Critical Role of Endoplasmic Reticulum Stress in Chronic Intermittent Hypoxia-Induced Deficits in Synaptic Plasticity and Long-Term Memory

Antioxidants and Redox Signaling

Volumn 23, Issue 9, 2015, Pages 695-710

  Xu, Lin Hao ^a   Xie, Hui ^a   Shi, Zhi Hui ^a   Du, Li Da ^a   Wing, Yun Kwok ^b   Li, Albert M ^b   Ke, Ya ^a   Yung, Wing Ho ^a  

^a and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

4 PHENYLBUTYRIC ACID; CASPASE 12; CASPASE 3; GLUCOSE REGULATED PROTEIN 78; MALONALDEHYDE; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; TAUROURSODEOXYCHOLIC ACID; 4-PHENYLBUTYRIC ACID; ARYLBUTYRIC ACID DERIVATIVE; TAUROCHENODEOXYCHOLIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CHRONIC INTERMITTENT HYPOXIA; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM STRESS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RECOGNITION; SCHAFFER COLLATERAL PATHWAY; SLEEP DISORDERED BREATHING; SPATIAL MEMORY; UPREGULATION; ANIMAL; C57BL MOUSE; CYTOLOGY; DRUG EFFECTS; HYPOXIA; MEMORY; METABOLISM; MITOCHONDRION; NERVE CELL; SPINE;

ANIMALS; CASPASE 3; ENDOPLASMIC RETICULUM STRESS; HIPPOCAMPUS; HYPOXIA; MALE; MEMORY; MEMORY, LONG-TERM; MICE, INBRED C57BL; MITOCHONDRIA; NEURONAL PLASTICITY; NEURONS; PHENYLBUTYRATES; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; SPINE; TAUROCHENODEOXYCHOLIC ACID;

EID: 84942043077     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2014.6122     Document Type: Article

References (71)

1. Achat-Mendes C, Anderson KL, and Itzhak Y. Impairment in consolidation of learned place preference following dopaminergic neurotoxicity in mice is ameliorated by N-acetylcysteine but not D1 and D2 dopamine receptor agonists. Neuropsychopharmacology 32: 531-541, 2007.
2. Alma do CE, Machado BH, and Leao RM. Chronic intermittent hypoxia depresses afferent neurotransmission in NTS neurons by a reduction in the number of active synapses. J Neurosci 32: 16736-16746, 2012.
3. Beebe DW and Gozal D. Obstructive sleep apnea and the prefrontal cortex: toward a comprehensive model linking nocturnal upper airway obstruction to daytime cognitive and behavioral deficits. J Sleep Res 11: 1-16, 2002.
4. Boyadjieva NI and Sarkar DK. Cyclic adenosine monophosphate and brain-derived neurotrophic factor decreased oxidative stress and apoptosis in developing hypothalamic neuronal cells: role of microglia. Alcohol Clin Exp Res 37: 1370-1379, 2013.
5. Briones TL, Suh E, Jozsa L, Hattar H, Chai J, and Wadowska M. Behaviorally-induced ultrastructural plasticity in the hippocampal region after cerebral ischemia. Brain Res 997: 137-146, 2004.
6. Cabello CM, Lamore SD, Bair WB, 3rd, Davis AL, Azimian SM, and Wondrak GT. DCPIP (2,6-dichlorophenolindophenol) as a genotype-directed redox chemotherapeutic targeting NQO1∗2 breast carcinoma. Free Radic Res 45: 276-292, 2011.
7. Calabrese V, Stella AM, Butterfield DA, and Scapagnini G. Redox regulation in neurodegeneration and longevity: role of the heme oxygenase and HSP70 systems in brainstress tolerance. Antioxid Redox Signal 6: 895-913, 2004.
8. Caldeira MV, Salazar IL, Curcio M, Canzoniero LM, and Duarte CB. Role of the ubiquitin-proteasome system in brain ischemia: friend or foe? Prog Neurobiol 112: 50-69, 2014.
9. Cao SS and Kaufman RJ. Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid Redox Signal 21: 396-413, 2014.
10. Castro-Caldas M, Carvalho AN, Rodrigues E, Henderson CJ, Wolf CR, Rodrigues CM, and Gama MJ. Tauroursodeoxycholic acid prevents MPTP-induced dopaminergic cell death in a mouse model of Parkinson's disease. Mol Neurobiol 46: 475-486, 2012.
11. Chen X, Winters C, Azzam R, Li X, Galbraith JA, Leapman RD, and Reese TS. Organization of the core structure of the postsynaptic density. Proc Natl Acad Sci U S A 105: 4453-4458, 2008.
12. Chou YT, Zhan G, Zhu Y, Fenik P, Panossian L, Li Y, Zhang J, and Veasey S. C/EBP homologous binding protein (CHOP) underlies neural injury in sleep apnea model. Sleep 36: 481-492, 2013.
13. Dayyat EA, Zhang SX, Wang Y, Cheng ZJ, and Gozal D. Exogenous erythropoietin administration attenuates intermittent hypoxia-induced cognitive deficits in a murine model of sleep apnea. BMC Neurosci 13: 77, 2012.
14. Dempsey JA, Veasey SC, Morgan BJ, and O'Connell CP. Pathophysiology of sleep apnea. Physiol Rev 90: 47-112, 2010.
15. Dere E, Huston JP, and De Souza Silva MA. The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci Biobehav Rev 31: 673-704, 2007.
16. Estornell E, Fato R, Pallotti F, and Lenaz G. Assay conditions for the mitochondrial NADH:coenzyme Q oxidoreductase. FEBS Lett 332: 127-131, 1993.
17. Friberg H, Wieloch T, and Castilho RF. Mitochondrial oxidative stress after global brain ischemia in rats. Neurosci Lett 334: 111-114, 2002.
18. Fuentes F, Zimmer D, Atienza M, Schottenfeld J, Penkala I, Bale T, Bence KK, and Arrequi CO. Protein tyrosine phosphatase PTP1B is involved in hippocampal synapse formation and learning. PloS One 7: e41536, 2012.
19. Fung SJ, Xi MC, Zhang JH, Sampogna S, Yamuy J, Morales FR, and Chase MH. Apnea promotes glutamate-induced excitotoxicity in hippocampal neurons. Brain Res 1179: 42-50, 2007.
20. Goldbart A, Row BW, Kheirandish L, Schurr A, Gozal E, Guo SZ, Payne RS, Cheng Z, Brittian KR, and 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 122: 585-590, 2003.
21. Gorman AM, Healy SJ, Jäger R, and Samali A. Stress management at the ER: regulators of ER stress-induced apoptosis. Pharmacol Ther 134: 306-316, 2012.
22. Gozal D. Obstructive sleep apnea in children: implications for the developing central nervous system. Semin Pediatr Neurol 15: 100-106, 2008.
23. Gozal D, Row BW, Kheirandish L, Liu R, Guo SZ, Qiang F, and Brittian KR. Increased susceptibility to intermittent hypoxia in aging rats: changes in proteasomal activity, neuronal apoptosis and spatial function. Neurochem 86: 1545-1552, 2003.
24. Hamada K, Takuwa N, Yokoyama K, and Takuwa Y. Stretch activates Jun N-terminal kinase/stress-activated protein kinase in vascular smooth muscle cells through mechanisms involving autocrine ATP stimulation of purinoceptors. J Biol Chem 273: 6334-6340, 1998.
25. Harris KM, Jensen FE, and Tsao B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 2: 2685-2705, 1992.
26. Henkel AS, Dewey AM, Anderson KA, Olivares S, and Green RM. Reducing endoplasmic reticulum stress does not improve steatohepatitis in mice fed a methionine-and choline-deficient diet. Am J Physiol Gastrointest Liver Physiol 303: 54-59, 2012.
27. Hetz C, Chevet E, and Harding HP. Targeting the unfolded protein response in disease. Nat Rev Drug Discov 12: 703-719, 2013.
28. Higa A and Chevet E. Redox signaling loops in the unfolded protein response. Cell Signal 24: 1548-1555, 2012.
29. Inoue T and Suzuki-Karasaki Y. Mitochondrial superoxide mediates mitochondrial and endoplasmic reticulum dysfunctions in TRAIL-inducedapoptosis in Jurkat cells. Free Radic Biol Med 61C: 273-284, 2013.
30. Kassed CA and Herkenham M. NF-kappaB p50-deficient mice show reduced anxiety-like behaviors in tests of exploratory drive and anxiety. Behav Brain Res 154: 577-584, 2004.
31. Kazlauckas V, Schuh J, Dall'Igna OP, Pereira GS, Bonan CD, and Lara DR. Behavioral and cognitive profile of mice with high and low exploratory phenotypes. Behav Brain Res 162: 272-278, 2005.
32. Kim J, Lee S, Bhattacharjee R, Khalyfa A, Kheirandish-Gozal L, and Gozal D. Leukocyte telomere length and plasma catestatin and myeloid-related protein 8/14 concentrations in children with obstructive sleep apnea. Chest 138: 91-99, 2010.
33. Kim R, Emi M, Tanabe K, and Murakami S. Role of the unfolded protein response in cell death. Apoptosis 11: 5-13, 2006.
34. Kumar GK, Rai V, Sharma SD, Ramakrishnan DP, Peng YJ, Souvannakitti D, and Prabhakar NR. Chronic intermittent hypoxia induces hypoxia-evoked catecholamine efflux in adult rat adrenal medulla via oxidative stress. J Physiol 575: 229-239, 2006.
35. Li RC, Row BW, Gozal E, Kheirandish L, Fan Q, Brittian KR, Guo SZ, Sachleben Je, and Gozal D. Cyclooxygenase 2 and intermittent hypoxia-induced spatial deficits in the rat. Am J Respir Crit Care Med 168: 469-475, 2003.
36. Lumeng JC and Chervin RD. Epidemiology of pediatric obstructive sleep apnea. Proc Am Thorac Soc 5: 242-252, 2008.
37. Malhotra JD and Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 9: 2277-2293, 2007.
38. Mathieu A, Mazza S, De'cary A, Massicotte-Marquez J, Petit D, Gosselin N, Malo J, and Montplaisir J. Effects of obstructive sleep apnea on cognitive function: a comparison between younger and older OSAS patient. Sleep Med 9: 112-120, 2007.
39. Molinaro P, Viggiano D, Nisticò R, Sirabella R, Secondo A, Boscia F, Pannaccione A, Scorziello A, Mehdawy B, Sokolow S, Herchuelz A, Di Renzo GF, and Annunziato L. Na+-Ca2+ exchanger (NCX3) knock-out mice display an impairment in hippocampal long term potentiation and spatial learning and memory. J Neurosci 31: 7312-7321, 2011.
40. Muller C, Bandemer J, Vindis C, Camaré C, Mucher E, Guéraud F, Larroque-Cardoso P, Bernis C, Auge N, Salvayre R, and Negre-Salvayre A. Protein disulfide isomerase modification and inhibition contribute to ER stress and apoptosis induced by oxidized low density lipoproteins. Antioxid Redox Signal 18: 731-742, 2013.
41. Nosyreva E and Kavalali ET. Activity-dependent augmentation of spontaneous neurotransmission during endoplasmic reticulum stress. J Neurosci 30: 7358-7368, 2010.
42. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Görgün CZ, and Hotamisligil GS. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313: 1137-1140, 2006.
43. Pan C, Prentice H, Price AL, and Wu JY. Beneficial effect of taurine on hypoxia- and glutamate induced endoplasmic reticulum stress pathways in primary neuronal culture. Amino Acids 43: 845-855, 2011.
44. Quiroz-Baez R, Ferrera P, Rosendo-Gutiérrez R, Morán J, Bermúdez-Rattoni F, and Arias C. Caspase-12 activation is involved in amyloid-β protein-induced synaptic toxicity. J Alzheimers Dis 26: 467-476, 2011.
45. Ramalho RM, Nunes AF, Dias RB, Amaral JD, Lo AC, D'Hooge R, Sebastião AM, and Rodrigues CM. Tauroursodeoxycholic acid suppresses amyloid β-induce synaptic toxicity in vitro and in APP/PS1 mice. Neurobiol Aging 34: 551-561, 2013.
46. Ricobaraza A, Cuadrado-Tejedor M, Pérez-Mediavilla A, Frechilla D, Del Río J, and García-Osta A. Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer's disease mouse model. Neuropsychopharmacology 34: 1721-1732, 2009.
47. Ron D and Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529, 2007.
48. Roussel BD, Kruppa AJ, Miranda E, Crowther DC, Lomas DA, and Marciniak SJ. Endoplasmic reticulum dysfunction in neurological disease. Lancet Neurol 112: 105-118, 2013.
49. Santos CX, Tanaka LY, Wosniak J, and Laurindo FR. 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 11: 2409-2427, 2009.
50. Sateia MJ. Neuropsychological impairment and quality of life in obstructive sleep apnea. Clin Chest Med 24: 249-259, 2003.
51. Schroder M and Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 74: 739-789, 2005.
52. Sims NR and Anderson MF. Isolation of mitochondria from rat brain using Percoll density gradient centrifugation. Nat Protoc 3: 1228-1239, 2008.
53. Sinha K, Das J, Pal PB, and Sil PC. Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol 87: 1157-1180, 2013.
54. Spitler KM, Matsumoto T, and Webb RC. Suppression of endoplasmic reticulum stress improves endothelium-dependent contractile responses in aorta of the spontaneously hypertensive rat. Am J Physiol Heart Circ Physiol 305: 344-353, 2013.
55. Szegezdi E, Fitzgerald U, and Samali A. Caspase-12 and ER-stress-mediated apoptosis: the story so far. Ann N Y Acad Sci 1010: 186-194, 2003.
56. Toumane A, Durkin T, Marighetto A, Galey D, and Jaffard R. Differential hippocampal and cortical cholinergic activation during the acquisition, retention, reversal and extinction of a spatial discrimination in an 8-arm radial maze by mice. Behav Brain Res 30: 225-234, 1988.
57. Upreti C, Otero R, Partida C, Skinner F, Thakker R, Pacheco LF, Zhou ZY, Maqlakelidze G, Velíšková J,Velíšek L, Romanovicz D, Jones T, Stanton PK, and Garrido-Sanabria ER. Altered neurotransmitter release, vesicle recycling and presynaptic structure in the pilocarpine model of temporal lobe epilepsy. Brain 135: 869-885, 2012.
58. Van der Vlies D, Makkinje M, Jansens A, Braakman I, Verkleij AJ, Wirtz KW, and Post JA. Oxidation of ER resident protein upon oxidative stress: effects of altering cellular redox/antioxidant status and implications for protein maturation. Antioxid Redox Signal 5: 381-387, 2003.
59. van Vliet AR, Verfaillie T, and Agostinis P. New functions of mitochondria associated membranes in cellular signaling. Biochim Biophys Acta 1843: 2253-2262, 2014.
60. Wall AM, Corcoran AE, O'Halloran KD, and O'Connor JJ. Effects of proly-hydroxylase inhibition and chronic intermittent hypoxia on synaptic transmission and plasticity in the rat CA1 and dentate gyrus. Neurobiol Dis 62: 8-17, 2014.
61. Wang S and Kaufman RJ. The impact of unfolded protein response on human disease. J Cell Biol 197: 857-867, 2012.
62. Wang Y, Zhang SX, and Gozal D. Reactive oxygen species and the brain in sleep apnea. Respir Physiol Neurobiol 174: 307-316, 2010.
63. Xie H, Leung KL, Chen L, Chan YS, Ng PC, Fok TF, Wing YK, Ke Ya, Li AM, and Yung WH. Brain-derived neurotrophic factor rescues and prevents chro nic intermittent hypoxia-induced impairment of hippocampal long-term synaptic plasticity. Neurobiol Dis 40: 155-162, 2010.
64. Xie Q, Khaoustov VI, Chung CC, Sohn J, Krishnan B, Lewis DE, and Yoffe B. Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress-induced caspase-12 activation. Hepatology 36: 592-601, 2002.
65. Xu W, Chi L, Row BW, Xu R, Ke Y, Xu B, Gozal D, and 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 126: 313-323, 2004.
66. Yeh CH, Chen TP, Wang YC, Lin YM, and Fang SW. AMP-activated protein kinase activation during cardioplegia-induced hypoxia/reoxygenation injury attenuates cardiomyocytic apoptosis via reduction of endoplasmic reticulum stress. Mediators Inflamm 2010: 130636, 2010.
67. Yong Z, Yan L, Dong Z, Wang X, Su R, and Gong Z. The effect of chronic thienorphine administration on long-term potentiation and synaptic structure in rat hippocampus. Synapse 67: 779-785, 2013.
68. Yoshida H, Okada T, Haze K, Yanagi H, Yura T, Negishi M, and Mori K. ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol Cell Biol 20: 6755-6767, 2000.
69. Yoshida J, Kubo T, and Yamashita T. Inhibition of branching and spine maturation by repulsive guidance molecule in cultured cortical neurons. Biochem Biophys Res Commun 372: 725-729, 2008.
70. Zhan G, Fenik P, Pratico D, and Veasey SC. Inducible nitric oxide synthase in long-term intermittent hypoxia: hypersomnolence and brain injury. Am J Respir Crit Care Med 171: 1414-1420, 2005.
71. Zhu Y, Fenik P, Zhan G, Sanfillipo-Cohn B, Naidoo N, and Veasey SC. Eif-2a protects brainstem motoneurons in a murine model of sleep apnea. J Neurosci 28: 2168-2178, 2008.