Neuronal machinery of sleep homeostasis in Drosophila

Neuron

Volumn 81, Issue 4, 2014, Pages 860-872

  Donlea, Jeffrey M ^a   Pimentel, Diogo ^a   Miesenböck, Gero ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR GAL4;

ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; CROSSVEINLESS C GENE; DOPAMINERGIC SYSTEM; FEMALE; GENE; GENE INSERTION; HETEROZYGOSITY; HOMEOSTASIS; LATENT PERIOD; MALE; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; MORPHOLOGY; MUTAGENESIS; NERVE EXCITABILITY; NERVE PROJECTION; NEUROMODULATION; NONHUMAN; OLFACTORY MEMORY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SHORT TERM MEMORY; SIGNAL TRANSDUCTION; SLEEP; SLEEP DEPRIVATION; SLEEP TIME; TRANSPOSON; CIRCADIAN RHYTHM; CV C GENE; DORSAL FAN SHAPED BODY NEURON; DROSOPHILA; GENE EXPRESSION REGULATION; INSOMNIA; MECHANOTRANSDUCTION; MUTATIONAL ANALYSIS; NERVE CELL; NERVE CELL EXCITABILITY; SLEEP PARAMETERS; SLEEP PATTERN; SLEEP PRESSURE;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GTPASE-ACTIVATING PROTEINS; HOMEOSTASIS; MUTATION; NEURONS; SLEEP; SLEEP DEPRIVATION;

EID: 84896738342     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.12.013     Document Type: Article

References (78)

1. Albrecht D.G., Hamilton D.B. Striate cortex of monkey and cat: contrast response function. J.Neurophysiol. 1982, 48:217-237.
2. Allada R., White N.E., So W.V., Hall J.C., Rosbash M. A mutant Drosophila homolog of mammalian Clock disrupts circadian rhythms and transcription of period and timeless. Cell 1998, 93:791-804.
3. Andretic R., van Swinderen B., Greenspan R.J. Dopaminergic modulation of arousal in Drosophila. Curr. Biol. 2005, 15:1165-1175.
4. Åström K.J., Murray R.M. Feedback systems 2008, Princeton University Press, Princeton.
5. Bargiello T.A., Jackson F.R., Young M.W. Restoration of circadian behavioural rhythms by gene transfer in Drosophila. Nature 1984, 312:752-754.
6. Bezzerides V.J., Ramsey I.S., Kotecha S., Greka A., Clapham D.E. Rapid vesicular translocation and insertion of TRP channels. Nat. Cell Biol. 2004, 6:709-720.
7. Billuart P., Winter C.G., Maresh A., Zhao X., Luo L. Regulating axon branch stability: the role of p190 RhoGAP in repressing a retraction signaling pathway. Cell 2001, 107:195-207.
8. Borbély A.A. A two process model of sleep regulation. Hum. Neurobiol. 1982, 1:195-204.
9. Brown R.E., Basheer R., McKenna J.T., Strecker R.E., McCarley R.W. Control of sleep and wakefulness. Physiol. Rev. 2012, 92:1087-1187.
10. Bushey D., Huber R., Tononi G., Cirelli C. Drosophila Hyperkinetic mutants have reduced sleep and impaired memory. J.Neurosci. 2007, 27:5384-5393.
11. Bushey D., Tononi G., Cirelli C. The Drosophila fragile X mental retardation gene regulates sleep need. J.Neurosci. 2009, 29:1948-1961.
12. Cachero T.G., Morielli A.D., Peralta E.G. The small GTP-binding protein RhoA regulates a delayed rectifier potassium channel. Cell 1998, 93:1077-1085.
13. Cao G., Nitabach M.N. Circadian control of membrane excitability in Drosophila melanogaster lateral ventral clock neurons. J.Neurosci. 2008, 28:6493-6501.
14. Cheng M.Y., Bullock C.M., Li C., Lee A.G., Bermak J.C., Belluzzi J., Weaver D.R., Leslie F.M., Zhou Q.-Y. Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 2002, 417:405-410.
15. Cirelli C., Bushey D., Hill S., Huber R., Kreber R., Ganetzky B., Tononi G. Reduced sleep in Drosophila Shaker mutants. Nature 2005, 434:1087-1092.
16. Claridge-Chang A., Roorda R.D., Vrontou E., Sjulson L., Li H., Hirsh J., Miesenböck G. Writing memories with light-addressable reinforcement circuitry. Cell 2009, 139:405-415.
17. Crocker A., Shahidullah M., Levitan I.B., Sehgal A. Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron 2010, 65:670-681.
18. Darlington T.K., Wager-Smith K., Ceriani M.F., Staknis D., Gekakis N., Steeves T.D., Weitz C.J., Takahashi J.S., Kay S.A. Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science 1998, 280:1599-1603.
19. Denholm B., Brown S., Ray R.P., Ruiz-Gómez M., Skaer H., Hombría J.C.-G. crossveinless-c is a RhoGAP required for actin reorganisation during morphogenesis. Development 2005, 132:2389-2400.
20. Donlea J.M., Thimgan M.S., Suzuki Y., Gottschalk L., Shaw P.J. Inducing sleep by remote control facilitates memory consolidation in Drosophila. Science 2011, 332:1571-1576.
21. Donlea J., Leahy A., Thimgan M.S., Suzuki Y., Hughson B.N., Sokolowski M.B., Shaw P.J. Foraging alters resilience/vulnerability to sleep disruption and starvation in Drosophila. Proc. Natl. Acad. Sci. USA 2012, 109:2613-2618.
22. Ewer J., Frisch B., Hamblen-Coyle M.J., Rosbash M., Hall J.C. Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells' influence on circadian behavioral rhythms. J.Neurosci. 1992, 12:3321-3349.
23. Florian C., Vecsey C.G., Halassa M.M., Haydon P.G., Abel T. Astrocyte-derived adenosine and A1 receptor activity contribute to sleep loss-induced deficits in hippocampal synaptic plasticity and memory in mice. J.Neurosci. 2011, 31:6956-6962.
24. Foltenyi K., Greenspan R.J., Newport J.W. Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila. Nat. Neurosci. 2007, 10:1160-1167.
25. Franken P., Chollet D., Tafti M. The homeostatic regulation of sleep need is under genetic control. J.Neurosci. 2001, 21:2610-2621.
26. Ishimoto H., Kitamoto T. The steroid molting hormone Ecdysone regulates sleep in adult Drosophila melanogaster. Genetics 2010, 185:269-281.
27. Joiner W.J., Crocker A., White B.H., Sehgal A. Sleep in Drosophila is regulated by adult mushroom bodies. Nature 2006, 441:757-760.
28. Kapfhamer D., Valladares O., Sun Y., Nolan P.M., Rux J.J., Arnold S.E., Veasey S.C., Bućan M. Mutations in Rab3a alter circadian period and homeostatic response to sleep loss in the mouse. Nat. Genet. 2002, 32:290-295.
29. Koh K., Joiner W.J., Wu M.N., Yue Z., Smith C.J., Sehgal A. Identification of SLEEPLESS, a sleep-promoting factor. Science 2008, 321:372-376.
30. Konopka R.J., Benzer S. Clock mutants of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 1971, 68:2112-2116.
31. Kottler B., Bao H., Zalucki O., Imlach W., Troup M., van Alphen B., Paulk A., Zhang B., van Swinderen B. A sleep/wake circuit controls isoflurane sensitivity in Drosophila. Curr. Biol. 2013, 23:594-598.
32. Kramer A., Yang F.C., Snodgrass P., Li X., Scammell T.E., Davis F.C., Weitz C.J. Regulation of daily locomotor activity and sleep by hypothalamic EGF receptor signaling. Science 2001, 294:2511-2515.
33. Kraves S., Weitz C.J. A role for cardiotrophin-like cytokine in the circadian control of mammalian locomotor activity. Nat. Neurosci. 2006, 9:212-219.
34. Kume K., Kume S., Park S.K., Hirsh J., Jackson F.R. Dopamine is a regulator of arousal in the fruit fly. J.Neurosci. 2005, 25:7377-7384.
35. Lear B.C., Lin J.-M., Keath J.R., McGill J.J., Raman I.M., Allada R. The ion channel narrow abdomen is critical for neural output of the Drosophila circadian pacemaker. Neuron 2005, 48:965-976.
36. Lehman M.N., Silver R., Gladstone W.R., Kahn R.M., Gibson M., Bittman E.L. Circadian rhythmicity restored by neural transplant. Immunocytochemical characterization of the graft and its integration with the host brain. J.Neurosci. 1987, 7:1626-1638.
37. Li W., Pan Y., Wang Z., Gong H., Gong Z., Liu L. Morphological characterization of single fan-shaped body neurons in Drosophila melanogaster. Cell Tissue Res. 2009, 336:509-519.
38. Li X., Yu F., Guo A. Sleep deprivation specifically impairs short-term olfactory memory in Drosophila. Sleep 2009, 32:1417-1424.
39. Liu Q., Liu S., Kodama L., Driscoll M.R., Wu M.N. Two dopaminergic neurons signal to the dorsal fan-shaped body to promote wakefulness in Drosophila. Curr. Biol. 2012, 22:2114-2123.
40. Lu J., Nelson L.E., Franks N., Maze M., Chamberlin N.L., Saper C.B. Role of endogenous sleep-wake and analgesic systems in anesthesia. J.Comp. Neurol. 2008, 508:648-662.
41. McGuire S.E., Le P.T., Osborn A.J., Matsumoto K., Davis R.L. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 2003, 302:1765-1768.
42. Moore J.T., Chen J., Han B., Meng Q.C., Veasey S.C., Beck S.G., Kelz M.B. Direct activation of sleep-promoting VLPO neurons by volatile anesthetics contributes to anesthetic hypnosis. Curr. Biol. 2012, 22:2008-2016.
43. Naka K.I., Rushton W.A. S-potentials from colour units in the retina of fish (Cyprinidae). J.Physiol. 1966, 185:536-555.
44. Naylor E., Bergmann B.M., Krauski K., Zee P.C., Takahashi J.S., Vitaterna M.H., Turek F.W. The circadian clock mutation alters sleep homeostasis in the mouse. J.Neurosci. 2000, 20:8138-8143.
45. Nelson L.E., Guo T.Z., Lu J., Saper C.B., Franks N.P., Maze M. The sedative component of anesthesia is mediated by GABA(A) receptors in an endogenous sleep pathway. Nat. Neurosci. 2002, 5:979-984.
46. Nitabach M.N., Blau J., Holmes T.C. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 2002, 109:485-495.
47. Parisky K.M., Agosto J., Pulver S.R., Shang Y., Kuklin E., Hodge J.J.L., Kang K., Liu X., Garrity P.A., Rosbash M., Griffith L.C. PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 2008, 60:672-682.
48. Pitman J.L., McGill J.J., Keegan K.P., Allada R. A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 2006, 441:753-756.
49. Porkka-Heiskanen T., Strecker R.E., Thakkar M., Bjorkum A.A., Greene R.W., McCarley R.W. Adenosine: a mediator of the sleep-inducing effects of prolonged wakefulness. Science 1997, 276:1265-1268.
50. Ralph M.R., Foster R.G., Davis F.C., Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science 1990, 247:975-978.
51. Reddy P., Zehring W.A., Wheeler D.A., Pirrotta V., Hadfield C., Hall J.C., Rosbash M. Molecular analysis of the period locus in Drosophila melanogaster and identification of a transcript involved in biological rhythms. Cell 1984, 38:701-710.
52. Reick M., Garcia J.A., Dudley C., McKnight S.L. NPAS2: an analog of clock operative in the mammalian forebrain. Science 2001, 293:506-509.
53. Renn S.C.P., Park J.H., Rosbash M., Hall J.C., Taghert P.H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 1999, 99:791-802.
54. Rihel J., Prober D.A., Arvanites A., Lam K., Zimmerman S., Jang S., Haggarty S.J., Kokel D., Rubin L.L., Peterson R.T., Schier A.F. Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 2010, 327:348-351.
55. Rutila J.E., Suri V., Le M., So W.V., Rosbash M., Hall J.C. CYCLE is a second bHLH-PAS clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell 1998, 93:805-814.
56. Sakai T., Kitamoto T. Differential roles of two major brain structures, mushroom bodies and central complex, for Drosophila male courtship behavior. J.Neurobiol. 2006, 66:821-834.
57. Saper C.B., Fuller P.M., Pedersen N.P., Lu J., Scammell T.E. Sleep state switching. Neuron 2010, 68:1023-1042.
58. Sclar G., Maunsell J.H., Lennie P. Coding of image contrast in central visual pathways of the macaque monkey. Vision Res. 1990, 30:1-10.
59. Sehgal A., Price J.L., Man B., Young M.W. Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science 1994, 263:1603-1606.
60. Seugnet L., Suzuki Y., Vine L., Gottschalk L., Shaw P.J. D1 receptor activation in the mushroom bodies rescues sleep-loss-induced learning impairments in Drosophila. Curr. Biol. 2008, 18:1110-1117.
61. Seugnet L., Suzuki Y., Merlin G., Gottschalk L., Duntley S.P., Shaw P.J. Notch signaling modulates sleep homeostasis and learning after sleep deprivation in Drosophila. Curr. Biol. 2011, 21:835-840.
62. Shaw P.J., Tononi G., Greenspan R.J., Robinson D.F. Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 2002, 417:287-291.
63. Sheeba V., Fogle K.J., Kaneko M., Rashid S., Chou Y.-T., Sharma V.K., Holmes T.C. Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr. Biol. 2008, 18:1537-1545.
64. Sherin J.E., Shiromani P.J., McCarley R.W., Saper C.B. Activation of ventrolateral preoptic neurons during sleep. Science 1996, 271:216-219.
65. Siwicki K.K., Eastman C., Petersen G., Rosbash M., Hall J.C. Antibodies to the period gene product of Drosophila reveal diverse tissue distribution and rhythmic changes in the visual system. Neuron 1988, 1:141-150.
66. Steriade M., McCormick D.A., Sejnowski T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993, 262:679-685.
67. Steriade M., Timofeev I., Grenier F. Natural waking and sleep states: a view from inside neocortical neurons. J.Neurophysiol. 2001, 85:1969-1985.
68. Stickgold R., Hobson J.A., Fosse R., Fosse M. Sleep, learning, and dreams: off-line memory reprocessing. Science 2001, 294:1052-1057.
69. Tononi G., Cirelli C. Sleep and synaptic homeostasis: a hypothesis. Brain Res. Bull. 2003, 62:143-150.
70. Ueno T., Tomita J., Tanimoto H., Endo K., Ito K., Kume S., Kume K. Identification of a dopamine pathway that regulates sleep and arousal in Drosophila. Nat. Neurosci. 2012, 15:1516-1523.
71. van Alphen B., Yap M.H.W., Kirszenblat L., Kottler B., van Swinderen B. A dynamic deep sleep stage in Drosophila. J.Neurosci. 2013, 33:6917-6927.
72. Viola A.U., Archer S.N., James L.M., Groeger J.A., Lo J.C.Y., Skene D.J., von Schantz M., Dijk D.-J. PER3 polymorphism predicts sleep structure and waking performance. Curr. Biol. 2007, 17:613-618.
73. Vitaterna M.H., King D.P., Chang A.M., Kornhauser J.M., Lowrey P.L., McDonald J.D., Dove W.F., Pinto L.H., Turek F.W., Takahashi J.S. Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 1994, 264:719-725.
74. Vyazovskiy V.V., Harris K.D. Sleep and the single neuron: the role of global slow oscillations in individual cell rest. Nat. Rev. Neurosci. 2013, 14:443-451.
75. Vyazovskiy V.V., Olcese U., Lazimy Y.M., Faraguna U., Esser S.K., Williams J.C., Cirelli C., Tononi G. Cortical firing and sleep homeostasis. Neuron 2009, 63:865-878.
76. Welsh D.K., Logothetis D.E., Meister M., Reppert S.M. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 1995, 14:697-706.
77. Wilson R.I., Laurent G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J.Neurosci. 2005, 25:9069-9079.
78. Yoo S.-H., Yamazaki S., Lowrey P.L., Shimomura K., Ko C.H., Buhr E.D., Siepka S.M., Hong H.-K., Oh W.J., Yoo O.J., et al. PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl. Acad. Sci. USA 2004, 101:5339-5346.