Pan-neuronal knockdown of Calcineurin reduces sleep in the fruit fly, Drosophila melanogaster

Journal of Neuroscience

Volumn 31, Issue 37, 2011, Pages 13137-13146

  Tomita, Jun ^a   Mitsuyoshi, Madoka ^a   Ueno, Taro ^a   Aso, Yoshinori ^b   Tanimoto, Hiromu ^b   Nakai, Yasuhiro ^c   Aigaki, Toshiro ^c   Kume, Shoen ^a   Kume, Kazuhiko ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^c TOKYO METROPOLITAN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CALCINEURIN A; PHOSPHOPROTEIN PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AVERSIVE BEHAVIOR; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; ENZYME REGULATION; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; GENE SILENCING; LOSS OF FUNCTION MUTATION; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; OLFACTORY MEMORY; PRIORITY JOURNAL; RNA INTERFERENCE; SLEEP TIME;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CALCINEURIN; DROSOPHILA MELANOGASTER; GENE KNOCKDOWN TECHNIQUES; MEMORY; MOTOR ACTIVITY; NEURONS; OLFACTORY PERCEPTION; PROTEIN SUBUNITS; RNA INTERFERENCE; SLEEP;

EID: 80052939377     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5860-10.2011     Document Type: Article

References (50)

1. Andretic R, van Swinderen B, Greenspan RJ (2005) Dopaminergic modulation of arousal in Drosophila. Curr Biol 15:1165-1175.
2. Aso Y, Siwanowicz I, Bracker L, Ito K, Kitamoto T, Tanimoto H (2010) Specific dopaminergic neurons for the formation of labile aversive memory. Curr Biol 20:1445-1451.
3. Bandyopadhyay J, Lee J, Lee J, Lee JI, Yu JR, Jee C, Cho JH, Jung S, Lee MH, Zannoni S, Singson A, Kim DH, Koo HS, Ahnn J (2002) Calcineurin, a calcium/calmodulin-dependent protein phosphatase, is involved in movement, fertility, egg laying, and growth in Caenorhabditis elegans. Mol Biol Cell 13:3281-3293.
4. Brown L, Chen MX, Cohen PT (1994) Identification of a cDNA encoding a Drosophila calcium/calmodulin regulated protein phosphatase, which has its most abundant expression in the early embryo. FEBS Lett 339:124-128.
5. Bushey D, Huber R, Tononi G, Cirelli C (2007) Drosophila Hyperkinetic mutants have reduced sleep and impaired memory. J Neurosci 27:5384-5393.
6. Bushey D, Tononi G, Cirelli C (2009) The Drosophila fragile X mental retardation gene regulates sleep need. J Neurosci 29:1948-1961.
7. Cirelli C (2009) The genetic and molecular regulation of sleep: from fruit flies to humans. Nat Rev Neurosci 10:549-560.
8. Cirelli C, Tononi G (2008) Is sleep essential? PLoS Biol 6:e216.
9. Cirelli C, Gutierrez CM, Tononi G (2004) Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41:35-43.
10. Cirelli C, Bushey D, Hill S, Huber R, Kreber R, Ganetzky B, Tononi G (2005) Reduced sleep in Drosophila Shaker mutants. Nature 434:1087-1092.
11. Crocker A, Shahidullah M, Levitan IB, Sehgal A (2010) Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron 65:670-681.
12. Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neu-rosci 11:114-126.
13. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, Couto A, Marra V, Keleman K, Dickson BJ (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151-156.
14. Donlea JM, Ramanan N, Shaw PJ (2009) Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science 324:105-108.
15. Foltenyi K, Greenspan RJ, Newport JW (2007) Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila. Nat Neurosci 10:1160-1167.
16. Gajewski K, Wang J, Molkentin JD, Chen EH, Olson EN, Schulz RA (2003) Requirement of the calcineurin subunit gene canB2 for indirect flight muscle formation in Drosophila. Proc Natl Acad Sci U SA 100:1040-1045.
17. Gilestro GF, Tononi G, Cirelli C (2009) Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science 324:109-112.
18. Greengard P, Allen PB, Nairn AC (1999) Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 23:435-447.
19. Groth RD, Dunbar RL, Mermelstein PG (2003) Calcineurin regulation of neuronal plasticity. Biochem Biophys Res Commun 311:1159-1171.
20. Han KA, Millar NS, Grotewiel MS, Davis RL (1996) DAMB, a novel dopa-mine receptor expressed specifically in Drosophila mushroom bodies. Neuron 16:1127-1135.
21. Hashimoto Y, Perrino BA, Soderling TR (1990) Identification of an autoin-hibitory domain in calcineurin. J Biol Chem 265:1924-1927.
22. Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, Sehgal A, Pack AI (2000) Rest in Drosophila is a sleep-like state. Neuron 25:129-138.
23. Huber R, Hill SL, Holladay C, Biesiadecki M, Tononi G, Cirelli C (2004) Sleep homeostasis in Drosophila melanogaster. Sleep 27:628-639.
24. Inoue S, Shimoda M, Nishinokubi I, Siomi MC, Okamura M, Nakamura A, Kobayashi S, Ishida N, Siomi H (2002) A role for the Drosophila fragile X-related gene in circadian output. Curr Biol 12:1331-1335.
25. Joiner WJ, Crocker A, White BH, Sehgal A (2006) Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441:757-760.
26. Kilka S, Erdmann F, Migdoll A, Fischer G, Weiwad M (2009) The proline-rich N-terminal sequence of calcineurin Abeta determines substrate binding. Biochemistry 48:1900-1910.
27. Kim YC, Lee HG, Seong CS, Han KA (2003) Expression of a D1 dopamine receptor dDA1/DmDOP1 in the central nervous system of Drosophila melanogaster. Gene Expr Patterns 3:237-245.
28. Kincaid RL, Nightingale MS, Martin BM (1988) Characterization of a cDNA clone encoding the calmodulin-binding domain of mouse brain calcineurin. Proc Natl Acad Sci USA 85:8983-8987.
29. Kume K (2006) A Drosophila dopamine transporter mutant, fumin (fmn), is defective in arousal regulation. Sleep Biol Rhythms 4:263-273.
30. Kume K, Kume S, Park SK, Hirsh J, Jackson FR (2005) Dopamine is a regulator of arousal in the fruit fly. J Neurosci 25:7377-7384.
31. Li X, Yu F, Guo A (2009) Sleep deprivation specifically impairs short-term olfactory memory in Drosophila. Sleep 32:1417-1424.
32. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302:1765-1768.
33. Mendoza-Angeles K, Cabrera A, Hernandez-Falcon J, Ramon F (2007) Slow waves during sleep in crayfish: a time-frequency analysis. J Neurosci Methods 162:264-271.
34. Miyakawa T, Leiter LM, Gerber DJ, Gainetdinov RR, Sotnikova TD, Zeng H, Caron MG, Tonegawa S (2003) Conditional calcineurin knockout mice exhibit multiple abnormal behaviors related to schizophrenia. Proc Natl Acad Sci USA 100:8987-8992.
35. Morales J, Hiesinger PR, Schroeder AJ, Kume K, Verstreken P, Jackson FR, Nelson DL, Hassan BA (2002) Drosophila fragile X protein, DFXR, regulates neuronal morphology and function in the brain. Neuron 34:961-972.
36. Nakai Y, Horiuchi J, Tsuda M, Takeo S, Akahori S, Matsuo T, Kume K, Aigaki T (2011) Calcineurin and its regulator Sra/DSCR1 are essential for sleep in Drosophila. J Neurosci, in press.
37. Pitman JL, McGill JJ, Keegan KP, Allada R (2006) A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441:753-756.
38. Seugnet L, Suzuki Y, Vine L, Gottschalk L, Shaw PJ (2008) D1 receptor activation in the mushroom bodies rescues sleep-loss-induced learning impairments in Drosophila. Curr Biol 18:1110-1117.
39. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834-1837.
40. Sullivan KM, Rubin GM (2002) The Ca2+-calmodulin-activated protein phosphatase calcineurin negatively regulates EGF receptor signaling in Drosophila development. Genetics 161:183-193.
41. Takeo S, Tsuda M, Akahori S, Matsuo T, Aigaki T (2006) The calcineurin regulator Sra plays an essential role in female meiosis in Drosophila. Curr Biol 16:1435-1440.
42. Thimgan MS, Berg JS, Stuart AE (2006) Comparative sequence analysis and tissue localization of members of the SLC6 family of transporters in adult Drosophila melanogaster. J Exp Biol 209:3383-3404.
43. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 157:263-277.
44. Winder DG, Sweatt JD (2001) Roles of serine/threonine phosphatases in hippocampal synaptic plasticity. Nat Rev Neurosci 2:461-474.
45. Wu CL, Xia S, Fu TF, Wang H, Chen YH, Leong D, Chiang AS, Tully T (2007) Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 10:1578-1586.
46. Wu JS, Luo L (2006) A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat Protoc 1:2110-2115.
47. Xia S, Miyashita T, Fu TF, Lin WY, Wu CL, Pyzocha L, Lin IR, Saitoe M, Tully T, Chiang AS (2005) NMDA receptors mediate olfactory learning and memory in Drosophila. Curr Biol 15:603-615.
48. Zeng H, Chattarji S, Barbarosie M, Rondi-Reig L, Philpot BD, Miyakawa T, Bear MF, Tonegawa S (2001) Forebrain-specific calcineurin knockout selectively impairs bidirectional synaptic plasticity and working/episodic-like memory. Cell 107:617-629.
49. Zhang S, Yin Y, Lu H, Guo A (2008) Increased dopaminergic signaling impairs aversive olfactory memory retention in Drosophila. Biochem Bio-phys Res Commun 370:82-86.
50. Zimmerman JE, Naidoo N, Raizen DM, Pack AI (2008) Conservation of sleep: insights from nonmammalian model systems. Trends Neurosci 31:371-376.