I ntermittent hypoxia from obstructive sleep apnea may cause neuronal impairment and dysfunction in central nervous system: The potential roles played by microglia

Neuropsychiatric Disease and Treatment

Volumn 9, Issue , 2013, Pages 1077-1086

  Yang, Qingchan ^a   Wang, Yan ^a   Feng, Jing ^a   Cao, Jie ^a   Chen, Baoyuan ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Inflammation; Intermittent hypoxia; Microglia; Obstructive sleep apnea

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CD40 LIGAND; CHOLINE; GLUCOCORTICOID; GLUCOSE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; N ACETYLASPARTIC ACID; NEUROTRANSMITTER; OXYGEN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SELECTIN; SUPPRESSOR OF CYTOKINE SIGNALING; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

AIRWAY OBSTRUCTION; APNEA; AROUSAL; BEHAVIOR DISORDER; BRAIN METABOLISM; BRAIN SIZE; CELL ACTIVATION; COGNITIVE DEFECT; COMPUTER ASSISTED EMISSION TOMOGRAPHY; CYTOKINE PRODUCTION; EXECUTIVE FUNCTION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HUMAN; INTELLIGENCE QUOTIENT; INTERMITTENT HYPOXIA; LANGUAGE ABILITY; LEARNING DISORDER; MEMORY DISORDER; MICROGLIA; MITOCHONDRION; NERVE CELL LESION; NERVOUS SYSTEM INFLAMMATION; NEUROLOGIC DISEASE; NEUROPROTECTION; NEUROTOXICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; OXIDATIVE STRESS; OXYGEN DESATURATION; PATHOPHYSIOLOGY; POSITIVE END EXPIRATORY PRESSURE; REVIEW; SIGNAL TRANSDUCTION; SLEEP DISORDERED BREATHING; VERBAL MEMORY; WORKING MEMORY;

EID: 84881290590     PISSN: 11766328     EISSN: 11782021     Source Type: Journal    
DOI: 10.2147/NDT.S49868     Document Type: Review

References (78)

1. Staats R, Stoll P, Zingler D, Virchow JC, Lommatzsch M. Regulation of brain-derived neurotrophic factor (BDNF) during sleep apnoea treatment. Thorax. 2005;60:688-692.
2. Saunamäki T, Himanen SL, Polo O, Jehkonen M. Executive dysfunction in patients with obstructive sleep apnea syndrome. Eur Neurol. 2009;62:237-242.
3. Feng J, Chen BY. Prevalence and incidence of hypertension in obstructive sleep apnea patients and the relationship between obstructive sleep apnea and its confounders. Chin Med J (Engl). 2009;122:1464-1468.
4. Young T, Peppard PE, Gottlieb DJ. Epidemiology of obstructive sleep apnea: a population health perspective. Am J Respir Crit Care Med. 2002;165:1217-1239.
5. National Heart, Lung, and Blood Institute Working Group on Sleep Apnea. Sleep apnea: is your patient at risk? Am Fam Physician. 1996;53:247-253.
6. Lumeng JC, Chervin RD. Epidemiology of pediatric obstructive sleep apnea. Proc Am Thorac Soc. 2008;5:242-252.
7. Feng J, Wu Q, Zhang D, Chen BY. Hippocampal impairments are associated with intermittent hypoxia of obstructive sleep apnea. Chin Med J (Engl). 2012;125:696-701.
8. Sin DD, Fitzgerald F, Parker JD, Newton G, Floras JS, Bradley TD. Risk factors for central and obstructive sleep apnea in 450men and women with congestive heart failure. Am J Respir Crit Care Med. 1999;160:1101-1106.
9. Wetter TC, Böhm GB. Article reviewed: Improvement of sleep apnea in patients with chronic renal failure who undergo nocturnal hemodialysis. Sleep Med. 2001;2:463-465.
10. Yaggi HK, Concato J, Kernan WN, Lichtman JH, Brass LM, Mohsenin V. Obstructive sleep apnea as a risk factor for stroke and death. N Engl J Med. 2005;353:2034-2041.
11. Young T, Palta M, Dempsey J, Skatrud J, Weber S, Badr S. The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med. 1993;328:1230-1235.
12. Young T, Evans L, Finn L, Palta M. Estimation of the clinically diagnosed proportion of sleep apnea syndrome in middle-aged men and women. Sleep. 1997;20:705-706.
13. Lavie L. Oxidative stress-a unifying paradigm in obstructive sleep apnea and comorbidities. Prog Cardiovasc Dis. 2009;51:303-312.
14. Lévy P, Bonsignore MR, Eckel J. Sleep, sleep-disordered breathing and metabolic consequences. Eur Respir J. 2009;34:243-260.
15. Sateia MJ. Neuropsychological impairment and quality of life in obstructive sleep apnea. Clin Chest Med. 2003;24:249-259.
16. Carotenuto M, Santoro N, Grandone A, etal. The insulin gene variable number of tandemrepeats (INS VNTR) genotype and sleep disordered breathing in childhood obesity. J Endocrinol Invest. 2009;32:752-755.
17. Carotenuto M, Bruni O, Santoro N, Del Giudice EM, Perrone L, Pascotto A. Waist circumference predicts the occurrence of sleep-disordered breathing in obese children and adolescents: a questionnaire-based study. Sleep Med. 2006;7:357-361.
18. Carotenuto M, Esposito M, Parisi L, etal. Depressive symptoms and childhood sleep apnea syndrome. Neuropsychiatr Dis Treat. 2012;8:369-373.
19. Daulatzai MA. Death by a thousand cuts in Alzheimer's disease: hypoxia-the prodrome. Neurotox Res. 2013;24(2):216-243.
20. Carotenuto M, Gimigliano F, Fiordelisi G, Ruberto M, Esposito M. Positional abnormalities during sleep in children affected by obstructive sleep apnea syndrome: the putative role of kinetic muscular chains. Med Hypotheses. 2013;81:306-308.
21. Suzuki YJ, Jain V, Park AM, Day RM. Oxidative stress and oxidant signaling in obstructive sleep apnea and associated cardiovascular diseases. Free Radic Biol Med. 2006;40:1683-1692.
22. Prilipko O, Huynh N, Schwartz S, etal. Task positive and default mode networks during a parametric working memory task in obstructive sleep apnea patients and healthy controls. Sleep. 2011;34:293A-301A.
23. Sforza E, Roche F. Sleep apnea syndrome and cognition. Front Neurol. 2012;3:87.
24. Veasey SC, Davis CW, Fenik P, etal. Long-term intermittent hypoxia in mice: protracted hypersomnolence with oxidative injury to sleep-wake brain regions. Sleep. 2004;27:194-201.
25. Polotsky VY, Rubin AE, Balbir A, etal. Intermittent hypoxia causes REM sleep deficits and decreases EEG delta power in NREM sleep in the C57BL/6J mouse. Sleep Med. 2006;7:7-16.
26. Gozal D, Daniel JM, Dohanich GP. Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat. J Neurosci. 2001;21:2442-2450.
27. Wang Y, Zhang SX, Gozal D. Reactive oxygen species and the brain in sleep apnea. Respir Physiol Neurobiol. 2010;174:307-316.
28. Baker TL, Fuller DD, Zabka AG, Mitchell GS. Respiratory plasticity: differential actions of continuous and episodic hypoxia and hypercapnia. Respir Physiol. 2001;129:25-35.
29. Goldbart A, Row BW, Kheirandish L, etal. 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.
30. Gozal D, Row BW, Gozal E, etal. Temporal aspects of spatial task performance during intermittent hypoxia in the rat: evidence for neurogenesis. Eur J Neurosci. 2003;18:2335-2342.
31. O'Hara R. The role of hypoxia in apolipoprotein E4-associated cognitive impairment: implications for neurodegeneration and sleep-disordered breathing. Sleep. 2005;28:1355-1357.
32. Zhan G, Fenik P, Pratico D, Veasey SC. Inducible nitric oxide synthase in long-term intermittent hypoxia: hypersomnolence and brain injury. Am J Respir Crit Care Med. 2005;171:1414-1420.
33. Almendros I, Farré R, Planas AM, etal. Tissue oxygenation in brain, muscle, and fat in a rat model of sleep apnea: differential effect of obstructive apneas and intermittent hypoxia. Sleep. 2011;34:1127-1133.
34. Badoer E. Microglia: activation in acute and chronic inflammatory states and in response to cardiovascular dysfunction. Int J Biochem Cell Biol. 2010;42:1580-1585.
35. Block ML, Hong JS. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol. 2005;76:77-98.
36. Venneti S, Wiley CA, Kofler J. Imaging microglial activation during neuroinflammation and Alzheimer's disease. J Neuroimmune Pharmacol. 2009;4:227-243.
37. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87:245-313.
38. Rock RB, Peterson PK. Microglia as a pharmacological target in infectious and inflammatory diseases of the brain. J Neuroimmune Pharmacol. 2006;1:117-126.
39. Rae C, Bartlett DJ, Yang Q, etal. Dynamic changes in brain bioenergetics during obstructive sleep apnea. J Cereb lood Flow Metab. 2009;29: 1421-1428.
40. Macey PM, Henderson LA, Macey KE, etal. Brain morphology associated with obstructive sleep apnea. Am J Respir Crit Care Med. 2002;166:1382-1387.
41. Dempsey JA, Veasey SC, Morgan BJ, O'Donnell CP. Pathophysiology of sleep apnea. Physiol Rev. 2010;90:47-112.
42. Jackson ML, Howard ME, Barnes M. Cognition and daytime functioning in sleep-related breathing disorders. Prog Brain Res. 2011; 190:53-68.
43. Grigg-Damberger M, Ralls F. Cognitive dysfunction and obstructive sleep apnea: from cradle to tomb. Curr Opin Pulm Med. 2012;18:580-587.
44. Halbower AC, Degaonkar M, Barker PB, etal. Childhood obstructive sleep apnea associates with neuropsychological deficits and neuronal brain injury. PLoS Med. 2006;3:e301.
45. Kamba M, Inoue Y, Higami S, Suto Y, Ogawa T, Chen W. Cerebral metabolic impairment in patients with obstructive sleep apnoea: an independent association of obstructive sleep apnoea with white matter change. J Neurol Neurosurg Psychiatry. 2001;71:334-339.
46. Petrella JR, Wang L, Krishnan S, etal. Cortical deactivation in mild cognitive impairment: high-field-strength functional MR imaging. Radiology. 2007;245:224-235.
47. Ayalon L, Ancoli-Israel S, Klemfuss Z, Shalauta MD, Drummond SP. Increased brain activation during verbal learning in obstructive sleep apnea. Neuroimage. 2006;31:1817-1825.
48. Castronovo V, Canessa N, Strambi LF, etal. Brain activation changes before and after CPAP treatment in obstructive sleep apnea. Sleep. 2009;32:1161-1172.
49. Cross RL, Kumar R, Macey PM, etal. Neural alterations and depressive symptoms in obstructive sleep apnea patients. Sleep. 2008;31:1103-1109.
50. Hasler G, Fromm S, Alvarez RP, Luckenbaugh DA, Drevets WC, Grillon C. Cerebral blood flow in immediate and sustained anxiety. J Neurosci. 2007;27:6313-6319.
51. Evans KC, Banzett RB, Adams L, McKay L, Frackowiak RS, Corfield DR. BOLD fMRI identifies limbic, paralimbic, and cerebellar activation during air hunger. J Neurophysiol. 2002;88:1500-1511.
52. Macey KE, Macey PM, Woo MA, etal. Inspiratory loading elicits aberrant fMRI signal changes in obstructive sleep apnea. Respir Physiol Neurobiol. 2006;151:44-60.
53. Macey PM, Kumar R, Woo MA, Valladares EM, Yan-Go FL, Harper RM. Brain structural changes in obstructive sleep apnea. Sleep. 2008;31:967-977.
54. Canessa N, Castronovo V, Cappa SF, etal. Obstructive sleep apnea: brain structural changes and neurocognitive function before and after treatment. Am J Respir Crit Care Med. 2011;183:1419-1426.
55. Veasey SC. Piecing together phenotypes of brain injury and dysfunction in obstructive sleep apnea. Front Neurol. 2012;3:139.
56. Xie H, Yung WH. Chronic intermittent hypoxia-induced deficits in synaptic plasticity and neurocognitive functions: a role for brain-derived neurotrophic factor. Acta Pharmacol Sin. 2012;33:5-10.
57. Row BW, Kheirandish L, Neville JJ, Gozal D. Impaired spatial learning and hyperactivity in developing rats exposed to intermittent hypoxia. Pediatr Res. 2002;52:449-453.
58. Zhang JH, Fung SJ, Xi M, Sampogna S, Chase MH. Recurrent apnea induces neuronal apoptosis in the guinea pig forebrain. Exp Neurol. 2009;216:290-294.
59. Numakawa T, Matsumoto T, Numakawa Y, Richards M, Yamawaki S, Kunugi H. Protective action of neurotrophic factors and estrogen against oxidative stress-mediated neurodegeneration. J Toxicol. 2011;2011: 405194.
60. Boutahar N, Reynaud E, Lassabliere F, Borg J. Brain-derived neurotrophic factor inhibits cell cycle reentry but not endoplasmic reticulum stress in cultured neurons following oxidative or excitotoxic stress. J Neurosci Res. 2010;88:2263-2271.
61. Khan SA, Nanduri J, Yuan G, etal. NADPH oxidase 2mediates intermittent hypoxia-induced mitochondrial complex I inhibition: relevance to blood pressure changes in rats. Antioxid Redox Signal. 2011;14: 533-542.
62. Glezer I, Simard AR, Rivest S. Neuroprotective role of the innate immune system by microglia. Neuroscience. 2007;147:867-883.
63. Van Eldik LJ, Thompson WL, Ralay Ranaivo H, Behanna HA, Martin Watterson D. Glia proinflammatory cytokine upregulation as a therapeutic target for neurodegenerative diseases: function-based and target-based discovery approaches. Int Rev Neurobiol. 2007;82: 277-296.
64. Rogers J, Mastroeni D, Leonard B, Joyce J, Grover A. Neuroinflammation in Alzheimer's disease and Parkinson's disease: are microglia pathogenic in either disorder? Int Rev Neurobiol. 2007;82:235-246.
65. Matsuzaki S, Szweda PA, Szweda LI, Humphries KM. Regulated production of free radicals by the mitochondrial electron transport chain: cardiac ischemic preconditioning. Adv Drug Deliv Rev. 2009;61:1324-1331.
66. Shan X, Chi L, Ke Y, etal. Manganese superoxide dismutase protects mouse cortical neurons from chronic intermittent hypoxia-mediated oxidative damage. Neurobiol Dis. 2007;28:206-215.
67. Zhu Y, Fenik P, Zhan G, etal. Selective loss of catecholaminergic wake active neurons in a murine sleep apnea model. J Neurosci. 2007;27:10060-10071.
68. Fung SJ, Xi MC, Zhang JH, etal. Apnea promotes glutamate-induced excitotoxicity in hippocampal neurons. Brain Res. 2007;1179:42-50.
69. Daiber A. Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim Biophys Acta. 2010;1797:897-906.
70. Floyd RA, Hensley K. Oxidative stress in brain aging. Implications for therapeutics of neurodegenerative diseases. Neurobiol Aging. 2002;23:795-807.
71. Brown GC. Mechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase. Biochem Soc Trans. 2007;35:1119-1121.
72. Jander S, Schroeter M, Saleh A. Imaging inflammation in acute brain ischemia. Stroke. 2007;38:642-645.
73. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci. 2007;10:1387-1394.
74. Kim YS, Joh TH. Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease. Exp Mol Med. 2006;38:333-347.
75. Gao HM, Zhou H, Zhang F, Wilson BC, Kam W, Hong JS. HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J Neurosci. 2011;31(3):1081-1092.
76. Zhang D, Hu X, Qian L, et al. Microglial MAC1 receptor and PI3K are essential in mediating β-amyloid peptide-induced microglial activation and subsequent neurotoxicity. J Neuroinflammation. 2011;8(1):3.
77. Wu HM, Tzeng NS, Qian L, et al. Novel neuroprotective mechanisms of memantine: increase in neurotrophic factor release from astroglia and anti-inflammation by preventing microglial activation. Neuropsychopharmacology. 2009;34(10):2344-2357.
78. Block ML, Wu X, Pei Z, etal. Nanometer size diesel exhaust particles are selectively toxic to dopaminergic neurons: the role of microglia, phagocytosis, and NADPH oxidase. FASEB J. 2004;18:1618-1620.