Genomic analysis of sleep deprivation reveals translational regulation in the hippocampus

Physiological Genomics

Volumn 44, Issue 20, 2012, Pages 981-991

  Abel, Ted ^b   Vecsey, Christopher G ^a   Peixoto, Lucia ^b   Choi, Jennifer H K ^b   Wimmer, Mathieu ^b   Jaganath, Devan ^b   Hernandez, Pepe J ^b   Blackwell, Jennifer ^b   Meda, Karuna ^b   Park, Alan J ^b   Hannenhalli, Sridhar ^c  

^a BRANDEIS UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Bldg 142   (United States)

Author keywords

Hippocampus; Microarray; mTOR; Protein synthesis; Sleep deprivation

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 2; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 40; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN FOS; RAPAMYCIN; TRANSCRIPTION FACTOR FKHR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENOMICS; HIPPOCAMPUS; MALE; MEMORY; MICROARRAY ANALYSIS; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SLEEP DEPRIVATION; UBIQUITINATION; UPREGULATION;

ANIMALS; COMPUTATIONAL BIOLOGY; GENE EXPRESSION REGULATION; GENOMICS; HIPPOCAMPUS; INSULIN; MALE; MEMORY; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN ARRAY ANALYSIS; PROTEIN BIOSYNTHESIS; SIGNAL TRANSDUCTION; SLEEP DEPRIVATION; TIME FACTORS; TOR SERINE-THREONINE KINASES;

EID: 84867730791     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00084.2012     Document Type: Article

References (89)

1. Abel T, Lattal KM. Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol 11: 180-187, 2001.
2. Abraham WC, Williams JM. LTP maintenance and its protein synthesis-dependence. Neurobiol Learn Mem 89: 260-268, 2008.
3. Aldabal L, Bahammam AS. Metabolic, endocrine, and immune consequences of sleep deprivation. Open Resp Med J 5: 31-43, 2011.
4. Banks S, Dinges DF. Behavioral and physiological consequences of sleep restriction. J Clin Sleep Med 3: 519-528, 2007.
5. Basheer R, Brown R, Ramesh V, Begum S, McCarley RW. Sleep deprivation-induced protein changes in basal forebrain: implications for synaptic plasticity. J Neurosci Res 82: 650-658, 2005.
6. Beihl DA, Liese AD, Haffner SM. Sleep duration as a risk factor for incident type 2 diabetes in a multiethnic cohort. Ann Epidemiol 19: 351-357, 2009.
7. Bekinschtein P, Katche C, Slipczuk LN, Igaz LM, Cammarota M, Izquierdo I, Medina JH. mTOR signaling in the hippocampus is necessary for memory formation. Neurobiol Learn Mem 87: 303-307, 2007.
8. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125: 279-284, 2001.
9. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B 57: 289-300, 1995.
10. Bourtchouladze R, Abel T, Berman N, Gordon R, Lapidus K, Kandel ER. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn Mem 5: 365-374, 1998.
11. Chikahisa S, Fujiki N, Kitaoka K, Shimizu N, Sei H. Central AMPK contributes to sleep homeostasis in mice. Neuropharmacology 57: 369-374, 2009.
12. Cirelli C, Gutierrez CM, Tononi G. Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41: 35-43, 2004.
13. Cirelli C, Tononi G. Locus ceruleus control of state-dependent gene expression. J Neurosci 24: 5410-5419, 2004.
14. Conti B, Maier R, Barr AM, Morale MC, Lu X, Sanna PP, Bilbe G, Hoyer D, Bartfai T. Region-specific transcriptional changes following the three antidepressant treatments electro convulsive therapy, sleep deprivation and fluoxetine. Mol Psychiatry 12: 167-189, 2007.
15. Curcio G, Ferrara M, De Gennaro L. Sleep loss, learning capacity and academic performance. Sleep Med Rev 10: 323-337, 2006.
16. Dash PK, Orsi SA, Moore AN. Spatial memory formation and memory-enhancing effect of glucose involves activation of the tuberous sclerosis complex-Mammalian target of rapamycin pathway. J Neurosci 26: 8048-8056, 2006.
17. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3, 2003.
18. Donga E, van Dijk M, van Dijk JG, Biermasz NR, Lammers GJ, van Kralingen KW, Corssmit EP, Romijn JA. A single night of partial sleep deprivation induces insulin resistance in multiple metabolic pathways in healthy subjects. J Clin Endocrinol Metab 95: 2963-2968, 2010.
19. Dresios J, Aschrafi A, Owens GC, Vanderklish PW, Edelman GM, Mauro VP. Cold stress-induced protein Rbm3 binds 60S ribosomal subunits, alters microRNA levels, and enhances global protein synthesis. Proc Natl Acad Sci USA 102: 1865-1870, 2005.
20. Dworak M, McCarley RW, Kim T, Kalinchuk AV, Basheer R. Sleep and brain energy levels: ATP changes during sleep. J Neurosci 30: 9007-9016, 2010.
21. Eckel-Mahan KL, Phan T, Han S, Wang H, Chan GC, Scheiner ZS, Storm DR. Circadian oscillation of hippocampal MAPK activity and cAMP: implications for memory persistence. Nat Neurosci 11: 1074-1082 2008.
22. Ferrara M, Iaria G, De Gennaro L, Guariglia C, Curcio G, Tempesta D, Bertini M. The role of sleep in the consolidation of route learning in humans: a behavioural study. Brain Res Bull 71: 4-9, 2006.
23. Ferrara M, Iaria G, Tempesta D, Curcio G, Moroni F, Marzano C, De Gennaro L, Pacitti C. Sleep to find your way: the role of sleep in the consolidation of memory for navigation in humans. Hippocampus 18: 844-851, 2008.
24. Frank MG, Issa NP, Stryker MP. Sleep enhances plasticity in the developing visual cortex. Neuron 30: 275-287, 2001.
25. Franken P, Chollet D, Tafti M. The homeostatic regulation of sleep need is under genetic control. J Neurosci 21: 2610-2621, 2001.
26. Gangwisch JE. Epidemiological evidence for the links between sleep, circadian rhythms and metabolism. Obes Rev 2: 37-45, 2009.
27. Gangwisch JE, Heymsfield SB, Boden-Albala B, Buijs RM, Kreier F, Pickering TG, Rundle AG, Zammit GK, Malaspina D. Sleep duration as a risk factor for diabetes incidence in a large US sample. Sleep 30: 1667-1673, 2007.
28. Garelick MG, Kennedy BK. TOR on the brain. Exp Gerontol 46: 155-163, 2011.
29. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80, 2004.
30. Graves L, Pack A, Abel T. Sleep and memory: a molecular perspective. Trends Neurosci 24: 237-243, 2001.
31. Graves LA, Heller EA, Pack AI, Abel T. Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning. Learn Mem 10: 168-176, 2003.
32. Guan Z, Peng X, Fang J. Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus. Brain Res 1018: 38-47, 2004.
33. Guzman-Marin R, Ying Z, Suntsova N, Methippara M, Bashir T, Szymusiak R, Gomez-Pinilla F, McGinty D. Suppression of hippocam-pal plasticity-related gene expression by sleep deprivation in rats. J Physiol 575: 807-819, 2006.
34. Hagewoud R, Havekes R, Novati A, Keijser JN, Van der Zee EA, Meerlo P. Sleep deprivation impairs spatial working memory and reduces hippocampal AMPA receptor phosphorylation. J Sleep Res 19: 280-288, 2010.
35. Havekes R, Vecsey CG, Abel T. The impact of sleep deprivation on neuronal and glial signaling pathways important for memory and synaptic plasticity. Cell Signal 24: 1251-1260, 2012.
36. Hernandez PJ, Abel T. A molecular basis for interactions between sleep and memory. Sleep Med Clin 6: 71-84, 2011.
37. Hernandez PJ, Abel T. The role of protein synthesis in memory consolidation: progress amid decades of debate. Neurobiol Learn Mem 89: 293-311, 2008.
38. Hoeffer CA, Klann E. mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci 33: 67-75, 2010.
39. Hoeffer CA, Tang W, Wong H, Santillan A, Patterson RJ, Martinez LA, Tejada-Simon MV, Paylor R, Hamilton SL, Klann E. Removal of FKBP12 enhances mTOR-Raptor interactions, LTP, memory, and perse-verative/repetitive behavior. Neuron 60: 832-845, 2008.
40. Huber R, Deboer T, Tobler I. Effects of sleep deprivation on sleep and sleep EEG in three mouse strains: empirical data and simulations. Brain Res 857: 8-19, 2000.
41. Hublin C, Kaprio J, Partinen M, Koskenvuo M. Insufficient sleep-a population-based study in adults. Sleep 24: 392-400, 2001.
42. Igaz LM, Bekinschtein P, Vianna MM, Izquierdo I, Medina JH. Gene expression during memory formation. Neurotox Res 6: 189-204, 2004.
43. Igaz LM, Vianna MR, Medina JH, Izquierdo I. Two time periods of hippocampal mRNA synthesis are required for memory consolidation of fear-motivated learning. J Neurosci 22: 6781-6789, 2002.
44. Kawamura H, Tomozoe Y, Akagi T, Kamei D, Ochiai M, Yamada M. Identification of the nucleocytoplasmic shuttling sequence of heterogeneous nuclear ribonucleoprotein D-like protein JKTBP and its interaction with mRNA. J Biol Chem 277: 2732-2739, 2002.
45. Kelleher RJ, Govindarajan A, Tonegawa S. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44: 59-73, 2004.
46. Knutson KL, Spiegel K, Penev P, Van Cauter E. The metabolic consequences of sleep deprivation. Sleep Med Rev 11: 163-178, 2007.
47. Knutson KL, Van Cauter E. Associations between sleep loss and increased risk of obesity and diabetes. Ann NY Acad Sci 1129: 287-304, 2008.
48. Kopp C, Longordo F, Nicholson JR, Luthi A. Insufficient sleep revers-ibly alters bidirectional synaptic plasticity and NMDA receptor function. J Neurosci 26: 12456-12465, 2006.
49. Levy S, Hannenhalli S. Identification of transcription factor binding sites in the human genome sequence. Mamm Genome 13: 510-514, 2002.
50. Lopez-Lastra M, Rivas A, Barria MI. Protein synthesis in eukaryotes: the growing biological relevance of cap-independent translation initiation. Biol Res 38: 121-146, 2005.
51. Mackiewicz M, Shockley KR, Romer MA, Galante RJ, Zimmerman JE, Naidoo N, Baldwin DA, Jensen ST, Churchill GA, Pack AI. Macromolecule biosynthesis: a key function of sleep. Physiol Genomics 31: 441-457, 2007.
52. Maret S, Dorsaz S, Gurcel L, Pradervand S, Petit B, Pfister C, Hagenbuchle O, O'Hara BF, Franken P, Tafti M. Homer1a is a core brain molecular correlate of sleep loss. Proc Natl Acad Sci USA 104: 20090-20095, 2007.
53. Martinez-Contreras R, Cloutier P, Shkreta L, Fisette JF, Revil T, Chabot B. hnRNP proteins and splicing control. Adv Exp Med Biol 623: 123-147, 2007.
54. Mazan-Mamczarz K, Gartenhaus RB. Post-transcriptional control of the MCT-1-associated protein DENR/DRP by RNA-binding protein AUF1. Cancer Genom Proteom 4: 233-239, 2007.
55. McDermott CM, LaHoste GJ, Chen C, Musto A, Bazan NG, Magee JC. Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons. J Neurosci 23: 9687-9695, 2003.
56. Meerlo P, de Bruin EA, Strijkstra AM, Daan S. A social conflict increases EEG slow-wave activity during subsequent sleep. Physiol Behav 73: 331-335, 2001.
57. Meerlo P, Turek FW. Effects of social stimuli on sleep in mice: non-rapid-eye-movement (NREM) sleep is promoted by aggressive interaction but not by sexual interaction. Brain Res 907: 84-92, 2001.
58. Mongrain V, Hernandez SA, Pradervand S, Dorsaz S, Curie T, Hagiwara G, Gip P, Heller HC, Franken P. Separating the contribution of glucocorticoids and wakefulness to the molecular and electrophysio-logical correlates of sleep homeostasis. Sleep 33: 1147-1157, 2010.
59. Morris RG, Moser EI, Riedel G, Martin SJ, Sandin J, Day M, O'Carroll C. Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. Philo Trans R Soc London B Biol Sci 358: 773-786, 2003.
60. Naidoo N, Giang W, Galante RJ, Pack AI. Sleep deprivation induces the unfolded protein response in mouse cerebral cortex. J Neurochem 92: 1150-1157, 2005.
61. Nakanishi H, Sun Y, Nakamura RK, Mori K, Ito M, Suda S, Namba H, Storch FI, Dang TP, Mendelson W, Mishkin M, Kennedy C, Gillin JC, Smith CB, Sokoloff L. Positive correlations between cerebral protein synthesis rates and deep sleep in Macaca mulatta. Eur J Neurosci 9: 271-279, 1997.
62. Nikonova EV, Naidoo N, Zhang L, Romer M, Cater JR, Scharf MT, Galante RJ, Pack AI. Changes in components of energy regulation in mouse cortex with increases in wakefulness. Sleep 33: 889-900, 2010.
63. Palchykova S, Winsky-Sommerer R, Meerlo P, Durr R, Tobler I. Sleep deprivation impairs object recognition in mice. Neurobiol Learn Mem 85: 263-271, 2006.
64. Parsons RG, Gafford GM, Helmstetter FJ. Translational control via the mammalian target of rapamycin pathway is critical for the formation and stability of long-term fear memory in amygdala neurons. J Neurosci 26: 12977-12983, 2006.
65. Pawlyk AC, Ferber M, Shah A, Pack AI, Naidoo N. Proteomic analysis of the effects and interactions of sleep deprivation and aging in mouse cerebral cortex. J Neurochem 103: 2301-2313, 2007.
66. Poirrier JE, Guillonneau F, Renaut J, Sergeant K, Luxen A, Maquet P, Leprince P. Proteomic changes in rat hippocampus and adrenals following short-term sleep deprivation. Proteome Sci 6: 14, 2008.
67. Pompeiano M, Cirelli C, Ronca-Testoni S, Tononi G. NGFI-A expression in the rat brain after sleep deprivation. Brain Res Mol Brain Res 46: 143-153, 1997.
68. Ramm P, Smith CT. Rates of cerebral protein synthesis are linked to slow wave sleep in the rat. Physiol Behav 48: 749-753, 1990.
69. Ravassard P, Pachoud B, Comte JC, Mejia-Perez C, Scote-Blachon C, Gay N, Claustrat B, Touret M, Luppi PH, Salin PA. 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. Sleep 32: 227-240, 2009.
70. Ruskin DN, Liu C, Dunn KE, Bazan NG, LaHoste GJ. Sleep deprivation impairs hippocampus-mediated contextual learning but not amygdala-mediated cued learning in rats. Eur J Neurosci 19: 3121-3124, 2004.
71. Schicknick H, Schott BH, Budinger E, Smalla KH, Riedel A, Seiden-becher CI, Scheich H, Gundelfinger ED, Tischmeyer W. Dopaminergic modulation of auditory cortex-dependent memory consolidation through mTOR. Cereb Cortex 18: 2646-2658, 2008.
72. Seibt J, Dumoulin MC, Aton SJ, Coleman T, Watson A, Naidoo N, Frank MG. Protein synthesis during sleep consolidates cortical plasticity in vivo. Curr Biol 22: 676-682, 2012.
73. Smart F, Aschrafi A, Atkins A, Owens GC, Pilotte J, Cunningham BA, Vanderklish PW. Two isoforms of the cold-inducible mRNA-binding protein RBM3 localize to dendrites and promote translation. J Neurochem 101: 1367-1379, 2007.
74. Smith C, Rose GM. Evidence for a paradoxical sleep window for place learning in the Morris water maze. Physiol Behav 59: 93-97, 1996.
75. Stoica L, Zhu PJ, Huang W, Zhou H, Kozma SC, Costa-Mattioli M. Selective pharmacogenetic inhibition of mammalian target of Rapamy-cin complex I (mTORC1) blocks long-term synaptic plasticity and memory storage. Proc Natl Acad Sci USA 108: 3791-3796, 2011.
76. Sweatt JD. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neuro-chem 76: 1-10, 2001.
77. Taishi P, Sanchez C, Wang Y, Fang J, Harding JW, Krueger JM. Conditions that affect sleep alter the expression of molecules associated with synaptic plasticity. Am J Physiol Regul Integr Comp Physiol 281: R839-R845, 2001.
78. Tannu NS, Hemby SE. Methods for proteomics in neuroscience. Prog Brain Res 158: 41-82, 2006.
79. Terao A, Wisor JP, Peyron C, Apte-Deshpande A, Wurts SW, Edgar DM, Kilduff TS. Gene expression in the rat brain during sleep deprivation and recovery sleep: an Affymetrix GeneChip study. Neuroscience 137: 593-605, 2006.
80. Thompson CL, Wisor JP, Lee CK, Pathak SD, Gerashchenko D, Smith KA, Fischer SR, Kuan CL, Sunkin SM, Ng LL, Lau C, Hawrylycz M, Jones AR, Kilduff TS, Lein ES. Molecular and anatomical signatures of sleep deprivation in the mouse brain. Front Neurosci 4: 165, 2010.
81. Van Cauter E, Knutson KL. Sleep and the epidemic of obesity in children and adults. Eur J Endocrinol 159, Suppl 1: S59-S66, 2008.
82. van der Borght K, Ferrari F, Klauke K, Roman V, Havekes R, Sgoifo A, van der Zee EA, Meerlo P. Hippocampal cell proliferation across the day: increase by running wheel activity, but no effect of sleep and wakefulness. Behav Brain Res 167: 36-41, 2006.
83. Vecsey CG, Baillie GS, Jaganath D, Havekes R, Daniels A, Wim-mer M, Huang T, Brown KM, Li XY, Descalzi G, Kim SS, Chen T, Shang YZ, Zhuo M, Houslay MD, Abel T. Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 461: 1122-1125, 2009.
84. Vecsey CG, Hawk JD, Lattal KM, Stein JM, Fabian SA, Attner MA, Cabrera SM, McDonough CB, Brindle PK, Abel T, Wood MA. Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J Neurosci 27: 6128-6140, 2007.
85. Wang H, Liu Y, Briesemann M, Yan J. Computational analysis of gene regulation in animal sleep deprivation. Physiol Genomics 42: 427-436, 2010.
86. Wulff K, Gatti S, Wettstein JG, Foster RG. Sleep and circadian rhythm disruption in psychiatric and neurodegenerative disease. Nat Rev Neurosci 11: 589-599, 2010.
87. Wullschleger S, Loewith R, Hall MN. TOR signaling in growth and metabolism. Cell 124: 471-484, 2006.
88. Youngblood BD, Zhou J, Smagin GN, Ryan DH, Harris RB. Sleep deprivation by the "flower pot" technique and spatial reference memory. Physiol Behav 61: 249-256, 1997.
89. Zimmerman JE, Rizzo W, Shockley KR, Raizen DM, Naidoo N, Mackiewicz M, Churchill GA, Pack AI. Multiple mechanisms limit the duration of wakefulness in Drosophila brain. Physiol Genomics 27: 337-350, 2006.