Sleep is not just for the brain: Transcriptional responses to sleep in peripheral tissues

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Anafi, Ron C ^a   Pellegrino, Renata ^a,b,c   Shockley, Keith R ^d   Romer, Micah ^a   Tufik, Sergio ^c   Pack, Allan I ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Circadian Rhythms; Heart; Lung; Sleep; Sleep Deprivation; Synchronization; Unfolded Protein Response

Indexed keywords

CARBOHYDRATE; DNA; SULFUR;

ANIMAL CELL; ANIMAL EUTHANASIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE METABOLISM; CELL STRESS; CIRCADIAN RHYTHM; CONTROLLED STUDY; DNA REPAIR; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSCRIPTION; HEART; LUNG PARENCHYMA; MALE; METABOLIC STRESS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN METABOLISM; SLEEP; SLEEP DEPRIVATION; SLEEP TIME; SLEEP WAKING CYCLE; TRANSCRIPTION REGULATION; UNFOLDED PROTEIN RESPONSE; WAKEFULNESS;

ANIMALS; BIOLOGICAL MARKERS; BRAIN; CIRCADIAN CLOCKS; DNA REPAIR; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION PROFILING; LUNG; MALE; MICE; MICE, INBRED C57BL; MYOCARDIUM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; PROTEOLYSIS; SLEEP; SLEEP DEPRIVATION; TRANSCRIPTION, GENETIC; UNFOLDED PROTEIN RESPONSE; WAKEFULNESS;

ANIMALIA; MUS;

EID: 84878231702     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-362     Document Type: Article

References (85)

1. Cirelli C, Tononi G. Is sleep essential?. PLoS Biol 2008, 6:e216. 10.1371/journal.pbio.0060216, 2525690, 18752355.
2. Tononi G, Cirelli C. Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 2003, 62:143-150. 10.1016/j.brainresbull.2003.09.004, 14638388.
3. Benington JH, Heller HC. Restoration of brain energy metabolism as the function of sleep. Prog Neurobiol 1995, 45:347-360. 10.1016/0301-0082(94)00057-O, 7624482.
4. Scharf MT, Naidoo N, Zimmerman JE, Pack AI. The energy hypothesis of sleep revisited. Prog Neurobiol 2008, 86:264-280. 10.1016/j.pneurobio.2008.08.003, 2948963, 18809461.
5. Walker MP, Stickgold R. Sleep, memory, and plasticity. Annu Rev Psychol 2006, 57:139-166. 10.1146/annurev.psych.56.091103.070307, 16318592.
6. 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 2007, 31:441-457. 10.1152/physiolgenomics.00275.2006, 17698924.
7. Hobson JA. Sleep is of the brain, by the brain and for the brain. Nature 2005, 437:1254-1256. 10.1038/nature04283, 16251949.
8. Rechtschaffen A, Gilliland MA, Bergmann BM, Winter JB. Physiological correlates of prolonged sleep deprivation in rats. Science (New York, N.Y.) 1983, 221:182-184.
9. Buxton OM, Cain SW, O'Connor SP, Porter JH, Duffy JF, Wang W, Czeisler CA, Shea SA. Adverse metabolic consequences in humans of prolonged sleep restriction combined with circadian disruption. Sci Transl Med 2012, 4:129ra43. 10.1126/scitranslmed.3003200, 3678519, 22496545.
10. Van Cauter E, Spiegel K, Tasali E, Leproult R. Metabolic consequences of sleep and sleep loss. Sleep Med 2008, 9(Suppl 1):S23-S28.
11. Hanlon EC, Van Cauter E. Quantification of sleep behavior and of its impact on the cross-talk between the brain and peripheral metabolism. Proc Natl Acad Sci USA 2011, 108:15609-15616. 10.1073/pnas.1101338108, 3176603, 21852576.
12. Faraut B, Boudjeltia KZ, Vanhamme L, Kerkhofs M. Immune, inflammatory and cardiovascular consequences of sleep restriction and recovery. Sleep Med Rev 2012, 16:137-149. 10.1016/j.smrv.2011.05.001, 21835655.
13. Lange T, Dimitrov S, Born J. Effects of sleep and circadian rhythm on the human immune system. Ann N Y Acad Sci 2010, 1193:48-59. 10.1111/j.1749-6632.2009.05300.x, 20398008.
14. Mackiewicz M, Zimmerman JE, Shockley KR, Churchill GA, Pack AI. What are microarrays teaching us about sleep?. Trends Mol Med 2009, 15:79-87. 10.1016/j.molmed.2008.12.002, 2942088, 19162550.
15. Cirelli C, Gutierrez CM, Tononi G. Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 2004, 41:35-43. 10.1016/S0896-6273(03)00814-6, 14715133.
16. 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 2007, 104:20090-20095. 10.1073/pnas.0710131104, 2148427, 18077435.
17. 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 2006, 27:337-350. 10.1152/physiolgenomics.00030.2006, 16954408.
18. Cirelli C, LaVaute TM, Tononi G. Sleep and wakefulness modulate gene expression in Drosophila. J Neurochem 2005, 94:1411-1419. 10.1111/j.1471-4159.2005.03291.x, 16001966.
19. Jones S, Pfister-Genskow M, Benca RM, Cirelli C. Molecular correlates of sleep and wakefulness in the brain of the white-crowned sparrow. J Neurochem 2008, 105:46-62. 10.1111/j.1471-4159.2007.05089.x, 18028333.
20. Wang H, Liu Y, Briesemann M, Yan J. Computational analysis of gene regulation in animal sleep deprivation. Physiol Genomics 2010, 42:427-436. 10.1152/physiolgenomics.00205.2009, 20501693.
21. Naidoo N. Cellular stress/the unfolded protein response: relevance to sleep and sleep disorders. Sleep Med Rev 2009, 13:195-204. 10.1016/j.smrv.2009.01.001, 2964262, 19329340.
22. Naidoo N, Giang W, Galante RJ, Pack AI. Sleep deprivation induces the unfolded protein response in mouse cerebral cortex. J Neurochem 2005, 92:1150-1157. 10.1111/j.1471-4159.2004.02952.x, 15715665.
23. Lange T, Perras B, Fehm HL, Born J. Sleep enhances the human antibody response to hepatitis A vaccination. Psychosom Med 2003, 65:831-835. 10.1097/01.PSY.0000091382.61178.F1, 14508028.
24. Nagai M, Hoshide S, Kario K. Sleep duration as a risk factor for cardiovascular disease- a review of the recent literature. Curr Cardiol Rev 2010, 6:54-61. 10.2174/157340310790231635, 2845795, 21286279.
25. Broussard JL, Ehrmann DA, Van Cauter E, Tasali E, Brady MJ. Impaired insulin signaling in human adipocytes after experimental sleep restriction: a randomized, crossover study. Ann Intern Med 2012, 157:549-557. 10.7326/0003-4819-157-8-201210160-00005, 23070488.
26. Spiegel K, Leproult R, Van Cauter E. Impact of sleep debt on metabolic and endocrine function. Lancet 1999, 354:1435-1439. 10.1016/S0140-6736(99)01376-8, 10543671.
27. Dattilo M, Antunes HKM, Medeiros A, Mônico-Neto M, De Souza HS, Lee KS, Tufik S, De Mello MT. Paradoxical sleep deprivation induces muscle atrophy. Muscle Nerve 2012, 45:431-433. 10.1002/mus.22322, 22334180.
28. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
29. Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13. 10.1093/nar/gkn923, 2615629, 19033363.
30. Shaw PJ. Correlates of Sleep and Waking in Drosophila melanogaster. Science 2000, 287:1834-1837. 10.1126/science.287.5459.1834, 10710313.
31. 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 electrophysiological correlates of sleep homeostasis. Sleep 2010, 33:1147-1157. 2938796, 20857860.
32. Cirelli C, Faraguna U, Tononi G. Changes in brain gene expression after long-term sleep deprivation. J Neurochem 2006, 98:1632-1645. 10.1111/j.1471-4159.2006.04058.x, 16923172.
33. Schröder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005, 74:739-789. 10.1146/annurev.biochem.73.011303.074134, 15952902.
34. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007, 8:519-529. 10.1038/nrm2199, 17565364.
35. Sugden MC, Holness MJ. Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am J Physiol Endocrinol Metab 2003, 284:E855-E862.
36. Eaton DL, Bammler TK. Concise review of the glutathione S-transferases and their significance to toxicology. Toxicological sciences: an official journal of the Society of Toxicology 1999, 49:156-164.
37. Meyer Y, Buchanan BB, Vignols F, Reichheld J-P. Thioredoxins and glutaredoxins: unifying elements in redox biology. Annu Rev Genet 2009, 43:335-367. 10.1146/annurev-genet-102108-134201, 19691428.
38. Kimura M, Kapás L, Krueger JM. Oxidized glutathione promotes sleep in rabbits. Brain Res Bull 1998, 45:545-548. 10.1016/S0361-9230(97)00441-3, 9566496.
39. D'Almeida V, Lobo LL, Hipólide DC, De Oliveira AC, Nobrega JN, Tufik S. Sleep deprivation induces brain region-specific decreases in glutathione levels. NeuroReport 1998, 9:2853-2856. 10.1097/00001756-199808240-00031, 9760133.
40. Everson CA, Laatsch CD, Hogg N. Antioxidant defense responses to sleep loss and sleep recovery. Am J Physiol Regul Integr Comp Physiol 2005, 288:R374-R383.
41. Ramanathan L, Hu S, Frautschy SA, Siegel JM. Short-term total sleep deprivation in the rat increases antioxidant responses in multiple brain regions without impairing spontaneous alternation behavior. Behav Brain Res 2010, 207:305-309. 10.1016/j.bbr.2009.10.014, 2815069, 19850085.
42. Rahman I. Oxidative stress, chromatin remodeling and gene transcription in inflammation and chronic lung diseases. J Biochem Mol Biol 2003, 36:95-109. 10.5483/BMBRep.2003.36.1.095, 12542980.
43. Smyth HS, Sleight P, PICKERING GW. Reflex Regulation of Arterial Pressure during Sleep in Man: A Quantitative Method of Assessing Baroreflex Sensitivity. Circ Res 1969, 24:109-121. 10.1161/01.RES.24.1.109, 4303309.
44. Monti A, Medigue C, Nedelcoux H, Escourrou P. Autonomic control of the cardiovascular system during sleep in normal subjects. Eur J Appl Physiol 2002, 87:174-181. 10.1007/s00421-002-0597-1, 12070629.
45. Lecker SH, Solomon V, Mitch WE, Goldberg AL. Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states. J Nutr 1999, 129:227S-237S.
46. Kipreos ET, Pagano M. The F-box protein family. Genome Biol 2000, 1(5):1. REVIEWS3002, 138841, 11178226.
47. Hirsch C, Gauss R, Horn SC, Neuber O, Sommer T. The ubiquitylation machinery of the endoplasmic reticulum. Nature 2009, 458:453-460. 10.1038/nature07962, 19325625.
48. Hall JE. Guyton and Hall Textbook of Medical Physiology: Enhanced E-book 2010, 1120. Philadelphia: Elsevier Health Sciences.
49. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabé-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisén J. Evidence for cardiomyocyte renewal in humans. Science (New York, N.Y.) 2009, 324:98-102.
50. Cesselli D, Jakoniuk I, Barlucchi L, Beltrami AP, Hintze TH, Nadal-Ginard B, Kajstura J, Leri A, Anversa P. Oxidative stress-mediated cardiac cell death is a major determinant of ventricular dysfunction and failure in dog dilated cardiomyopathy. Circ Res 2001, 89:279-286. 10.1161/hh1501.094115, 11485979.
51. Hare JM. Oxidative Stress and Apoptosis in Heart Failure Progression. Circ Res 2001, 89:198-200.
52. Siggens L, Figg N, Bennett M, Foo R. Nutrient deprivation regulates DNA damage repair in cardiomyocytes via loss of the base-excision repair enzyme OGG1. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 2012, 26:2117-2124.
53. Singh KK, Shukla PC, Quan A, Desjardins J-F, Lovren F, Pan Y, Garg V, Gosal S, Garg A, Szmitko PE, Schneider MD, Parker TG, Stanford WL, Leong-Poi H, Teoh H, Al-Omran M, Verma S. BRCA2 protein deficiency exaggerates doxorubicin-induced cardiomyocyte apoptosis and cardiac failure. J Biol Chem 2012, 287:6604-6614. 10.1074/jbc.M111.292664, 3325595, 22157755.
54. Kang T-H, Reardon JT, Kemp M, Sancar A. Circadian oscillation of nucleotide excision repair in mammalian brain. Proc Natl Acad Sci USA 2009, 106:2864-2867. 10.1073/pnas.0812638106, 2629438, 19164551.
55. Kang T-H, Lindsey-Boltz LA, Reardon JT, Sancar A. Circadian control of XPA and excision repair of cisplatin-DNA damage by cryptochrome and HERC2 ubiquitin ligase. Proc Natl Acad Sci USA 2010, 107:4890-4895. 10.1073/pnas.0915085107, 2841896, 20304803.
56. Franken P, Dijk D-J. Circadian clock genes and sleep homeostasis. Eur J Neurosci 2009, 29:1820-1829. 10.1111/j.1460-9568.2009.06723.x, 19473235.
57. Franken P, Dudley CA, Estill SJ, Barakat M, Thomason R, O'Hara BF, McKnight SL. NPAS2 as a transcriptional regulator of non-rapid eye movement sleep: genotype and sex interactions. Proc Natl Acad Sci USA 2006, 103:7118-7123. 10.1073/pnas.0602006103, 1459027, 16636276.
58. Wisor JP, Pasumarthi RK, Gerashchenko D, Thompson CL, Pathak S, Sancar A, Franken P, Lein ES, Kilduff TS. Sleep deprivation effects on circadian clock gene expression in the cerebral cortex parallel electroencephalographic differences among mouse strains. The Journal of neuroscience: the official journal of the Society for Neuroscience 2008, 28:7193-7201.
59. Honma S, Kawamoto T, Takagi Y, Fujimoto K, Sato F, Noshiro M, Kato Y, Honma K. Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature 2002, 419:841-844. 10.1038/nature01123, 12397359.
60. He Y, Jones CR, Fujiki N, Xu Y, Guo B, Holder JL, Rossner MJ, Nishino S, Fu Y-H. The transcriptional repressor DEC2 regulates sleep length in mammals. Science (New York, N.Y.) 2009, 325:866-870.
61. Saini C, Morf J, Stratmann M, Gos P, Schibler U. Simulated body temperature rhythms reveal the phase-shifting behavior and plasticity of mammalian circadian oscillators. Genes Dev 2012, 26:567-580. 10.1101/gad.183251.111, 3315118, 22379191.
62. Buhr ED, Yoo S-H, Takahashi JS. Science (New York, N.Y.) 2010, 330:379-385.
63. Brown SA, Zumbrunn G, Fleury-Olela F, Preitner N, Schibler U. Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Current biology: CB 2002, 12:1574-1583. 10.1016/S0960-9822(02)01145-4, 12372249.
64. Morf J, Rey G, Schneider K, Stratmann M, Fujita J, Naef F, Schibler U. Cold-inducible RNA-binding protein modulates circadian gene expression posttranscriptionally. Science (New York, N.Y.) 2012, 338:379-383.
65. Dardente H, Mendoza J, Fustin J-M, Challet E, Hazlerigg DG. Implication of the F-Box Protein FBXL21 in circadian pacemaker function in mammals. PLoS One 2008, 3:e3530. 10.1371/journal.pone.0003530, 2568807, 18953409.
66. Hirano A, Yumimoto K, Tsunematsu R, Matsumoto M, Oyama M, Kozuka-Hata H, Nakagawa T, Lanjakornsiripan D, Nakayama KI, Fukada Y. FBXL21 Regulates Oscillation of the Circadian Clock through Ubiquitination and Stabilization of Cryptochromes. Cell 2013, 152:1106-1118. 10.1016/j.cell.2013.01.054, 23452856.
67. Yoo S-H, Mohawk JA, Siepka SM, Shan Y, Huh SK, Hong H-K, Kornblum I, Kumar V, Koike N, Xu M, Nussbaum J, Liu X, Chen Z, Chen ZJ, Green CB, Takahashi JS. Competing E3 Ubiquitin Ligases Govern Circadian Periodicity by Degradation of CRY in Nucleus and Cytoplasm. Cell 2013, 152:1091-1105. 10.1016/j.cell.2013.01.055, 23452855.
68. Fonjallaz P, Ossipow V, Wanner G, Schibler U. The two PAR leucine zipper proteins, TEF and DBP, display similar circadian and tissue-specific expression, but have different target promoter preferences. EMBO J 1996, 15:351-362. 449950, 8617210.
69. Mongrain V, La Spada F, Curie T, Franken P. Sleep loss reduces the DNA-binding of BMAL1, CLOCK, and NPAS2 to specific clock genes in the mouse cerebral cortex. PLoS One 2011, 6:e26622. 10.1371/journal.pone.0026622, 3200344, 22039518.
70. Bartlett M. Properties of sufficiency and statistical tests. Proceedings of the Royal Society of London. Series A, Mathematical and Physical Sciences 1937, 160:268-282.
71. NIST/SEMATECH e-Handbook of Statistical Methods [http://www.itl.nist.gov/div898/handbook.
72. Brown MB, Forsythe AB. Robust Tests for the Equality of Variances. J Am Stat Assoc 1974, 69:364-367.
73. Sukumaran S, Jusko WJ, Dubois DC, Almon RR. Light-dark oscillations in the lung transcriptome: implications for lung homeostasis, repair, metabolism, disease, and drug action. J Appl Physiol 2011, 110:1732-1747. Bethesda, Md. : 1985, 10.1152/japplphysiol.00079.2011, 3119131, 21436464.
74. Abraham U, Granada AE, Westermark PO, Heine M, Kramer A, Herzel H. Coupling governs entrainment range of circadian clocks. Mol Syst Biol 2010, 6:438. 3010105, 21119632.
75. Möller-Levet CS, Archer SN, Bucca G, Laing EE, Slak A, Kabiljo R, Lo JCY, Santhi N, Von Schantz M, Smith CP, Dijk D-J. Effects of insufficient sleep on circadian rhythmicity and expression amplitude of the human blood transcriptome. Proceedings of the National Academy of Sciences of the United States of America 2013, 110(12):E1132-41. 10.1073/pnas.1217154110, 3607048, 23440187.
76. Pack AI, Galante RJ, Maislin G, Cater J, Metaxas D, Lu S, Zhang L, Von Smith R, Kay T, Lian J, Svenson K, Peters LL. Novel method for high-throughput phenotyping of sleep in mice. Physiol Genomics 2007, 28:232-238.
77. Carvalho BS, Irizarry RA. A framework for oligonucleotide microarray preprocessing. Bioinformatics (Oxford, England) 2010, 26:2363-7.
78. Carvalho B, Bengtsson H, Speed TP, Irizarry RA. Exploration, normalization, and genotype calls of high-density oligonucleotide SNP array data. Biostatistics (Oxford, England) 2007, 8:485-499.
79. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics (Oxford, England) 4, 249-264.
80. Churchill GA. Using ANOVA to analyze microarray data. Biotechniques 2004, 37(177):173-175.
81. Wu H, Kerr M, Cui X, Churchill G, MAANOVA A Software Package for the Analysis of Spotted cDNA Microarray Experiments. The Analysis of Gene Expression Data 2003, 313-341. New York: Springer-Verlag, Parmigiani G, Garrett E, Irizarry R, Zeger S, MAANOVA.
82. Cui X, Hwang JTG, Qiu J, Blades NJ, Churchill GA. Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics (Oxford, England) 2005, 6:59-75.
83. Yang H, Churchill G. Estimating p-values in small microarray experiments. Bioinformatics (Oxford, England) 2007, 23:38-43.
84. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B 1995, 57(1):289-300.
85. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M. KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 2010, 38:D355-D360. 10.1093/nar/gkp896, 2808910, 19880382.