Review on the Impact of Rapid Eye Movement Sleep Deprivation on Synaptic Plasticity and its Molecular Mechanisms

Abstract

Abstract: Insufficient sleep is an increasing serious problem to men and women in fast-paced modern society. Long-term insufficient sleep can lead to cognitive dysfunction. It has been widely recognized that sleep deprivation can affect the learning and memory ability of experimental animals. In this review, we summarized the new developments regarding the impact of rapid eye movement sleep deprivation on synaptic plasticity and its molecular mechanisms in recent years, which we hope can provide some basis for relevant studies of therapeutic targets and treatment drugs in future studies.

Key words: sleep deprivation, memory, synaptic plasticity, NMDA receptor, adenosine, cAMP/PKA/CREB signal path, MAPK/ERK signal path

CLC Number:

R740

LI Wei，LI Ting-ting，QI Sai-qing，ZHANG Gui-rong. Review on the Impact of Rapid Eye Movement Sleep Deprivation on Synaptic Plasticity and its Molecular Mechanisms[J]. Acta Neuropharmacologica, 2013, 3(4): 47-57.

References

[1] 张庆柱. 睡眠与觉醒[M]//张均田，张庆柱，张永祥.神经药理学.第1版.北京：人民卫生出版社，2008年：413-414

[2] National Health Interview Survey, MMWR. Percentage of adults who reported an average of <6 hours of sleep per 24-hour period, by sex and age group ¬—united states, 1985 and 2004[J]. Morbidity and Mortality Weekly Report, 2005, 54(37):933-934.

[3] 沈洁，徐展. 睡眠对记忆巩固的研究进展[C]. 2012 Conference on Psychology and Social Harmony, 2012: 363-366

[4] Shantha M M Rajaratnam, Josephine Arendt. Health in a 24-h society[J]. Lancet, 2001, 358(9286):999–1005

[5] Robert Stickgold, Matthew P Walker. Sleep-dependent memory consolidation and reconsolidation[J]. Sleep Medicine, 2007, 8(4):331-343.

[6] Matthew P Walker. The role of sleep in cognition and emotion [J]. Annals New York Academy of Sci, 2009, 1156(1):168-197

[7] Paul Whitney, John M Hinson. Measurement of cognition in studies of sleep deprivation[J]. Pro Brain Res, 2010, 185:37–48.

[8] Campbell I G, Guinan M J, Horowitz J M. Sleep deprivation impairs long-term potentiation in rat hippocampal slices[J]. J Neurophysiology, 2002, 88(2):1073-1076.

[9] Jaime L Tartar, Christopher P Ward, James T McKenna, et al. Hippocampal synaptic plasticity and spatial learning are impaired in a rat model of sleep fragmentation[J]. Eur J Neurosci, 2006, 23(10):2739-2748.

[10] Christopher J Davis, Joseph W Harding, John W Wright. REM sleep deprivation-induced deficits in the latency-to-peak induction and maintenance of long-term potentiation within the CA1 region of the hippocampus[J]. Brain Res, 2003, 973(2):293-297.

[11] Carmel M McDermott, Mattie N Hardy, N G Bazan, et al. Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus[J]. J Physiol, 2006, 570(Pt 3):553-565.

[12] Pascal Ravassard, Bastien Pachoud, J C Comte, et al. Paradoxical (REM) sleep deprivation causes a large and rapidly reversible decrease in long-term potentiation, synaptic transmission, glutamate receptor protein levels, and ERK/MAPK activation in the dorsal hippocampus[J]. Sleep, 2009, 32(2):227-240.

[13] Ibrahim A Alhaider, Abdulaziz M Aleisa, Trinh T Tran, et al. Sleep deprivation prevents stimulation- induced increases of levels of P-CREB and BDNF: protection by caffeine[J]. Mol Cell Neurosci, 2011, 46(4):742-751.

[14] Carolyn A Marks, Matthew J Wayner. Effects of sleep disruption on rat dentate granule cell LTP in vivo[J]. Brain Res Bull, 2005, 66(2):114-119.

[15] Caroline Kopp, Fabio Longordo, Janet R Nicholson, et al. Insufficient sleep reversibly alters bidirectional synaptic plasticity and NMDA receptor function[J]. J Neurosci, 2006, 26(48):12456-12465.

[16] Christopher G Vecsey, George S Baillie, Devan Jaganath, et al. Sleep deprivation impairs cAMP signalling in the hippocampus[J]. Nature, 2009, 461(7267):1122-1125.

[17] Rodrigo Romcy-Pereira, Constantine Pavlides. Distinct modulatory effects of sleep on the maintenance of hippocampal and medial prefrontal cortex LTP[J]. Eur J Neurosci, 2004, 20(12):3453-3462.

[18] Tadavarty R, Kaan T K, Sastry B R. Long-term depression of excitatory synaptic transmission in rat hippocampal CA1 neurons following sleep-deprivation[J]. Exp Neurol, 2009, 216(1):239-242.

[19] Ramakrishna Tadavarty, Padmesh S Rajput, Jennifer M Wong, et al. Sleep-deprivation induces changes in GABA(B) and mGlu receptor expression and has consequences for synaptic long-term depression[J]. PLoS One, 2011,6(9):e24933.

[20] Vladyslav V Vyazovskiy, Chiara Cirelli, Martha Pfister-Genskow, et al. Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep[J]. Nature Neurosci, 2008, 11(2):200-208.

[21] 张永杰，唐冬梅，徐桂萍. 突触可塑性分子机制的相关研究[J]. 医学综述, 2012，18(8):1141-1143

[22] Stefano Vicini, Wang Jian-feng, Li Jin-hong, et al. Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors[J]. J Neurophysiol, 1998, 79(2):555-566.

[23] Chen Chu, Hardy Mattie, Zhang Jian, et al. Altered NMDA receptor trafficking contributes to sleep deprivation-induced hippocampal synaptic and cognitive impairments[J]. Biochem Biophys Res Commun, 2006, 340(2):435-440.

[24] Bennett M R. The concept of long term potentiation of transmission at synapses [J]Prog Neurobiol, 2000, 60(2):109-137.

[25] Akinori Ishikawa, Yasuyo Kanayama, Hideki Matsumura. Selective rapid eye movement sleep deprivation impairs the maintenance of long-term potentiation in the rat hippocampus[J]. Eur J Neurosci, 2006, 24(1):243-248.

[26] Cedrick Florian, Christopher G Vecsey, Michael M Halassa, et al. Astrocyte-derived adenosine and A1 receptor activity contribute to sleep loss-induced deficits in hippocampal synaptic plasticity and memory in mice[J]. J Neurosci, 2011, 31(19):6956-6962.

[27] Verena Tretter, Raquel Revilla-Sanchez, Catriona Houston, et al. Deficits in spatial memory correlate with modified γ-aminobutyric acid type A receptor tyrosine phosphorylation in the hippocampus[J]. Proc Natl Acad Sci USA, 2009, 106(47):20039-20044.

[28] 王升旭, 李求实. 睡眠剥夺对大鼠脑组织氨基酸类神经递质含量的影响[J]. 第一军医大学学报, 2002, 22(10):888-890.

[29] Mandana Modirrousta, Lynda Mainville, Barbara E Jones. Dynamic changes in GABAA receptors on basal forebrain cholinergic neurons following sleep deprivation and recovery[J]. BMC Neuroscience, 2007,8:15.

[30] Robbert Havekes, Ted Abel, Eddy A Van der Zee. The cholinergic system and neostriatal memory functions[J]. Behav Brain Res, 2011,221(2):412-423.

[31] Serena Deiana, Bettina Platt, Gernot Riedel. The cholinergic system and spatial learning[J]. Behav Brain Res, 2011, 221(2):389-411.

[32] Benedito M A, Camarini R. Rapid eye movement sleep deprivation induces an increase in acetylcholinesterase activity in discrete rat brain regions[J]. Braz J Med Biol Res, 2001, 34(1):103-109.

[33] Rafael J Salín-Pascual, Mauricio Díaz-Muñoz, Lorena Rivera-Valerdi, et al. Decrease in muscarinic M2 receptors from synaptosomes in the pons and hippocampus after REM sleep deprivation in rats[J]. Sleep Research Online, 1998, 1(1):19-23.

[34] Aleisa A M, Alzoubi K H, Alkadhi K A. Post-learning REM sleep deprivation impairs long-term memory: reversal by acute nicotine treatment[J]. Neurosci Lett, 2011, 499(1):28-31.

[35] Aleisa A M, Helal G, Alhaider I A, et al. Acute nicotine treatment prevents REM sleep deprivation-induced learning and memory impairment in rat[J]. Hippocampus, 2011, 21(8):899-909.

[36] Richard Gray, Arun S Rajan, Kristofer A Radcliffe, et al. Hippocampal synaptic transmission enhanced by low concentrations of nicotine[J]. Nature, 1996, 383(6602):713-716.

[37] Alkondon M, Braga M F, Pereira E F, et al. alpha7 nicotinic acetylcholine receptors and modulation of gabaergic synaptic transmission in the hippocampus[J]. Eur J Pharmacol, 2000, 393(1-3):59-67.

[38] Aleisa A M, Alzoubi K H, Gerges N Z. Chronic psychosocial stress-induced impairment of hippocampal LTP: possible role of BDNF[J]. Neurobiol Dis, 2006, 22(3):453-462.

[39] Ruben Guzman-Marin, Ying Zhe, Natalia Suntsova, et al. Suppression of hippocampal plasticity-related gene expression by sleep deprivation in rats[J]. J Physiol, 2006, 575(Pt 3):807-819.

[40] Ibrahim A Alhaider, Abdulaziz M Aleisa, Trinh T Tran, et al. Caffeine prevents sleep loss-induced deficits in long-term potentiation and related signaling molecules in the dentate gyrus[J]. Eur J Neurosci, 2010, 31(8):1368-1376.

[41] Joel H Benington, H Craig Heller. Restoration of brain energy metabolism as the function of sleep[J]. Prog Neurobiol, 1995, 45(4):347-360.

[42] Matthew T Scharf, Nirinjini Naidoo, John E Zimmerman, et al. The energy hypothesis of sleep revisited[J]. Prog Neurobiol, 2008, 86(3):264-280.

[43] Huston J P, Haas H L, Boix F, et al. Extracellular adenosine levels in neostriatum and hippocampus during rest and activity periods of rats[J]. Neuroscience, 1996, 73(1):99- 107.

[44] Porkka-Heiskanen T, Strecker R E, Thakkar M, et al. Adenosine: a mediator of the sleep-inducing effects of prolonged wakefulness[J]. Science, 1997, 276(5316):1265-1268.

[45] Eric A Newman. Glial cell inhibition of neurons by release of ATP[J]. J Neurosci, 2003, 23(5):1659-1666.

[46] Theresa E Bjorness, Christine L Kelly, Tian-shu Gao, et al. Control and function of the homeostatic sleep response by adenosine A1 receptors[J]. J Neurosci, 2009, 29(5):1267-1276.

[47] Libert F, Van Sande J, Lefort A, et al. Cloning and functional characterization of a human A1 adenosine receptor[J]. Biochem Biophys Res, 1992, 187(2):919-926.

[48] Olah M E, Stiles G L. Adenosine receptor subtypes: characterization and therapeutic regulation[J]. Annu Rev Pharmacol Toxicol, 1995, 35:581-606.

[49] Donald G Rainnie, Heinz C Grunze, R W McCarley, et al. Adenosine inhibition of mesopontine cholinergic neurons: implications for EEG arousal[J]. Science, 1994, 263(5147):689-692.

[50] Tarja Porkka-Heiskanen, Anna V Kalinchuk. Adenosine, energy metabolism and sleep homeostasis[J]. Sleep Med Rev, 2011, 15(2):123-135.

[51] 刘少林. 神经胶质细胞对突触可塑性的影响[M]//张均田，张庆柱，张永祥.神经药理学.第1版.北京：人民卫生出版社，2008年：296

[52] Pascual O, Casper K B, Kubera C, et al. Astrocytic purinergic signaling coordinates synaptic networks[J].Science, 2005, 310(5745):113-116.

[53] Pascal Jourdain, Linda H Bergersen, Khaleel Bhaukaurally, et al. Glutamate exocytosis from astrocytes controls synaptic strength[J]. Nat Neurosci, 2007, 10(3):331-339.

[54] Vladimir Parpura, Robert Zorec. Gliotransmission: Exocytotic release from astrocytes[J]. Brain Res Rev, 2010, 63(1-2):83-92.

[55] Suzie J Scales, Yu A Chen, Bryan Y Yoo, et al. SNAREs contribute to the specificity of membrane fusion[J].Neuron, 2000, 26(2):457-464.

[56] Michael M Halassa, Cedrick Florian, Tommaso Fellin, et al. Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss[J].Neuron, 2009, 61(2):213-219.

[57] Thomas V Dunwiddie, Li-hong Diao, William R Proctor. Adenine nucleotides undergo rapid, quantitative conversion to adenosine in the extracellular space in rat hippocampus[J]. J Neurosci, 1997, 17(20):7673-7682.

[58] Robbert Havekes, Ted Abel. Genetic dissection of neural circuits and behavior in Mus musculus[J]. Adv Genetics, 2009, 65:1-38.

[59] Ted Abel, Eric Kandel. Positive and negative regulatory mechanisms that mediate long-term memory storage[J]. Brain Res Rev, 1998, 26(2-3):360-378.

[60] Zhao Z, Huang L, Wu H, et al. Neuropeptide S mitigates spatial memory impairment induced by rapid eye movement sleep deprivation in rats[J]. Neuroreport, 2010, 21(9):623-628.

[61] Miles D Houslay. Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown[J]. Trend Biochemi Sci, 2010, 35(2):91-100.

[62] Kirsty F MacKenzie, Derek A Wallace, Elaine V Hill, et al. Phosphorylation of cAMP-specific PDE4A5 (phosphodiesterase-4A5) by MK2 (MAPKAPK2) attenuates its activation through protein kinase A phosphorylation[J]. Biochem J, 2011, 435(3):755-769.

[63] Elaine Huston, Matthew Beard, Fraser McCallum, et al. The cAMP-specific phosphodiesterase PDE4A5 is cleaved downstream of its SH3 interaction domain by caspase-3. Consequences for altered intracellular distribution[J]. J Biol Chem, 2000, 275(36): 28063-28074.

[64] Graeme B Bolger, Alexander H Peden, Michael R Steele, et al. Attenuation of the activity of the cAMP-specific phosphodiesterase PDE4A5 by interaction with the immunophilin XAP2[J]. J Biol Chem, 2003, 278(35):33351-33363.

[65] Miles D Houslay, Peter Schafer, Kam Y J Zhang. Keynote review: phosphodiesterase-4 as a therapeutic target[J]. Drug Discov Today, 2005, 10(22):1503-1519.

[66] Ribeiro J A, Sebastiao A M. Caffeine and Adenosine[J]. J Alzheimer's Dis, 2010, 20(suppl 1):S3–S15.

[67] Mark N Wu, Karen Ho, Amanda Crocker, et al. The effects of caffeine on sleep in Drosophila require PKA activity, but not the adenosine receptor[J]. J Neurosci, 2009, 29(35): 11029-11037.

[68] 胡亚卓, 吕佩源. MAPK/ERK信号转导通路与学习记忆[J]. 中国神经免疫学和神经病学杂志, 2006, 13(6)：369-372

[69] Soren Impey, Karl Obrietan, Daniel R Storm. Making new connections: role of ERK/MAP kinase signaling in neuronal plasticity[J]. Neuron, 1999, 23(1):11-14.

[70] Mazzucchelli C, Brambilla R. Ras-related and MAPK signalling in neuronal plasticity and memory formation[J]. Cell Mol Life Sci, 2000, 57(4):604-611.

[71] J David Sweatt. Mitogen-activated protein kinases in synaptic plasticity and memory[J]. Curr Opin Neurobiol, 2004, 14(3):311-317.

[72] Carlos B Sindreu, Zachary S Scheiner, Daniel R Storm. Ca2+-stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning[J]. Neuron, 2007, 53(1):79-89.

[73] Tania L Roth, J David Sweatt. Rhythms of memory[J]. Nature Neuroscience, 2008, 11(9):993-994.

[74] Guan Zhi-wei, Peng Xu-wen, Fang Ji-dong. Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus[J]. Brain Research, 2004, 1018(1):38-47.

[75] Chiara Cirelli. How sleep deprivation affects gene expression in the brain: a review of recent findings[J]. J Appl Physiol, 2002, 92(1):394-400.

[76] Chiara Cirelli, Ugo Faraguna, Giulio Tononi. Changes in brain gene expression after long-term sleep deprivation[J]. J Neurochem, 2006, 98(5):1632-1645.

[77] Miroslaw Mackiewicz, John E Zimmerman, Keith R Shockley, et al. What are microarrays teaching us about sleep? [J]. Trends Mol Med, 2009, 15(2):79-87.

[78] Wang Hai-fang, Liu Yu-ting, Marko Briesemann, et al. Computational analysis of gene regulation in animal sleep deprivation[J]. Physiol Genomics, 2010, 42(3):427-436.

[79] Helene Cheval, Carine Chagneau, Gregoire Levasseur, et al. Distinctive features of Egr transcription factor regulation and DNA binding activity in CA1 of the hippocampus in synaptic plasticity and consolidation and reconsolidation of fear memory[J]. Hippocampus, 2012, 22(3):631-642.

[80] Peter Ramm, Carlye T Smith. Rates of cerebral protein synthesis are linked to slow wave sleep in the rat[J]. Physiol Behav, 1990, 48(5):749-753.

[81] Hajime Nakanishi, Sun Yun, Richard K Nakamura, et al. Positive correlations between cerebral protein synthesis rates and deep sleep in Macaca mulatta[J]. Eur J Neurosci, 1997, 9(2):271-279.

[82] Nirinjini Naidoo, William Giang, Raymond J Galante, et al. Sleep deprivation induces the unfolded protein response in mouse cerebral cortex[J]. J Neurochem, 2005, 92(5):1150-1157.

[83] Chiara Cirelli, Christina M Gutierrez, Gutierrez Tononi. Extensive and divergent effects of sleep and wakefulness on brain gene expression[J]. Neuron, 2004, 41(1):35-43.

[84] Laurel Graves, Allan Pack, Ted Abel. Sleep and memory: a molecular perspective[J].Trends Neurosci, 2001, 24(4):237-243.

[85] Roelina Hagewoud, Shamiso N Whitcomb, Heeringa A N, et al. A time for learning and a time for sleep: the effect of sleep deprivation on contextual fear conditioning at different times of the day[J]. Sleep, 2010, 33(10):1315-1322.

[86] Franken P, Dijk D J, Tobler I, et al. Sleep deprivation in rats: effects on EEG power spectra, vigilance states, and cortical temperature[J]. Am J Physiol, 1991, 261(1 Pt 2):R198-R208.

[87] Tang Xiang-dong, Yang Ling-hui, Sanford L D. Individual variation in sleep and motor activity in rats[J]. Behav Brain Res, 2007, 180(1):62-68.

[88] Gina R Poe, Christine M Walsh, Theresa E Bjorness. Both duration and timing of sleep are important to memory consolidation[J]. Sleep, 2010, 33(10):1277-1278.

[89] Antoine R Adamantidis, Zhang Feng, Alexander M Aravanis, et al. Neural substrates of awakening probed with optogenetic control of hypocretin neurons[J]. Nature, 2007, 450(7168):420-424.

[90] Asya Rolls, Daminen Colas, Antoine Adamantidis, et al. Optogenetic disruption of sleep continuity impairs memory consolidation[J]. Procee National Academ Sciences United States of America, 2011, 108(32):13305-13310.

[91] Rorlina Hagewoud, Robbert Havekes, Tiba P A, et al. Coping with sleep deprivation: shifts in regional brain activity and learning strategy[J]. Sleep, 2010, 33(11):1465-1473.