Molecular correlates of sleep and wakefulness in the brain of the white-crowned sparrow

Journal of Neurochemistry

Volumn 105, Issue 1, 2008, Pages 46-62

  Jones, Stephany ^a,b   Pfister Genskow, Martha ^b   Benca, Ruth M ^b   Cirelli, Chiara ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Avian brain; Gene expression; Microarray; Sleep

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BRAIN CORTEX; BRAIN FUNCTION; CELL ADHESION; CHOLESTEROL SYNTHESIS; ENERGY METABOLISM; GENE EXPRESSION; GENETIC TRANSCRIPTION; MICROARRAY ANALYSIS; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN FOLDING; SLEEP DEPRIVATION; SLEEP WAKING CYCLE; SPARROW; TELENCEPHALON; TRANSLATION REGULATION; UNINDEXED SEQUENCE; WAKEFULNESS;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRODUCIBILITY OF RESULTS; SLEEP; SLEEP DEPRIVATION; SPARROWS; TRANSCRIPTION FACTORS; WAKEFULNESS;

AVES; MAMMALIA; RODENTIA; ZONOTRICHIA LEUCOPHRYS; ZONOTRICHIA LEUCOPHRYS GAMBELII;

EID: 41149142331     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.05089.x     Document Type: Article

References (90)

1. Abraham U., Albrecht U., Gwinner E. Brandstatter R. (2002) Spatial and temporal variation of passer Per2 gene expression in two distinct cell groups of the suprachiasmatic hypothalamus in the house sparrow (Passer domesticus). Eur. J. Neurosci. 16, 429 436.
2. Adjaye J., Herwig R., Herrmann D. et al. (2004) Cross-species hybridisation of human and bovine orthologous genes on high density cDNA microarrays. BMC Genomics 5, 83.
3. Akhtar R. A., Reddy A. B., Maywood E. S., Clayton J. D., King V. M., Smith A. G., Gant T. W., Hastings M. H. Kyriacou C. P. (2002) Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr. Biol. 12, 540 550.
4. Amlaner C. Ball N. J. (1994) Avian sleep, in Principles and Practice of Sleep Medicine (Kryger M., Roth T. Dement W., eds pp. 81 94. W.B. Saunders Company, Philadelphia, PA.
5. Aruga J. Mikoshiba K. (2003) Identification and characterization of Slitrk, a novel neuronal transmembrane protein family controlling neurite outgrowth. Mol. Cell. Neurosci. 24, 117 129.
6. Bahr B. A., Staubli U., Xiao P., Chun D., Ji Z. X., Esteban E. T. Lynch G. (1997) Arg-Gly-Asp-Ser-selective adhesion and the stabilization of long-term potentiation: pharmacological studies and the characterization of a candidate matrix receptor. J. Neurosci. 17, 1320 1329.
7. Bar-Or C., Bar-Eyal M., Gal T. Z., Kapulnik Y., Czosnek H. Koltai H. (2006) Derivation of species-specific hybridization-like knowledge out of cross-species hybridization results. BMC Genomics 7, 110.
8. Bar-Or C., Czosnek H. Koltai H. (2007) Cross-species microarray hybridizations: a developing tool for studying species diversity. Trends Genet. 23, 200 207.
9. Barros L. F., Porras O. H. Bittner C. X. (2005) Why glucose transport in the brain matters for PET. Trends Neurosci. 28, 117 119.
10. Bernard-Trifilo J. A., Kramar E. A., Torp R., Lin C. Y., Pineda E. A., Lynch G. Gall C. M. (2005) Integrin signaling cascades are operational in adult hippocampal synapses and modulate NMDA receptor physiology. J. Neurochem. 93, 834 849.
11. Brown T. C., Tran I. C., Backos D. S. Esteban J. A. (2005) NMDA receptor-dependent activation of the small GTPase Rab5 drives the removal of synaptic AMPA receptors during hippocampal LTD. Neuron 45, 81 94.
12. Calabrese B. Halpain S. (2005) Essential role for the PKC target MARCKS in maintaining dendritic spine morphology. Neuron 48, 77 90.
13. Campbell S. S. Tobler I. (1984) Animal sleep: a review of sleep duration across phylogeny. Neurosci. Biobehav. Rev. 8, 269 300.
14. Chalmers A. D., Goldstone K., Smith J. C., Gilchrist M., Amaya E. Papalopulu N. (2005) A Xenopus tropicalis oligonucleotide microarray works across species using RNA from Xenopus laevis. Mech. Dev. 122, 355 363.
15. Chavis P. Westbrook G. (2001) Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 411, 317 321.
16. Chong N. W., Chaurasia S. S., Haque R., Klein D. C. Iuvone P. M. (2003) Temporal-spatial characterization of chicken clock genes: circadian expression in retina, pineal gland, and peripheral tissues. J. Neurochem. 85, 851 860.
17. Churchill G. A. (2002) Fundamentals of experimental design for cDNA microarrays. Nat. Genet. 32 (Suppl. 490 495.
18. Cirelli C. Tononi G. (2000a) Gene expression in the brain across the sleep-waking cycle. Brain Res. 885, 303 321.
19. Cirelli C. Tononi G. (2000b) Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system [in process citation]. J. Neurosci. 20, 9187 9194.
20. Cirelli C., Gutierrez C. M. Tononi G. (2004) Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41, 35 43.
21. Cirelli C., LaVaute T. M. Tononi G. (2005) Sleep and wakefulness modulate gene expression in Drosophila. J. Neurochem. 94, 1411 1419.
22. Cirelli C., Faraguna U. Tononi G. (2006) Changes in brain gene expression after long-term sleep deprivation. J. Neurochem. 98, 1632 1645.
23. D'Almeida V., Lobo L. L., Hipolide D. C., de Oliveira A. C., Nobrega J. N. Tufik S. (1998) Sleep deprivation induces brain region-specific decreases in glutathione levels. Neuroreport 9, 2853 2856.
24. Dai Y., Taru H., Deken S. L., Grill B., Ackley B., Nonet M. L. Jin Y. (2006) SYD-2 Liprin-alpha organizes presynaptic active zone formation through ELKS. Nat. Neurosci. 9, 1479 1487.
25. Dave A. S. Margoliash D. (2000) Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290, 812 816.
26. Deregnaucourt S., Mitra P. P., Feher O., Pytte C. Tchernichovski O. (2005) How sleep affects the developmental learning of bird song. Nature 433, 710 716.
27. Drucker-Colin R. R., Spanis C. W., Cotman C. W. McGaugh J. L. (1975) Changes in protein levels in perfusates of freely moving cats: relation to behavioral state. Science 187, 963 965.
28. Duelli R., Staudt R., Grunwald F. Kuschinsky W. (1998) Increase of glucose transporter densities (Glut1 and Glut3) during chronic administration of nicotine in rat brain. Brain Res. 782, 36 42.
29. Durmer J. S. Dinges D. F. (2005) Neurocognitive consequences of sleep deprivation. Semin. Neurol. 25, 117 129.
30. Eroglu C., Brugger B., Wieland F. Sinning I. (2003) Glutamate-binding affinity of Drosophila metabotropic glutamate receptor is modulated by association with lipid rafts. Proc. Natl Acad. Sci. USA 100, 10219 10224.
31. Gopalakrishnan A., Ji L. L. Cirelli C. (2004) Sleep deprivation and cellular responses to oxidative stress. Sleep 27, 27 35.
32. Grigoryev D. N., Ma S. F., Simon B. A., Irizarry R. A., Ye S. Q. Garcia J. G. (2005) In vitro identification and in silico utilization of interspecies sequence similarities using GeneChip technology. BMC Genomics 6, 62.
33. Gruenbaum L. M., Gilligan D. M., Picciotto M. R., Marinesco S. Carew T. J. (2003) Identification and characterization of Aplysia adducin, an Aplysia cytoskeletal protein homologous to mammalian adducins: increased phosphorylation at a protein kinase C consensus site during long-term synaptic facilitation. J. Neurosci. 23, 2675 2685.
34. Guan Z., Saraswati S., Adolfsen B. Littleton J. T. (2005) Genome-wide transcriptional changes associated with enhanced activity in the Drosophila nervous system. Neuron 48, 91 107.
35. Guzowski J. F., Timlin J. A., Roysam B., McNaughton B. L., Worley P. F. Barnes C. A. (2005) Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr. Opin. Neurobiol. 15, 599 606.
36. Hairston I. S., Peyron C., Denning D. P., Ruby N. F., Flores J., Sapolsky R. M., Heller H. C. O'Hara B. F. (2004) Sleep deprivation effects on growth factor expression in neonatal rats: a potential role for BDNF in the mediation of delta power. J. Neurophysiol. 91, 1586 1595.
37. Helfer G., Fidler A. E., Vallone D., Foulkes N. S. Brandstaetter R. (2006) Molecular analysis of clock gene expression in the avian brain. Chronobiol. Int. 23, 113 127.
38. Horne J. A. (1985) Sleep function, with particular reference to sleep deprivation. Ann. Clin. Res. 17, 199 208.
39. Huang Z., Shimazu K., Woo N. H., Zang K., Muller U., Lu B. Reichardt L. F. (2006) Distinct roles of the beta 1-class integrins at the developing and the mature hippocampal excitatory synapse. J. Neurosci. 26, 11208 11219.
40. Huber R., Hill S. L., Holladay C., Biesiadecki M., Tononi G. Cirelli C. (2004) Sleep homeostasis in Drosophila melanogaster. Sleep 27, 628 639.
41. Katz S., Irizarry R. A., Lin X., Tripputi M. Porter M. W. (2006) A summarization approach for Affymetrix GeneChip data using a reference training set from a large, biologically diverse database. BMC Bioinformatics 7, 464.
42. Kramar E. A., Lin B., Rex C. S., Gall C. M. Lynch G. (2006) Integrin-driven actin polymerization consolidates long-term potentiation. Proc. Natl Acad. Sci. USA 103, 5579 5584.
43. Leitner S., Voigt C., Metzdorf R. Catchpole C. K. (2005) Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J. Neurobiol. 64, 275 284.
44. Mackiewicz M., Shockley K. R., Romer M. A., Galante R. J., Zimmerman J. E., Naidoo N., Baldwin D. A., Jensen S. T., Churchill G. A. Pack A. I. (2007) Macromolecule biosynthesis - a key function of sleep. Physiol. Genomics In press.
45. Magistretti P. J. (2006) Neuron-glia metabolic coupling and plasticity. J. Exp. Biol. 209, 2304 2311.
46. Malenka R. C. Bear M. F. (2004) LTP and LTD: an embarrassment of riches. Neuron 44, 5 21.
47. Mallick B. N. Gulyani S. (1996) Alterations in synaptosomal calcium concentrations after rapid eye movement sleep deprivation in rats. Neuroscience 75, 729 736.
48. Mauch D. H., Nagler K., Schumacher S., Goritz C., Muller E. C., Otto A. Pfrieger F. W. (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294, 1354 1357.
49. McDonald M. J. Rosbash M. (2001) Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107, 567 578.
50. Mitter D., Reisinger C., Hinz B., Hollmann S., Yelamanchili S. V., Treiber-Held S., Ohm T. G., Herrmann A. Ahnert-Hilger G. (2003) The synaptophysin/synaptobrevin interaction critically depends on the cholesterol content. J. Neurochem. 84, 35 42.
51. Murthy V. N. De Camilli P. (2003) Cell biology of the presynaptic terminal. Annu. Rev. Neurosci. 26, 701 728.
52. Naidoo N., Giang W., Galante R. J. Pack A. I. (2005) Sleep deprivation induces the unfolded protein response in mouse cerebral cortex. J. Neurochem. 92, 1150 1157.
53. Naidoo N., Casiano V., Cater J., Zimmerman J. Pack A. I. (2007) A role for the molecular chaperone protein BiP/GRP78 in Drosophila sleep homeostasis. Sleep 30, 557 565.
54. Nakanishi H., Sun Y., Nakamura R. K. et al. (1997) Positive correlations between cerebral protein synthesis rates and deep sleep in Macaca mulatta. Eur. J. Neurosci. 9, 271 279.
55. Nelson S. E., Duricka D. L., Campbell K., Churchill L. Krueger J. M. (2004) Homer1a and 1bc levels in the rat somatosensory cortex vary with the time of day and sleep loss. Neurosci. Lett. 367, 105 108.
56. Nowrousian M., Ringelberg C., Dunlap J. C., Loros J. J. Kuck U. (2005) Cross-species microarray hybridization to identify developmentally regulated genes in the filamentous fungus Sordaria macrospora. Mol. Genet. Genomics 273, 137 149.
57. Okano T., Yamamoto K., Okano K., Hirota T., Kasahara T., Sasaki M., Takanaka Y. Fukada Y. (2001) Chicken pineal clock genes: implication of BMAL2 as a bidirectional regulator in circadian clock oscillation. Genes Cells 6, 825 836.
58. Petit J. M., Tobler I., Allaman I., Borbely A. A. Magistretti P. J. (2002) Sleep deprivation modulates brain mRNAs encoding genes of glycogen metabolism. Eur. J. Neurosci. 16, 1163 1167.
59. Pfister-Genskow M. T. G. Cirelli C. (2007) Molecular evidence for synaptic potentiation during waking and synaptic downscaling during sleep. Sleep Abstract Suppl. 30, A5.
60. Rabenstein R. L., Addy N. A., Caldarone B. J., Asaka Y., Gruenbaum L. M., Peters L. L., Gilligan D. M., Fitzsimonds R. M. Picciotto M. R. (2005) Impaired synaptic plasticity and learning in mice lacking beta-adducin, an actin-regulating protein. J. Neurosci. 25, 2138 2145.
61. Ramanathan L., Gulyani S., Nienhuis R. Siegel J. M. (2002) Sleep deprivation decreases superoxide dismutase activity in rat hippocampus and brainstem. Neuroreport 13, 1387 1390.
62. Ramm P. Smith C. T. (1990) Rates of cerebral protein synthesis are linked to slow wave sleep in the rat. Physiol. Behav. 48, 749 753.
63. Rattenborg N. Amlaner C. (2002) Phylogeny of sleep, in Sleep Medicine (Lee-Chiong T., Sateia M. Carskadon M., eds pp. 7 22. Hanley & Belfus, Inc., Philadelphia, PA.
64. Rattenborg N. Martinez-Gonzalez D. (2007) Avian slow-wave sleep homeostasis. Sleep Abstract Suppl. 30, A127.
65. Rattenborg N. C., Mandt B. H., Obermeyer W. H., Winsauer P. J., Huber R., Wikelski M. Benca R. M. (2004) Migratory sleeplessness in the white-crowned sparrow (Zonotrichia leucophrys gambelii). PLoS Biol. 2, E212.
66. Reich P., Driver J. K. Karnovsky M. L. (1967) Sleep: effects on incorporation of inorganic phosphate into brain fractions. Science 157, 336 338.
67. Roth II. T. C., Lesku J. A., Amlaner C. J. Lima S. L. (2006) A phylogenetic analysis of the correlates of sleep in birds. J. Sleep Res. 15, 395 402.
68. Schroder M. Kaufman R. J. (2005) The mammalian unfolded protein response. Annu. Rev. Biochem. 74, 739 789.
69. Shah G., Azizian M., Bruch D., Mehta R. Kittur D. (2004) Cross-species comparison of gene expression between human and porcine tissue, using single microarray platform - preliminary results. Clin. Transplant. 18 (Suppl. 12 76 80.
70. Shaw P. J., Cirelli C., Greenspan R. J. Tononi G. (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834 1837.
71. Shaw P. J., Tononi G., Greenspan R. J. Robinson D. F. (2002) Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 417, 287 291.
72. 2+/calmodulin- dependent protein kinase II-mediated actin reorganization. J. Neurosci. 26, 1813 1822.
73. Sooksawate T. Simmonds M. A. (2001) Effects of membrane cholesterol on the sensitivity of the GABA(A) receptor to GABA in acutely dissociated rat hippocampal neurones. Neuropharmacology 40, 178 184.
74. Storch K. F., Lipan O., Leykin I., Viswanathan N., Davis F. C., Wong W. H. Weitz C. J. (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417, 78 83.
75. Taishi P., Sanchez C., Wang Y., Fang J., Harding J. W. Krueger J. M. (2001) Conditions that affect sleep alter the expression of molecules associated with synaptic plasticity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281, R839 R845.
76. Terao A., Steininger T. L., Hyder K., Apte-Deshpande A., Ding J., Rishipathak D., Davis R. W., Heller H. C. Kilduff T. S. (2003) Differential increase in the expression of heat shock protein family members during sleep deprivation and during sleep. Neuroscience 116, 187 200.
77. Terao A., Wisor J. P., Peyron C., Apte-Deshpande A., Wurts S. W., Edgar D. M. Kilduff T. S. (2006) Gene expression in the rat brain during sleep deprivation and recovery sleep: an Affymetrix GeneChip study. Neuroscience 137, 593 605.
78. Tobler I. (2005) Phylogeny of sleep regulation, in Principles and practice of sleep medicine, 4th edn (Kryger M., Roth T. Dement W., eds), pp. 72 81. W.B. Saunders Company, Philadelphia, PA.
79. Tobler I. Borbély A. A. (1988) Sleep and EEG spectra in the pigeon (Columba livia) under baseline conditions and after sleep deprivation. J. Comp. Physiol. 163, 729 738.
80. Tononi G. Cirelli C. (2006) Sleep function and synaptic homeostasis. Sleep Med. Rev. 10, 49 62.
81. Ueda H. R., Matsumoto A., Kawamura M., Iino M., Tanimura T. Hashimoto S. (2002) Genome-wide transcriptional orchestration of circadian rhythms in Drosophila. J. Biol. Chem. 277, 14048 14052.
82. Velho T. A., Pinaud R., Rodrigues P. V. Mello C. V. (2005) Co-induction of activity-dependent genes in songbirds. Eur. J. Neurosci. 22, 1667 1678.
83. Wisor J. P., O'Hara B. F., Terao A., Selby C. P., Kilduff T. S., Sancar A., Edgar D. M. Franken P. (2002) A role for cryptochromes in sleep regulation. BMC Neurosci. 3, 20.
84. Yamamoto K., Okano T. Fukada Y. (2001) Chicken pineal Cry genes: light-dependent up-regulation of cCry1 and cCry2 transcripts. Neurosci. Lett. 313, 13 16.
85. Yang Y. H. Speed T. (2002) Design issues for cDNA microarray experiments. Nat. Rev. Genet. 3, 579 588.
86. Yokota Y. Mori S. (2002) Role of Id family proteins in growth control. J. Cell. Physiol. 190, 21 28.
87. Yoshimura T., Suzuki Y., Makino E., Suzuki T., Kuroiwa A., Matsuda Y., Namikawa T. Ebihara S. (2000) Molecular analysis of avian circadian clock genes. Brain Res. Mol. Brain Res. 78, 207 215.
88. Zerial M. McBride H. (2001) Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107 117.
89. Zhen M. Jin Y. (1999) The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401, 371 375.
90. Zimmerman J. E., Rizzo W., Shockley K. R., Raizen D. M., Naidoo N., Mackiewicz M., Churchill G. A. Pack A. I. (2006) Multiple mechanisms limit the duration of wakefulness in Drosophila brain. Physiol. Genomics 27, 337 350.