Sleep fragmentation induces cognitive deficits via nicotinamide adenine dinucleotide phosphate oxidase-dependent pathways in mouse

American Journal of Respiratory and Critical Care Medicine

Volumn 184, Issue 11, 2011, Pages 1305-1312

  Nair, Deepti ^a   Zhang, Shelley X L ^a   Ramesh, Vijay ^a   Hakim, Fahed ^a   Kaushal, Navita ^a   Wang, Yang ^a   Gozal, David ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

NADPH oxidase; Neurocognitive impairments; Sleep fragmentation

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; MALONALDEHYDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; BRAIN DYSFUNCTION; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME ACTIVITY; FORCED SWIMMING TEST; GENE EXPRESSION; HIPPOCAMPUS; LEARNING; LIPID PEROXIDATION; MALE; MAZE TEST; MENTAL PERFORMANCE; MOUSE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SLEEP APNEA SYNDROME; SLEEP TIME; SPATIAL MEMORY;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; COGNITION DISORDERS; DEOXYGUANOSINE; DISEASE MODELS, ANIMAL; LIPID PEROXIDATION; MALE; MAZE LEARNING; MICE; MICE, TRANSGENIC; NADPH OXIDASE; OXIDATIVE STRESS; SLEEP DEPRIVATION;

EID: 82555168382     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201107-1173OC     Document Type: Article

References (79)

1. Bonnet MH. Sleep restoration as a function of periodic awakening, movement, or electroencephalographic change. Sleep 1987;10:364-373.
2. Franken P. Long-term vs. short-term processes regulating REM sleep. J Sleep Res 2002;11:17-28. (Pubitemid 34227210)
3. Stepanski EJ. The effect of sleep fragmentation on daytime function. Sleep 2002;25:268-276. (Pubitemid 34496408)
4. Tartar JL, Ward CP, McKenna JT, Thakkar M, Arrigoni E, McCarley RW, Brown RE, Strecker RE. Hippocampal synaptic plasticity and spatial learning are impaired in a rat model of sleep fragmentation. Eur J Neurosci 2006;23:2739-2748. (Pubitemid 43801466)
5. Ward CP, McCoy JG, McKenna JT, Connolly NP, McCarley RW, Strecker RE. Spatial learning and memory deficits following exposure to 24 h of sleep fragmentation or intermittent hypoxia in a rat model of obstructive sleep apnea. Brain Res 2009;1294:128-137.
6. Ward CP, McCarley RW, Strecker RE. Experimental sleep fragmentation impairs spatial reference but not working memory in Fischer/ brown Norway rats. J Sleep Res 2009;18:238-244.
7. Tartar JL,McKenna JT,Ward CP,McCarley RW, Strecker RE, Brown RE. Sleep fragmentation reduces hippocampal Ca1 pyramidal cell excitability and response to adenosine. Neurosci Lett 2010;469:1-5.
8. Coleman RM, Roffwarg HP, Kennedy SJ, Guilleminault C, Cinque J, Cohn MA, Karacan I, Kupfer DJ, Lemmi H, Miles LE, et al. Sleep-wake disorders based on a polysomnographic diagnosis. A national cooperative study. JAMA 1982;247:997-1003. (Pubitemid 12162303)
9. Montplaisir J, Bedard MA, Richer F, Rouleau I. Neurobehavioral manifestations in obstructive sleep apnea syndrome before and after treatment with continuous positive airway pressure. Sleep 1992;15:S17-S19. (Pubitemid 23004826)
10. Beebe DW, 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. (Pubitemid 34227209)
11. Carpagnano GE, Kharitonov SA, Resta O, Foschino-Barbaro MP, Gramiccioni E, Barnes PJ. Increased 8-isoprostane and interleukin-6 in breath condensate of obstructive sleep apnea patients. Chest 2002; 122:1162-1167. (Pubitemid 35339525)
12. Macey PM, Henderson LA, Macey KE, Alger JR, Frysinger RC, Woo MA, Harper RK, Yan-Go FL, Harper RM. Brain morphology associated with obstructive sleep apnea. Am J Respir Crit Care Med 2002; 166:1382-1387. (Pubitemid 35292706)
13. Gozal D, Crabtree VM, Sans Capdevila O, Witcher LA, Kheirandish- Gozal L. C-reactive protein, obstructive sleep apnea, and cognitive dysfunction in school-aged children. Am J Respir Crit Care Med 2007;176:188-193. (Pubitemid 47057856)
14. Nair D, Dayyat EA, Zhang SX, Wang Y, Gozal D. Intermittent hypoxia-induced cognitive deficits are mediated by NADPH oxidase activity in a murine model of sleep apnea. PLoS ONE 2011;6:e19847.
15. Silva RH, Abilio VC, Takatsu AL, Kameda SR, Grassl C, Chehin AB, Medrano WA, Calzavara MB, Registro S, Andersen ML, et al. Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice. Neuropharmacology 2004;46:895-903. (Pubitemid 38368922)
16. Gopalakrishnan A, Ji LL, Cirelli C. Sleep deprivation and cellular responses to oxidative stress. Sleep 2004;27:27-35. (Pubitemid 43906309)
17. Ramanathan L, Gulyani S, Nienhuis R, Siegel JM. Sleep deprivation decreases superoxide dismutase activity in rat hippocampus and brainstem. Neuroreport 2002;13:1387-1390.
18. Kumar A, Kalonia H. Protective effect of withania somnifera dunal on the behavioral and biochemical alterations in sleep-disturbed mice (grid over water suspended method). Indian J Exp Biol 2007;45:524-528.
19. Ikeda M, Ikeda-Sagara M, Okada T, Clement P, Urade Y, Nagai T, Sugiyama T, Yoshioka T, Honda K, Inoue S. Brain oxidation is an initial process in sleep induction. Neuroscience 2005;130:1029-1040. (Pubitemid 40094633)
20. Ikeda-Sagara M, Ikeda M. Oxidative stress and sleep homeostasis. Nippon Yakurigaku Zasshi 2007;129:404-407. (Pubitemid 351325836)
21. Honda K, Komoda Y, Inoue S. Oxidized glutathione regulates physiological sleep in unrestrained rats. Brain Res 1994;636:253-258. (Pubitemid 24044642)
22. Quinn MT, Gauss KA. Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. J Leukoc Biol 2004;76:760-781. (Pubitemid 39313712)
23. Tejada-Simon MV, Serrano F, Villasana LE, Kanterewicz BI, Wu GY, Quinn MT, Klann E. Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol Cell Neurosci 2005;29:97-106. (Pubitemid 40603884)
24. Dringen R. Oxidative and antioxidative potential of brain microglial cells. Antioxid Redox Signal 2005;7:1223-1233. (Pubitemid 41232519)
25. Serrano F, Kolluri NS,Wientjes FB, Card JP, Klann E. NADPH oxidase immunoreactivity in the mouse brain. Brain Res 2003;988:193-198. (Pubitemid 37289510)
26. Vallet P, Charnay Y, Steger K, Ogier-Denis E, Kovari E, Herrmann F, Michel JP, Szanto I. Neuronal expression of the NADPH oxidase NOX4, and its regulation in mouse experimental brain ischemia. Neuroscience 2005;132:233-238. (Pubitemid 40417898)
27. Bedard K, Krause KH. The NIX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007;87:245-313. (Pubitemid 46209993)
28. Abramov AY, Jacobson J, Wientjes F, Hothersall J, Canevari L, Duchen MR. Expression and modulation of an NADPH oxidase in mammalian astrocytes. J Neurosci 2005;25:9176-9184. (Pubitemid 41500826)
29. Kaplan R. Obstructive sleep apnoea and depression: diagnostic and treatment implications. Aust N Z J Psychiatry 1992;26:586-591. (Pubitemid 23033232)
30. Borak J, Cieslicki JK, Koziej M, Matuszewski A, Zielinski J. Effects of CPAP treatment on psychological status in patients with severe obstructive sleep apnoea. J Sleep Res 1996;5:123-127. (Pubitemid 26236004)
31. Bardwell WA, Ancoli-Israel S, Dimsdale JE. Types of coping strategies are associated with increased depressive symptoms in patients with obstructive sleep apnea. Sleep 2001;24:905-909. (Pubitemid 33116991)
32. Sanchez AI, Buela-Casal G, Bermudez MP, Casas-Maldonado F. The effects of continuous positive air pressure treatment on anxiety and depression levels in apnea patients. Psychiatry Clin Neurosci 2001;55:641-646. (Pubitemid 33126539)
33. Akashiba T, Kawahara S, Akahoshi T, Omori C, Saito O, Majima T, Horie T. Relationship between quality of life and mood or depression in patients with severe obstructive sleep apnea syndrome. Chest 2002;122:861-865.
34. El-Sheikh M, Kelly RJ, Buckhalt JA, Benjamin Hinnant J. Children's sleep and adjustment over time: the role of socioeconomic context. Child Dev 2010;81:870-883.
35. Ramesh V, Kaushal N, Gozal D. Sleep fragmentation modifies EEG delta power during slow wave sleep in socially isolated and paired mice. Sleep Science 2009;2:64-75.
36. Espana RA, McCormack SL, Mochizuki T, Scammell TE. Running promotes wakefulness and increases cataplexy in orexin knockout mice. Sleep 2007;30:1417-1425. (Pubitemid 350036969)
37. Morris RG, Garrud P, Rawlins JN, O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982;297:681-683. (Pubitemid 12096189)
38. Gerlai R, Clayton NS. Analysing hippocampal function in transgenic mice: an ethological perspective. Trends Neurosci 1999;22:47-51. (Pubitemid 29125549)
39. Eckeli AL, Dach F, Rodrigues AL. Acute treatments with GMP produce antidepressant-like effects in mice. Neuroreport 2000;11:1839-1843. (Pubitemid 30429121)
40. Dias Elpo Zomkowski A, Oscar Rosa A, Lin J, Santos AR, Calixto JB, Lucia Severo Rodrigues A. Evidence for serotonin receptor subtypes involvement in agmatine antidepressant like-effect in the mouse forced swimming test. Brain Res 2004;1023:253-263. (Pubitemid 39221428)
41. Miller FJ Jr, Griendling KK. Functional evaluation of nonphagocytic NAD(P)H oxidases. Methods Enzymol 2002;353:220-233. (Pubitemid 34625593)
42. Gozal D, Nair D, Goldbart AD. Physical activity attenuates intermittent hypoxia-induced spatial learning deficits and oxidative stress. Am J Respir Crit Care Med 2010;182:104-112.
43. Zhan G, Serrano F, Fenik P, Hsu R, Kong L, Pratico D, Klann E. 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. (Pubitemid 41369078)
44. Smith CT, Conway JM, Rose GM. Brief paradoxical sleep deprivation impairs reference, but not working, memory in the radial arm maze task. Neurobiol Learn Mem 1998;69:211-217. (Pubitemid 28364517)
45. Alhaider IA, Aleisa AM, Tran TT, Alzoubi KH, Alkadhi KA. Chronic caffeine treatment prevents sleep deprivation-induced impairment of cognitive function and synaptic plasticity. Sleep 2010;33:437-444.
46. Youngblood BD, Smagin GN, Elkins PD, Ryan DH, Harris RB. The effects of paradoxical sleep deprivation and valine on spatial learning and brain 5-HT metabolism. Physiol Behav 1999;67:643-649.
47. Graves LA, Heller EA, Pack AI, Abel T. Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning. Learn Mem 2003;10:168-176. (Pubitemid 36666394)
48. Bjorness TE, Riley BT, Tysor MK, Poe GR. REM restriction persistently alters strategy used to solve a spatial task. Learn Mem 2005;12:352-359. (Pubitemid 40958347)
49. Dworak M, McCarley RW, Kim T, Kalinchuk AV, Basheer R. Sleep and brain energy levels: ATP changes during sleep. J Neurosci 2010;30:9007-9016.
50. Droge W. The plasma redox state and ageing. Ageing Res Rev 2002;1:257-278. (Pubitemid 38340345)
51. Akki A, Zhang M, Murdoch C, Brewer A, Shah AM. NADPH oxidase signaling and cardiac myocyte function. J Mol Cell Cardiol 2009;47:15-22.
52. Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 2004;4:181-189. (Pubitemid 38339084)
53. Lambeth JD. NOX enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic Biol Med 2007;43:332-347. (Pubitemid 46992767)
54. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007;39:44-84. (Pubitemid 44566469)
55. Berry CE, Hare JM. Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms and pathophysiological implications. J Physiol 2004;555:589-606. (Pubitemid 38404582)
56. Muralikrishna Adibhatla R, Hatcher JF. Phospholipase A2, reactive oxygen species, and lipid peroxidation in cerebral ischemia. Free Radic Biol Med 2006;40:376-387. (Pubitemid 43139673)
57. 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.
58. Fukui T, Lassegue B, Kai H, Alexander RW, Griendling KK. Cytochrome B-558 alpha-subunit cloning and expression in rat aortic smooth muscle cells. Biochim Biophys Acta 1995;1231:215-219.
59. Colton CA, Fagni L, Gilbert D. The action of hydrogen peroxide on paired pulse and long-term potentiation in the hippocampus. Free Radic Biol Med 1989;7:3-8. (Pubitemid 19165148)
60. Auerbach JM, Segal M. Peroxide modulation of slow onset potentiation in rat hippocampus. J Neurosci 1997;17:8695-8701. (Pubitemid 27481735)
61. Kamsler A, Segal M. Hydrogen peroxide modulation of synaptic plasticity. J Neurosci 2003;23:269-276. (Pubitemid 36050427)
62. Kamsler A, Segal M. Paradoxical actions of hydrogen peroxide on long-term potentiation in transgenic superoxide dismutase-1 mice. J Neurosci 2003;23:10359-10367. (Pubitemid 37444613)
63. Kishida KT, Klann E. Sources and targets of reactive oxygen species in synaptic plasticity and memory. Antioxid Redox Signal 2007;9:233-244. (Pubitemid 46105422)
64. Hidalgo C, Carrasco MA, Munoz P, Nunez MT. A role for reactive oxygen/nitrogen species and iron on neuronal synaptic plasticity. Antioxid Redox Signal 2007;9:245-255. (Pubitemid 46105423)
65. Benoit CE, Bastianetto S, Brouillette J, Tse Y, Boutin JA, Delagrange P, Wong T, Sarret P, Quirion R. Loss of quinone reductase 2 function selectively facilitates learning behaviors. J Neurosci 2010;30:12690-12700.
66. Noh KM, Koh JY. Induction and activation by zinc of NADPH oxidase in cultured cortical neurons and astrocytes. J Neurosci 2000;20:RC111.
67. Jang HJ, Hwang S, Cho KY. Kim DK, Chay KO, Kim JK. Taxol induces oxidative neuronal cell death by enhancing the activity of NADPH oxidase in mouse cortical cultures. Neurosci Lett 2008;443:17-22.
68. Dennis KE, Aschner JL, Milatovic D, Schmidt JW, Aschner M, Kaplowitz MR, Zhang Y, Fike CD. 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.
69. Rathore R, Zheng YM, Niu CF, Liu QH, Korde A, Ho YS, Wang YX. Hypoxia activates NADPH oxidase to increase [ROS]i and [Ca21]i through the mitochondrial ROS-pkcepsilon signaling axis in pulmonary artery smooth muscle cells. Free Radic Biol Med 2008;45:1223-1231.
70. 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.
71. Gharib S, Dayyat E, Khalyfa A, Kim JK, Clair H, Kucia M, Gozal D. Intermittent hypoxia mobilizes bone marrow-derived very small embryonic-like stem cells and activates developmental transcriptional programs in mice. Sleep 2010;11:1439-1446.
72. Ohayon MM. The effects of breathing-related sleep disorders on mood disturbances in the general population. J Clin Psychiatry 2003;64:1195-1200; quiz, 1274-1196.
73. File SE. Behavioural detection of anxiolytic action. In: Elliott JM, Heal DJ, Marsden CA, editors. Experimental approaches to anxiety and depression. Chichester, UK: Wiley; 1992. pp. 25-44.
74. D'Almeida V, Lobo LL, Hipolide DC, de Oliveira AC, Nobrega JN, Tufik S. Sleep deprivation induces brain region-specific decreases in glutathione levels. Neuroreport 1998;9:2853-2856. (Pubitemid 28435176)
75. Singh R, Kiloung J, Singh S, Sharma D. Effect of paradoxical sleep deprivation on oxidative stress parameters in brain regions of adult and old rats. Biogerontology 2008;9:153-162.
76. Khadrawy YA, Nour NA, Aboul Ezz HS. Effect of oxidative stress induced by paradoxical sleep deprivation on the activities of Na+, K+- ATPase and acetylcholinesterase in the cortex and hippocampus of rat. Transl Res 2011;157:100-107.
77. Hovatta I, Juhila J, Donner J. Oxidative stress in anxiety and comorbid disorders. Neurosci Res 2010;68:261-275.
78. Pellow S, Chopin P, File SE, Briley M. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985;14:149-167. (Pubitemid 16239568)
79. 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.