Circadian light-input pathways in Drosophila

Communicative and Integrative Biology

Volumn 9, Issue 1, 2016, Pages

  Yoshii, Taishi ^a   Hermann Luibl, Christiane ^b   Helfrich Föorster, Charlotte ^b  

^a OKAYAMA UNIVERSITY   (Japan)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Circadian clock; Circadian rhythm; Cryptochrome; Drosophila melanogaster; Light entrainment; Photoreceptor; Pigmentdispersing factor

Indexed keywords

EID: 84960916789     PISSN: None     EISSN: 19420889     Source Type: Journal    
DOI: 10.1080/19420889.2015.1102805     Document Type: Review

References (69)

1. 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
2. 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
3. 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
4. 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
5. 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
6. 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
7. Yoshii T, Wülbeck C, Sehadova H, Veleri S, Bichler D, Stanewsky R, Helfrich-Förster C. The neuropeptide pigmentdispersing 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
8. 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
9. 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
10. 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
11. 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
12. 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
13. 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
14. 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/annurevarplant-042110-103759
15. 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
16. 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
17. 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
18. 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
19. Benito J, Houl JH, Roman GW, Hardin PE. The bluelight 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
20. 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
21. 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
22. 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
23. 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
24. 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
25. 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
26. Yoshii T, Hermann-Luibl C, Kistenpfennig C, Schmid B, Tomioka K, Helfrich-F€orster 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
27. 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
28. 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
29. 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 b-subunit redox sensor. Proc Natl Acad Sci USA 2015; 112:2245-50; PMID:25646452; http://dx.doi.org/10.1073/pnas.1416586112
30. 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
31. 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
32. Bachleitner W, Kempinger L, W€ulbeck C, Rieger D, Helfrich- F€orster 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
33. Schlichting M, Grebler R, Peschel N, Yoshii T, Helfrich- F€orster 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
34. 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
35. Kempinger L, Dittmann R, Rieger D, Helfrich-F€orster 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
36. 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
37. Rieger D, Fraunholz C, Popp J, Bichler D, Dittmann R, Helfrich-F€orster 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
38. 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
39. 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
40. 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
41. 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
42. Hofbauer A, Buchner E. Dose Drosophila have seven eyes? Naturwissenschaften 1989; 76:335-6; http://dx.doi.org/10.1007/BF00368438
43. 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
44. 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
45. 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
46. 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
47. Wegener C, Hamasaka Y, N€assel DR. Acetylcholine increases intracellular Ca2C 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
48. 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
49. 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
50. 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
51. 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-b signaling. J Biol Rhyth 2012; 27:25-36; http://dx.doi.org/10.1177/0748730411431673
52. 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
53. 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
54. 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
55. 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
56. 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
57. 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
58. 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
59. 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
60. 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
61. 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
62. 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
63. 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
64. Guo F, Cerullo I, Chen X, Rosbash M. PDF neuron firing phase-shifts key circadian activity neurons in Drosophila. ELife 2014; 17:3
65. 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
66. 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
67. 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
68. 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
69. 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