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Mini-Review

Circadian light-input pathways in Drosophila

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Article: e1102805 | Received 08 Sep 2015, Accepted 25 Sep 2015, Published online: 11 Feb 2016

References

  • Hermann-Luibl C, Helfrich-Förster C. Clock network in Drosophila. Curr Opin Insect Sci 2015; 7:65-70; http://dx.doi.org/10.1016/j.cois.2014.11.003
  • Yoshii T, Rieger D, Helfrich-Förster C. Two clocks in the brain: an update of the morning and evening oscillator model in Drosophila. Prog Brain Res 2012; 199:59-82; PMID:22877659; http://dx.doi.org/10.1016/B978-0-444-59427-3.00027-7
  • Helfrich-Förster C. The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster. Proc Natl Acad Sci USA 1995; 92:612-6; PMID:7831339; http://dx.doi.org/10.1073/pnas.92.2.612
  • Peng Y, Stoleru D, Levine JD, Hall JC, Rosbash M. Drosophila free-running rhythms require intercellular communication. PLoS Biol 2003; 1:32-40; http://dx.doi.org/10.1371/journal.pbio.0000013
  • Lin Y, Stormo GD, Taghert PH. The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J Neurosci 2004; 24:7951-7; PMID:15356209; http://dx.doi.org/10.1523/JNEUROSCI.2370-04.2004
  • Shafer OT, Kim DJ, Dunbar-Yaffe R, Nikolaev VO, Lohse MJ, Taghert PH. Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 2008; 58:223-37; PMID:18439407; http://dx.doi.org/10.1016/j.neuron.2008.02.018
  • Yoshii T, Wülbeck C, Sehadova H, Veleri S, Bichler D, Stanewsky R, Helfrich-Förster C. The neuropeptide pigment-dispersing factor adjusts period and phase of Drosophila's clock. J Neurosci 2009; 29:2597-610; PMID:19244536; http://dx.doi.org/10.1523/JNEUROSCI.5439-08.2009
  • Yao Z, Shafer OT. The Drosophila circadian clock is a variably coupled network of multiple peptidergic units. Science 2014; 343:1516-20; PMID:24675961; http://dx.doi.org/10.1126/science.1251285
  • Renn SC, Park JH, Rosbash M, Hall JC, Taghert PH. 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; PMID:10619432; http://dx.doi.org/10.1016/S0092-8674(00)81676-1
  • Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993; 118:401-15; PMID:8223268
  • Grima B, Chelot E, Xia R, Rouyer F. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 2004; 431:869-73; PMID:15483616; http://dx.doi.org/10.1038/nature02935
  • Stoleru D, Peng Y, Agosto J, Rosbash M. Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 2004; 431:862-8; PMID:15483615; http://dx.doi.org/10.1038/nature02926
  • Rieger D, Shafer OT, Tomioka K, Helfrich-Förster C. Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 2006; 26:2531-43; PMID:16510731; http://dx.doi.org/10.1523/JNEUROSCI.1234-05.2006
  • Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen LO, van der Horst GT, Batschauer A, Ahmad M. The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol 2011; 62:335-64; PMID:21526969; http://dx.doi.org/10.1146/annurev-arplant-042110-103759
  • Stanewsky R, Kaneko M, Emery P, Beretta B, Wager-Smith K, Kay SA, Rosbash M, Hall JC. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 1998; 95:681-92; PMID:9845370; http://dx.doi.org/10.1016/S0092-8674(00)81638-4
  • Emery P, Stanewsky R, Hall JC, Rosbash M. Drosophila cryptochromes: a unique circadian-rhythm photoreceptor. Nature 2000; 404:456-7; PMID:10761904; http://dx.doi.org/10.1038/35006558
  • Helfrich-Förster C, Winter C, Hofbauer A, Hall JC, Stanewsky R. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 2001; 30:249-61; PMID:11343659; http://dx.doi.org/10.1016/S0896-6273(01)00277-X
  • Kistenpfennig C, Hirsh J, Yoshii T, Helfrich-Förster C. Phase-shifting the fruit fly clock without cryptochrome. J Biol Rhythms 2012; 27:117-25; PMID:22476772; http://dx.doi.org/10.1177/0748730411434390
  • Benito J, Houl JH, Roman GW, Hardin PE. The blue-light photoreceptor cryptochrome is expressed in a subset of circadian oscillator neurons in the Drosophila CNS. J Biol Rhythms 2008; 23:296-307; PMID:18663237; http://dx.doi.org/10.1177/0748730408318588
  • Yoshii T, Todo T, Wülbeck C, Stanewsky R, Helfrich-Förster C. Cryptochrome is present in the compound eyes and a subset of Drosophila's clock neurons. J Comp Neurol 2008; 508:952-66; PMID:18399544; http://dx.doi.org/10.1002/cne.21702
  • Koh K, Zheng X, Sehgal A. Jetlag resets the Drosophila circadian clock by promoting light-induced degradation of timeless. Science 2006; 312:1809-12; PMID:16794082; http://dx.doi.org/10.1126/science.1124951
  • Peschel N, Chen KF, Szabo G, Stanewsky R. Light-dependent interactions between the Drosophila circadian clock factors cryptochrome, jetlag, and timeless. Curr Biol 2009; 19:241-7; PMID:19185492; http://dx.doi.org/10.1016/j.cub.2008.12.042
  • Tang CH, Hinteregger E, Shang Y, Rosbash M. Light-mediated TIM degradation within Drosophila pacemaker neurons (s-LNvs) is neither necessary nor sufficient for delay zone phase shifts. Neuron 2010; 66:378-85; PMID:20471351; http://dx.doi.org/10.1016/j.neuron.2010.04.015
  • Lamba P, Bilodeau-Wentworth D, Emery P, Zhang Y. Morning and evening oscillators cooperate to reset circadian behavior in response to light input. Cell Rep 2014; 7:601-8; PMID:24746814; http://dx.doi.org/10.1016/j.celrep.2014.03.044
  • Busza A, Emery-Le M, Rosbash M, Emery P. Roles of the two Drosophila Cryptochrome structural domains in circadian photoreception. Science 2004; 304:1503-6; PMID:15178801; http://dx.doi.org/10.1126/science.1096973
  • Yoshii T, Hermann-Luibl C, Kistenpfennig C, Schmid B, Tomioka K, Helfrich-Förster C. Cryptochrome-dependent and -independent circadian entrainment circuits in Drosophila. J Neurosci 2015; 35:6131-41; PMID:25878285; http://dx.doi.org/10.1523/JNEUROSCI.0070-15.2015
  • Vinayak P, Coupar J, Hughes SE, Fozdar P, Kilby J, Garren E, Yoshii T, Hirsh J. Exquisite light sensitivity of Drosophila melanogaster cryptochrome. PLoS Genet 2013; 9:e1003615; PMID:23874218; http://dx.doi.org/10.1371/journal.pgen.1003615
  • Fogle KJ, Parson KG, Dahm NA, Holmes TC. Cryptochrome is a blue-light sensor that regulates neuronal firing rate. Science 2011; 331:1409-13; PMID:21385718; http://dx.doi.org/10.1126/science.1199702
  • Fogle KJ, Baik LS, Houl JH, Tran TT, Roberts L, Dahm NA, Cao Y, Zhou M, Holmes TC. Cryptochrome-mediated phototransduction by modulation of the potassium ion channel β-subunit redox sensor. Proc Natl Acad Sci USA 2015; 112:2245-50; PMID:25646452; http://dx.doi.org/10.1073/pnas.1416586112
  • Helfrich-Förster C, Edwards T, Yasuyama K, Wisotzki B, Schneuwly S, Stanewsky R, Meinertzhagen IA, Hofbauer A. The extraretinal eyelet of Drosophila: development, ultrastructure, and putative circadian function. J Neurosci 2002; 22:9255-66; PMID:12417651
  • Rieger D, Stanewsky R, Helfrich-Förster C. Cryptochrome, compound eyes, Hofbauer-Buchner eyelets, and ocelli play different roles in the entrainment and masking pathway of the locomotor activity rhythm in the fruit fly Drosophila melanogaster. J Biol Rhythms 2003; 18:377-91; PMID:14582854; http://dx.doi.org/10.1177/0748730403256997
  • Bachleitner W, Kempinger L, Wülbeck C, Rieger D, Helfrich-Förster C. Moonlight shifts the endogenous clock of Drosophila melanogaster. Proc Natl Acad Sci USA 2007; 104:3538-43; PMID:17307880; http://dx.doi.org/10.1073/pnas.0606870104
  • Schlichting M, Grebler R, Peschel N, Yoshii T, Helfrich-Förster C. Moonlight detection by Drosophila's endogenous clock depends on multiple photopigments in the compound eyes. J Biol Rhythms 2014; 29:75-86; PMID:24682202; http://dx.doi.org/10.1177/0748730413520428
  • Helfrich-Förster C. Differential control of morning and evening components in the activity rhythm of Drosophila melanogaster–sex-specific differences suggest a different quality of activity. J Biol Rhythms 2000; 15:135-54; PMID:10762032; http://dx.doi.org/10.1177/074873040001500208
  • Kempinger L, Dittmann R, Rieger D, Helfrich-Förster C. The nocturnal activity of fruit flies exposed to artificial moonlight is partly caused by direct light effects on the activity level that bypass the endogenous clock. Chronobiol Int 2009; 26:151-66; http://dx.doi.org/10.1080/07420520902747124
  • Behnia R, Desplan C. Visual circuits in flies: beginning to see the whole picture. Curr Opin Neurobiol 2015; 34:125-32; PMID:25881091; http://dx.doi.org/10.1016/j.conb.2015.03.010
  • Rieger D, Fraunholz C, Popp J, Bichler D, Dittmann R, Helfrich-Förster C. The fruit fly Drosophila melanogaster favors dim light and times its activity peaks to early dawn and late dusk. J Biol Rhythms 2007; 22:387-99; PMID:17876060; http://dx.doi.org/10.1177/0748730407306198
  • Vanin S, Bhutani S, Montelli S, Menegazzi P, Green EW, Pegoraro M, Sandrelli F, Costa R, Kyriacou CP. Unexpected features of Drosophila circadian behavioural rhythms under natural conditions. Nature 2012; 484:371-5; PMID:22495312; http://dx.doi.org/10.1038/nature10991
  • Menegazzi P, Vanin S, Yoshii T, Rieger D, Hermann C, Dusik V, Kyriacou CP, Helfrich-Förster C, Costa R. Drosophila clock neurons under natural conditions. J Biol Rhythm 2013; 28:3-14; http://dx.doi.org/10.1177/0748730412471303
  • Schlichting M, Grebler R, Menegazzi P, Helfrich-Förster C. Twilight dominates over moonlight in adjusting Drosophila's activity pattern. J Biol Rhythms 2015; 30:117-28; PMID:25838418; http://dx.doi.org/10.1177/0748730415575245
  • Schlichting M, Menegazzi P, Helfrich-Förster C. Normal vision can compensate for the loss of the circadian clock. Proc Biol Sci 2015; 282(1815). pii:20151846 PMID:26378222
  • Hofbauer A, Buchner E. Dose Drosophila have seven eyes? Naturwissenschaften 1989; 76:335-6; http://dx.doi.org/10.1007/BF00368438
  • Yasuyama K, Meinertzhagen IA. Extraretinal photoreceptors at the compound eye's posterior margin in Drosophila melanogaster. J Comp Neurol 1999; 412:193-202; PMID:10441750; http://dx.doi.org/10.1002/(SICI)1096-9861(19990920)412:2<193::AID-CNE1>3.0.CO;2-0
  • Malpel S, Klarsfeld A, Rouyer F. Larval optic nerve and adult extra-retinal photoreceptors sequentially associate with clock neurons during Drosophila brain development. Development 2002; 129:1443-53; PMID:11880353
  • Yuan Q, Xiang Y, Yan Z, Han C, Jan LY, Jan YN. Light-induced structural and functional plasticity in Drosophila larval visual system. Science 2011; 333:1458-62; PMID:21903815; http://dx.doi.org/10.1126/science.1207121
  • Pollack I, Hofbauer A. Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster. Cell Tissue Res 1991; 266:391-8; PMID:1684918; http://dx.doi.org/10.1007/BF00318195
  • Wegener C, Hamasaka Y, Nässel DR. Acetylcholine increases intracellular Ca2+ via nicotinic receptors in cultured PDF-containing clock neurons of Drosophila. J Neurophysiol 2004; 91:912-23; PMID:14534288; http://dx.doi.org/10.1152/jn.00678.2003
  • Lelito KR, Shafer OT. Reciprocal cholinergic and GABAergic modulation of the small ventrolateral pacemaker neurons of Drosophila's circadian clock neuron network. J Neurophysiol 2012; 107:2096-108; PMID:22279191; http://dx.doi.org/10.1152/jn.00931.2011
  • Klarsfeld A, Picot M, Vias C, Chelot E, Rouyer F. Identifying specific light inputs for each subgroup of brain clock neurons in Drosophila larvae. J Neurosci 2011; 31:17406-15; PMID:22131402; http://dx.doi.org/10.1523/JNEUROSCI.5159-10.2011
  • Veleri S, Rieger D, Helfrich-Förster C, Stanewsky R. Hofbauer-Buchner eyelet affects circadian photosensitivity and coordinates TIM and PER expression in Drosophila clock neurons. J Biol Rhythms 2007; 22:29-42; PMID:17229923; http://dx.doi.org/10.1177/0748730406295754
  • Szular J, Sehadova H, Gentile C, Szabo G, Chou WH, Britt SG, Stanewsky R. Rhodopsin 5- and Rhodopsin 6-mediated clock synchronization in Drosophila melanogaster is independent of retinal phospholipase C-β signaling. J Biol Rhyth 2012; 27:25-36; http://dx.doi.org/10.1177/0748730411431673
  • Hong ST, Bang S, Paik D, Kang J, Hwang S, Jeon K, et al. Histamine and its receptors modulate temperature-preference behaviors in Drosophila. J Neurosci 2006; 26:7245-56; PMID:16822982; http://dx.doi.org/10.1523/JNEUROSCI.5426-05.2006
  • Pantazis A, Segaran A, Liu CH, Nikolaev A, Rister J, Thum AS, Chun B, Hyun S, Lee Y, Kim J. Distinct roles for two histamine receptors (hclA and hclB) at the Drosophila photoreceptor synapse. J Neurosci 2008; 28:7250-9; PMID:18632929; http://dx.doi.org/10.1523/JNEUROSCI.1654-08.2008
  • Yuan Q, Lin F, Zheng X, Sehgal A. Serotonin modulates circadian entrainment in Drosophila. Neuron 2005; 47:115-27; PMID:15996552; http://dx.doi.org/10.1016/j.neuron.2005.05.027
  • Hirsh J, Riemensperger T, Coulom H, Iche M, Coupar J, Birman S. Roles of dopamine in circadian rhythmicity and extreme light sensitivity of circadian entrainment. Curr Biol 2010; 20:209-14; PMID:20096587; http://dx.doi.org/10.1016/j.cub.2009.11.037
  • Mazzotta G, Rossi A, Leonardi E, Mason M, Bertolucci C, Caccin L, Spolaore B, Martin AJ, Schlichting M, Grebler R, et al. Fly cryptochrome and the visual system. Proc Natl Acad Sci USA 2013; 110:6163-8; PMID:23536301; http://dx.doi.org/10.1073/pnas.1212317110
  • Emery P, Stanewsky R, Helfrich-Förster C, Emery-Le M, Hall JC, Rosbash M. Drosophila CRY is a deep brain circadian photoreceptor. Neuron 2000; 26:493-504; PMID:10839367; http://dx.doi.org/10.1016/S0896-6273(00)81181-2
  • Im SH, Taghert PH. PDF receptor expression reveals direct interactions between circadian oscillators in Drosophila. J Comp Neurol 2010; 518:1925-45; PMID:20394051; http://dx.doi.org/10.1002/cne.22311
  • Shang Y, Griffith LC, Rosbash M. Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc Natl Acad Sci USA 2008; 105:19587-94; PMID:19060186; http://dx.doi.org/10.1073/pnas.0809577105
  • Cusumano P, Klarsfeld A, Chelot E, Picot M, Richier B, Rouyer F. PDF-modulated visual inputs and cryptochrome define diurnal behavior in Drosophila. Nat Neurosci 2009; 12:1431-7; PMID:19820704; http://dx.doi.org/10.1038/nn.2429
  • Zhang L, Lear BC, Seluzicki A, Allada R. The Cryptochrome photoreceptor gates PDF neuropeptide signaling to set circadian network hierarchy in Drosophila. Curr Biol 2009; 19:2050-5; PMID:19913424; http://dx.doi.org/10.1016/j.cub.2009.10.058
  • Im SH, Li W, Taghert PH. PDFR and CRY signaling converge in a subset of clock neurons to modulate the amplitude and phase of circadian behavior in Drosophila. PLoS One 2011; 6:e18974; PMID:21559487; http://dx.doi.org/10.1371/journal.pone.0018974
  • Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ, Garrity PA. An internal thermal sensor controlling temperature preference in Drosophila. Nature 2008; 454:217-20; PMID:18548007; http://dx.doi.org/10.1038/nature07001
  • Guo F, Cerullo I, Chen X, Rosbash M. PDF neuron firing phase-shifts key circadian activity neurons in Drosophila. ELife 2014; 17:3
  • Duvall LB, Taghert PH. The circadian neuropeptide PDF signals preferentially through a specific adenylate cyclase isoform AC3 in M pacemakers of Drosophila. PLoS Biol 2012; 10:e1001337; PMID:22679392; http://dx.doi.org/10.1371/journal.pbio.1001337
  • Li Y, Guo F, Shen J, Rosbash M. PDF and cAMP enhance PER stability in Drosophila clock neurons. Proc Natl Acad Sci U S A 2014; 111:E1284-90; PMID:24707054; http://dx.doi.org/10.1073/pnas.1402562111
  • Seluzicki A, Flourakis M, Kula-Eversole E, Zhang L, Kilman V, Allada R. Dual PDF signaling pathways reset clocks via TIMELESS and acutely excite target neurons to control circadian behavior. PLoS Biol 2014; 12:e1001810; PMID:24643294; http://dx.doi.org/10.1371/journal.pbio.1001810
  • Veleri S, Brandes C, Helfrich-Förster C, Hall JC, Stanewsky R. A self-sustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr Biol 2003; 13:1758-67; PMID:14561400; http://dx.doi.org/10.1016/j.cub.2003.09.030
  • Chen KF, Peschel N, Zavodska R, Sehadova H, Stanewsky R. Quasimodo, a Novel GPI-anchored zona pellucida protein involved in light input to the Drosophila circadian clock. Curr Biol 2011; 21:719-29; PMID:21530261; http://dx.doi.org/10.1016/j.cub.2011.03.049