Browse > Article
http://dx.doi.org/10.14348/molcells.2014.2371

SIFamide and SIFamide Receptor Define a Novel Neuropeptide Signaling to Promote Sleep in Drosophila  

Park, Sangjin (Department of Biological Sciences, College of Life Science and Bioengineering, Korea Advanced Institute of Science and Technology)
Sonn, Jun Young (Department of Biological Sciences, College of Life Science and Bioengineering, Korea Advanced Institute of Science and Technology)
Oh, Yangkyun (Department of Biological Sciences, College of Life Science and Bioengineering, Korea Advanced Institute of Science and Technology)
Lim, Chunghun (Department of Biological Sciences, School of Life Sciences, Ulsan National Institute of Science and Technology)
Choe, Joonho (Department of Biological Sciences, College of Life Science and Bioengineering, Korea Advanced Institute of Science and Technology)
Publication Information
Molecules and Cells / v.37, no.4, 2014 , pp. 295-301 More about this Journal
Abstract
SIFamide receptor (SIFR) is a Drosophila G protein-coupled receptor for the neuropeptide SIFamide (SIFa). Although the sequence and spatial expression of SIFa are evolutionarily conserved among insect species, the physiological function of SIFa/SIFR signaling remains elusive. Here, we provide genetic evidence that SIFa and SIFR promote sleep in Drosophila. Either genetic ablation of SIFa-expressing neurons in the pars intercerebralis (PI) or pan-neuronal depletion of SIFa expression shortened baseline sleep and reduced sleep-bout length, suggesting that it caused sleep fragmentation. Consistently, RNA interference-mediated knockdown of SIFR expression caused short sleep phenotypes as observed in SIFa-ablated or depleted flies. Using a panel of neuron-specific Gal4 drivers, we further mapped SIFR effects to subsets of PI neurons. Taken together, these results reveal a novel physiological role of the neuropeptide SIFa/SIFR pathway to regulate sleep through sleep-promoting neural circuits in the PI of adult fly brains.
Keywords
Drosophila melanogaster; Pars Intercerebralis; sleep; SIFamide; SIFamide receptor;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Gwack, Y., Sharma, S., Nardone, J., Tanasa, B., Iuga, A., Srikanth, S., Okamura, H., Bolton, D., Feske, S., Hogan, P.G., et al. (2006). A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 441, 646-650.   DOI   ScienceOn
2 Joiner, W.J., Crocker, A., White, B.H., and Sehgal, A. (2006). Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441, 757-760.   DOI   ScienceOn
3 Jorgensen, L.M., Hauser, F., Cazzamali, G., Williamson, M., and Grimmelikhuijzen, C.J. (2006). Molecular identification of the first SIFamide receptor. Biochem. Biophys. Res. Commun. 340, 696-701.   DOI   ScienceOn
4 Kahsai, L., and Winther, A.M. (2011). Chemical neuroanatomy of the Drosophila central complex: distribution of multiple neuropeptides in relation to neurotransmitters. J. Comp. Neurol. 519, 290-315.   DOI   ScienceOn
5 Keene, A.C., Duboue, E.R., McDonald, D.M., Dus, M., Suh, G.S.B., Waddell, S., and Blau, J. (2010). Clock and cycle limit starvationinduced sleep loss in Drosophila. Curr. Biol. 20, 1209-1215.   DOI   ScienceOn
6 Liu, Q.L., Liu, S., Kodama, L., Driscoll, M.R., and Wu, M.N. (2012). Two dopaminergic neurons signal to the dorsal fan-shaped body to promote wakefulness in Drosophila. Curr. Biol. 22, 2114-2123.   DOI   ScienceOn
7 Neely, G.G., Hess, A., Costigan, M., Keene, A.C., Goulas, S., Langeslag, M., Griffin, R.S., Belfer, I., Dai, F., Smith, S.B., et al. (2010). A genome-wide Drosophila screen for heat nociception identifies alpha 2 delta 3 as an evolutionarily conserved pain gene. Cell 143, 628-638.   DOI   ScienceOn
8 Macfadye, U.M., Oswald, I., and Lewis, S.A. (1973). Starvation and human slow-wave sleep. J. Appl. Physiol. 35, 391-394.   DOI
9 Mignot, E. (2008). Why we sleep: the temporal organization of recovery. PLoS Biol. 6, e106.   DOI   ScienceOn
10 Mignot, E., Taheri, S., and Nishino, S. (2002). Sleeping with the hypothalamus: emerging therapeutic targets for sleep disorders. Nat. Neurosci. 5, 1071-1075.   DOI   ScienceOn
11 Paik, D., Jang, Y.G., Lee, Y.E., Lee, Y.N., Yamamoto, R., Gee, H.Y., Yoo, S., Bae, E., Min, K.J., Tatar, M., et al. (2012). Misexpression screen delineates novel genes controlling Drosophila lifespan. Mech. Ageing Dev. 133, 234-245.   DOI   ScienceOn
12 Pitman, J.L., McGill, J.J., Keegan, K.P., and Allada, R. (2006). A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441, 753-756.   DOI   ScienceOn
13 Rechtschaffen, A., and Bergmann, B.M. (2002). Sleep deprivation in the rat: An update of the 1989 paper. Sleep 25, 18-24.   DOI
14 Roeder, T. (1999). Octopamine in invertebrates. Prog. Neurobiol. 59, 533-561.   DOI   ScienceOn
15 Selbie, L.A., and Hill, S.J. (1998). G protein-coupled-receptor crosstalk: the fine-tuning of multiple receptor-signalling pathways. Trends Pharmacol. Sci. 19, 87-93.   DOI   ScienceOn
16 Southall, T.D., Elliott, D.A., and Brand, A.H. (2008). The GAL4 system: a versatile toolkit for gene expression in Drosophila. CSH Protoc. 2008, pdb.top49.
17 Shang, Y.H., Donelson, N.C., Vecsey, C.G., Guo, F., Rosbash, M., and Griffith, L.C. (2013). Short neuropeptide F is a sleep-promoting inhibitory modulator. Neuron 80, 171-183.   DOI   ScienceOn
18 Shaw, P.J., Cirelli, C., Greenspan, R.J., and Tononi, G. (2000). Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834-1837.   DOI   ScienceOn
19 Smith, T.A.D. (2001). Type A gamma-aminobutyric acid (GABA(A)) receptor subunits and benzodiazepine binding: significance to clinical syndromes and their treatment. Br. J. Biomed. Sci. 58, 111-121.
20 Terhzaz, S., Rosay, P., Goodwin, S.F., and Veenstra, J.A. (2007). The neuropeptide SIFamide modulates sexual behavior in Drosophila. Biochem. Biophys. Res. Commun. 352, 305-310.   DOI   ScienceOn
21 Tononi, G., and Cirelli, C. (2014). Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81, 12-34.   DOI   ScienceOn
22 Wisor, J.P., Nishino, S., Sora, I., Uhl, G.H., Mignot, E., and Edgar, D.M. (2001). Dopaminergic role in stimulant-induced wakefulness. J. Neurosci. 21, 1787-1794.
23 Crocker, A., and Sehgal, A. (2008). Octopamine regulates sleep in Drosophila through protein kinase A-dependent mechanisms. J. Neurosci. 28, 9377-9385.   DOI   ScienceOn
24 Cirelli, C. (2009). The genetic and molecular regulation of sleep: from fruit flies to humans. Nat. Rev. Neurosci. 10, 549-560.   DOI   ScienceOn
25 Agrawal, T., Sadaf, S., and Hasan, G. (2013). A genetic RNAi screen for IP3/$Ca^{2+}$ coupled GPCRs in Drosophila identifies the PdfR as a regulator of insect flight. PLoS Genet. 9, e1003849.   DOI
26 Berger, R.J., and Phillips, N.H. (1995). Energy-conservation and sleep. Behav. Brain Res. 69, 65-73.   DOI   ScienceOn
27 Besedovsky, L., Lange, T., and Born, J. (2012). Sleep and immune function. Pflug. Arch. Eur. J. Phy. 463, 121-137.   DOI
28 Broeck, J.V. (2001). Neuropeptides and their precursors in the fruitfly, Drosophila melanogaster. Peptides 22, 241-254.   DOI   ScienceOn
29 Crocker, A., and Sehgal, A. (2010). Genetic analysis of sleep. Genes Dev. 24, 1220-1235.   DOI   ScienceOn
30 Crocker, A., Shahidullah, M., Levitan, I.B., and Sehgal, A. (2010). Identification of a neural circuit that underlies the effects of octopamine on sleep: wake behavior. Neuron 65, 670-681.   DOI   ScienceOn
31 Dworak, M., McCarley, R.W., Kim, T., Kalinchuk, A.V., and Basheer, R. (2010). Sleep and brain energy levels: ATP changes during sleep. J. Neurosci. 30, 9007-9016.   DOI   ScienceOn
32 Foltenyi, K., Greenspan, R.J., and Newport, J.W. (2007). Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila. Nat. Neurosci. 10, 1160-1167.   DOI   ScienceOn
33 Janssen, I., Schoofs, L., Spittaels, K., Neven, H., VandenBroeck, J., Devreese, B., VanBeeumen, J., Shabanowitz, J., Hunt, D.F., and DeLoof, A. (1996). Isolation of NEB-LFamide, a novel myotropic neuropeptide from the grey fleshfly. Mol. Cell. Endocrinol. 117, 157-165.   DOI   ScienceOn
34 Groth, A.C., Fish, M., Nusse, R., and Calos, M.P. (2004). Construction of transgenic Drosophila by using the site-specific integrase from phage phi C31. Genetics 166, 1775-1782.   DOI
35 Verleyen, P., Huybrechts, J., Baggerman, G., Van Lommel, A., De Loof, A., and Schoofs, L. (2004). SIFamide is a highly conserved neuropeptide: a comparative study in different insect species. Biochem. Biophys. Res. Commun. 320, 334-341.   DOI   ScienceOn
36 Hendricks, J.C., Finn, S.M., Panckeri, K.A., Chavkin, J., Williams, J.A., Sehgal, A., and Pack, A.I. (2000). Rest in Drosophila is a sleep-like state. Neuron 25, 129-138.   DOI   ScienceOn
37 Parisky, K.M., Agosto, J., Pulver, S.R., Shang, Y.H., Kuklin, E., Hodge, J.J.L., Kang, K., Liu, X., Garrity, P.A., Rosbash, M., et al. (2009). PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit (vol. 60, pg. 672-682, 2008). Neuron 61, 152.