Abstract
ATP-binding cassette (ABC) transporters are widespread among organisms, and 56 genes encode ABC transporters in Drosophila melanogaster (Meigen). Their functions are thought to be divergent. In this study, we examined whether there is a clock-related ABC transporter by performing genome-wide screening using tissue-specific RNA interference. We obtained five candidates when we used tim(UAS)-gal4, which expresses in virtually all clock-related cells. Because their phenotypes were principally reproducible even when we used pdf-gal4, which expresses in a subset of pacemaker neurons only, those transporters were presumed to function in pacemaker neurons. Those five candidates can be categorized into two groups according to the phenotype of the knockdown flies. In one group, CG9281 and CG15410 (E23), the circadian period of knockdown flies was altered. In the other group, CG5944, CG6052, and CG18633, some of the knockdown flies became arrhythmic whereas for others rhythmicity remained intact. Our results suggest that some ABC transporters that have a significant function in the Drosophila circadian system.
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References
Andersen DS, Leevers SJ (2007) The essential Drosophila ATP-binding cassette domain protein, pixie, binds the 40 S ribosome in an ATP-dependent manner and is required for translation initiation. J Biol Chem 282:14752–14760. doi:10.1074/jbc.M701361200
Blau J, Young MW (1999) Cycling vrille expression is required for a functional Drosophila clock. Cell 99:661–671. doi:10.1016/S0092-8674(00)81554-8
Childs S, Ling V (1994) The MDR superfamily of genes and its biological implications. Import Adv Oncol 21–36
Coelho CM, Kolevski B, Bunn C, Walker C, Dahanukar A, Leevers SJ (2005) Growth and cell survival are unevenly impaired in pixie mutant wing discs. Development 132:5411–5424. doi:10.1242/dev.02148
Dean M, Allikmets R (1995) Evolution of ATP-binding cassette transporter genes. Curr Opin Genet Dev 5:779–785. doi:10.1016/0959-437X(95)80011-S
Dean M, Rzhetsky A, Allikmets R (2001) The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11:1156–1166. doi:10.1101/gr.184901
Fernández MP, Chu J, Villella A, Atkinson N, Kay SA, Ceriani MF (2007) Impaired clock output by altered connectivity in the circadian network. Proc Natl Acad Sci USA 104:5650–5655. doi:10.1073/pnas.0608260104
Górska-Andrzejak J, Salvaterra PM, Meinertzhagen IA, Krzeptowski W, Görlich A, Pyza E (2009) Cyclical expression of Na+/K+-ATPase in the visual system of Drosophila melanogaster. J Insect Physiol 55:459–468. doi:10.1016/j.jinsphys.2009.02.003
Hardin PE (2006) Essential and expendable features of the circadian timekeeping mechanism. Curr Opin Neurobiol 16:686–692. doi:10.1016/j.conb.2006.09.001
Helfrich-Förster C (2005) Neurobiology of the fruit fly’s circadian clock. Genes Brain Behav 4:65–76. doi:10.1111/j.1601-183X.2004.00092.x
Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113. doi:10.1146/annurev.cb.08.110192.000435
Hodge JJ, Stanewsky R (2008) Function of the Shaw potassium channel within the Drosophila circadian clock. PLoS One 3:e2274. doi:10.1371/journal.pone.0002274
Hyde SC, Emsley P, Hartshorn MJ, Mimmack MM, Gileadi U, Pearce SR, Gallagher MP, Gill DR, Hubbard RF, Higgins CF (1990) Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature 346:362–365. doi:10.1038/346362a0
Hyun S, Lee Y, Hong ST, Bang S, Paik D, Kang J, Shin J, Lee J, Jeon K, Hwang S, Bae E, Kim J (2005) Drosophila GPCR Han is a receptor for the circadian clock neuropeptide PDF. Neuron 48:267–278. doi:10.1016/j.neuron.2005.08.025
Itoh TQ, Tanimura T, Matsumoto A (2011a) bHLH-ORANGE family genes regulate the expression of E-box clock genes in Drosophila. Appl Entomol Zool 46:391–397. doi:10.1007/s13355-011-0052-z
Itoh TQ, Tanimura T, Matsumoto A (2011b) Membrane-bound transporter controls the circadian transcription of clock genes in Drosophila. Genes Cells 16:1159–1167. doi:10.1111/j.1365-2443.2011.01559.x
Johnsson N, Varshavsky A (1994) Split ubiquitin as a sensor of protein interactions in vivo. Proc Natl Acad Sci USA 91:10340–10344. doi:10.1073/pnas.91.22.10340
Kaneko M, Hall JC (2000) Neuroanatomy of cells expressing clock genes in Drosophila: transgenic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections. J Comp Neurol 422:66–94. doi:10.1002/(SICI)1096-9861(20000619)422:1<66::AID-CNE5>3.0.CO;2-2
Kerr ID (2004) Sequence analysis of twin ATP binding cassette proteins involved in translational control, antibiotic resistance, and ribonuclease L inhibition. Biochem Biophys Res Commun 315:166–173. doi:10.1016/j.bbrc.2004.01.044
Lear BC, Lin JM, Keath JR, McGill JJ, Raman IM, Allada R (2005a) The ion channel narrow abdomen is critical for neural output of the Drosophila circadian pacemaker. Neuron 48:965–976. doi:10.1016/j.neuron.2005.10.030
Lear BC, Merrill CE, Lin JM, Schroeder A, Zhang L, Allada R (2005b) A G protein-coupled receptor, groom-of-PDF, is required for PDF neuron action in circadian behavior. Neuron 48:221–227. doi:10.1016/j.neuron.2005.09.008
Matsumoto A, Ukai-Tadenuma M, Yamada RG, Houl J, Uno KD, Kasukawa T, Dauwalder B, Itoh TQ, Takahashi K, Ueda R, Hardin PE, Tanimura T, Ueda HR (2007) A functional genomics strategy reveals clockwork orange as a transcriptional regulator in the Drosophila circadian clock. Genes Dev 21:1687–1700. doi:10.1101/gad.1552207
Mertens I, Vandingenen A, Johnson EC, Shafer OT, Li W, Trigg JS, De Loof A, Schoofs L, Taghert PH (2005) PDF receptor signaling in Drosophila contributes to both circadian and geotactic behaviors. Neuron 48:213–219. doi:10.1016/j.neuron.2005.09.009
Pili-Floury S, Leulier F, Takahashi K, Saigo K, Samain E, Ueda R, Lemaitre B (2004) In vivo RNA interference analysis reveals an unexpected role for GNBP1 in the defense against gram-positive bacterial infection in Drosophila adults. J Biol Chem 279:12848–12853. doi:10.1074/jbc.M313324200
Renn SC, Park JH, Rosbash M, Hall JC, Taghert PH (1999) A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99:791–802. doi:10.1016/S0092-8674(00)81676-1
Rosbash M (2009) The implications of multiple circadian clock origins. PLoS Biol. 7:e62. doi:10.1371/journal.pbio.1000062
Sharma P, Asztalos Z, Ayyub C, de Bruyne M, Dornan AJ, Gomez-Hernandez A, Keane J, Killeen J, Kramer S, Madhavan M, Roe H, Sherkhane PD, Siddiqi K, Silva E, Carlson JR, Goodwin SF, Heisenberg M, Krishnan K, Kyriacou CP, Partridge L, Riesgo-Escovar J, Rodrigues V, Tully T, O’Kane CJ (2005) Isogenic autosomes to be applied in optimal screening for novel mutants with viable phenotypes in Drosophila melanogaster. J Neurogenet 19:57–85. doi:10.1080/01677060591007155
Sheeba V (2008) The Drosophila melanogaster circadian pacemaker circuit. J Genet 87:485–493. doi:10.1007/s12041-008-0071-x
Sokolove PG, Bushell WN (1978) The Chi square periodogram: its utility for analysis of circadian rhythm. J Theor Biol 72:131–160. doi:10.1016/0022-5193(78)90022-X
Stagljar I, Korostensky C, Johnsson N, te Heesen S (1998) A genetic system based on split-ubiquitin for the analysis of interactions between membrane proteins in vivo. Proc Natl Acad Sci USA 95:5187–5192. doi:10.1073/pnas.95.9.5187
Taghert PH, Shafer OT (2006) Mechanisms of clock output in the Drosophila circadian pacemaker system. J Biol Rhythms 21:445–457. doi:10.1177/0748730406293910
Tomioka K, Matsumoto A (2009) A comparative view of insect circadian clock systems. Cell Mol Life Sci 67:1397–1406. doi:10.1007/s00018-009-0232-y
Ueda HR, Matsumoto A, Kawamura M, Tanimura T, Hashimoto S (2002) Genome-wide transcriptional orchestration of circadian rhythms in Drosophila. J Biol Chem 277:14048–14052. doi:10.1074/jbc.C100765200
Acknowledgments
We thank Justin Blau for the tim(UAS)-gal4 line and Jeffrey C. Hall for the pdf-gal4 line. The UAS strains were obtained from the Genetic Strains Research Center at the National Institute of Genetics and the Vienna Drosophila RNAi Center. We thank Kenji Tomioka, Takahisa Miyatake, and Hideharu Numata for helpful discussion, and Bruce Allen for critical reading of an earlier version of this manuscript. This work is supported in part by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan to A.M.
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Itoh, T.Q., Matsumoto, A. Genome-wide RNA interference screening for the clock-related gene of ATP-binding cassette transporters in Drosophila melanogaster (Diptera: Drosophilidae). Appl Entomol Zool 47, 79–86 (2012). https://doi.org/10.1007/s13355-012-0091-0
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DOI: https://doi.org/10.1007/s13355-012-0091-0