosniak J., Santos C.X., Kowaltowski A.J., Laurindo F.R. Cross-talk between mitochondria and NADPH oxidase: effects of mild mitochondrial dysfunction on angiotensin II-mediated increase in Nox isoform expression and activity in vascular smooth muscle cells. Antioxid. Redox Signal. 2009, 11:1265-1278.
131. Wu D.C., Re D.B., Nagai M., Ischiropoulos H., Przedborski S. The inflammatory NADPH oxidase enzyme modulates motor neuron degeneration in amyotrophic lateral sclerosis mice. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:12132-12137.
132. Xu J., Long Y.S., Gozal D., Epstein P.N. Beta-cell death and proliferation after intermittent hypoxia: role of oxidative stress. Free Radic. Biol. Med. 2009, 46:783-790.
133. Xu W., Chi L., Row B.W., Xu R., Ke Y., Xu B., Luo C., Kheirandish L., Gozal D., Liu R. Increased oxidative stress is associated with chronic intermittent hypoxia-mediated brain cortical neuronal cell apoptosis in a mouse model of sleep apnea. Neuroscience 2004, 126:313-323.
134. Yasui H., Hayashi S., Sakurai H. Possible involvement of singlet oxygen species as multiple oxidants in p450 catalytic reactions. Drug Metab. Pharmacokinet. 2005, 20:1-13.
135. Zhan G., Serrano F., Fenik P., Hsu R., Kong L., Pratico D., Klann E., Veasey S.C. NADPH oxidase mediates hypersomnolence and brain oxidative injury in a murine model of sleep apnea. Am. J. Respir. Crit. Care Med. 2005, 172:921-929.
136. Zorov D.B., Juhaszova M., Sollott S.J. Mitochondrial ROS-induced ROS release: an update and review. Biochim. Biophys. Acta 2006, 1757:509-517.