PDF-modulated visual inputs and cryptochrome define diurnal behavior in Drosophila

Nature Neuroscience

Volumn 12, Issue 11, 2009, Pages 1431-1437

  Cusumano, Paola ^a   Klarsfeld, André ^a   Chélot, Elisabeth ^a   Picot, Marie ^a   Richier, Benjamin ^a   Rouyer, François ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME; PIGMENT DISPERSING FACTOR; PIGMENT DISPERSING FACTOR RECEPTOR; RECEPTOR PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; NEUROPEPTIDE; NEUROPEPTIDE RECEPTOR; PDF PROTEIN, DROSOPHILA; PIGMENT EPITHELIUM DERIVED FACTOR RECEPTOR; PIGMENT EPITHELIUM-DERIVED FACTOR RECEPTOR;

ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DROSOPHILA; LIGHT DARK CYCLE; MOLECULAR CLOCK; NONHUMAN; OSCILLATION; OSCILLATOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VISUAL SYSTEM; ANIMAL; ANIMAL BEHAVIOR; BIOLOGICAL RHYTHM; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MOTOR ACTIVITY; MUTATION; NERVE CELL; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; BIOLOGICAL CLOCKS; CRYPTOCHROMES; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; MALE; MOTOR ACTIVITY; MUTATION; NEURONS; NEUROPEPTIDES; RECEPTORS, NEUROPEPTIDE; SIGNAL TRANSDUCTION; VISUAL PATHWAYS;

EID: 74949097778     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2429     Document Type: Article

References (50)

1. Dunlap, J.C., Loros, J.J. & DeCoursey, P.J. Chronobiology. Biological Timekeeping (Sinauer Associates, Sunderland, Massachusetts, 2004).
2. Matsumoto, A., Matsumoto, N., Harui, Y., Sakomoto, M. & Tomioka, K. Light and temperature cooperate to regulate the circadian locomotor rhythm of wild type and period mutants of Drosophila melanogaster. J. Insect Physiol. 44, 587-596 (1998). (Pubitemid 28330927)
3. Majercak, J., Sidote, D., Hardin, P.E. & Edery, I. How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 24, 219-230 (1999). (Pubitemid 29466160)
4. Rieger, D., Stanewsky, R. & Helfrich-Förster, C. Cryptochrome, compound eyes, H-B 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 18, 377-391 (2003). (Pubitemid 37204460)
5. Stoleru, D. et al. The Drosophila circadian network is a seasonal timer. Cell 129, 207-219 (2007). (Pubitemid 46507587)
6. Shafer, O.T., Helfrich-Forster, C., Renn, S.C. & Taghert, P.H. Reevaluation of Drosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes. J. Comp. Neurol. 498, 180-193 (2006). (Pubitemid 44182459)
7. Helfrich-Förster, C. et al. Development and morphology of the clock gene-expressing lateral neurons of Drosophila melanogaster. J. Comp. Neurol. 500, 47-70 (2007). (Pubitemid 44904301)
8. Emery, P. et al. Drosophila CRY is a deep brain circadian photoreceptor. Neuron 26, 493-504 (2000).
9. Klarsfeld, A. et al. Novel features of cryptochrome-mediated photoreception in the brain circadian clock of Drosophila. J. Neurosci. 24, 1468-1477 (2004). (Pubitemid 38222999)
10. Picot, M., Cusumano, P., Klarsfeld, A., Ueda, R. & Rouyer, F. Light activates output from evening neurons and inhibits output from morning neurons in the Drosophila circadian clock. PLoS Biol. 5, e315 (2007).
11. Benito, J., Houl, J.H., Roman, G.W. & Hardin, P.E. The blue-light photoreceptor cryptochrome is expressed in a subset of circadian oscillator neurons in the Drosophila CNS. J. Biol. Rhythms 23, 296-307 (2008). (Pubitemid 352010014)
12. Yoshii, T., Todo, T., Wulbeck, C., Stanewsky, R. & Helfrich-Forster, C. Cryptochrome is present in the compound eye and a subset of Drosophila's clock neurons. J. Comp. Neurol. 508, 952-966 (2008). (Pubitemid 351693553)
13. Dubruille, R. & Emery, P. A plastic clock: how circadian rhythms respond to environmental cues in Drosophila. Mol. Neurobiol. 38, 129-145 (2008).
14. Grima, B., Chélot, E., Xia, R. & Rouyer, F. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431, 869-873 (2004). (Pubitemid 39434085)
15. Stoleru, D., Peng, P., Agosto, J. & Rosbash, M. Coupled oscillators control morning and evening locomotor behavior of Drosophila. Nature 431, 862-868 (2004). (Pubitemid 39434084)
16. Stoleru, D., Peng, Y., Nawathean, P. & Rosbash, M. A resetting signal between Drosophila pacemakers synchronizes morning and evening activity. Nature 438, 238-242 (2005). (Pubitemid 41599877)
17. Stanewsky, R. et al. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95, 681-692 (1998). (Pubitemid 28544129)
18. Emery, P., Stanewsky, R., Hall, J.C. & Rosbash, M. A unique circadian-rhythm photoreceptor. Nature 404, 456-457 (2000). (Pubitemid 30186878)
19. Dolezelova, E., Dolezel, D. & Hall, J.C. Rhythm defects caused by newly engineered null mutations in Drosophila's cryptochrome gene. Genetics 177, 329-345 (2007). (Pubitemid 47555852)
20. Shang, Y., Griffith, L.C. & Rosbash, M. Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc. Natl. Acad. Sci. USA 105, 19587-19594 (2008).
21. Helfrich-Förster, C. et al. The extraretinal eyelet of Drosophila: development, ultrastructure and putative circadian function. J. Neurosci. 22, 9255-9266 (2002). (Pubitemid 35356169)
22. Malpel, S., Klarsfeld, A. & Rouyer, F. Larval optic nerve and adult extra-retinal photoreceptors sequentially associate with the clock neurons during Drosophila brain development. Development 129, 1443-1453 (2002). (Pubitemid 34874165)
23. Veleri, S., Rieger, D., Helfrich-Forster, C. & Stanewsky, R. Hofbauer-Buchner eyelet affects circadian photosensitivity and coordinates TIM and PER expression in Drosophila clock neurons. J. Biol. Rhythms 22, 29-42 (2007). (Pubitemid 46041611)
24. Helfrich-Förster, C., Winter, C., Hofbauer, A., Hall, J.C. & Stanewsky, R. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30, 249-261 (2001). (Pubitemid 32441691)
25. Renn, S.C., Park, J.H., Rosbash, M., Hall, J.C. & Taghert, P.H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99, 791-802 (1999). (Pubitemid 30017649)
26. Hyun, S. et al. Drosophila GPCR Han is a receptor for the circadian clock neuropeptide PDF. Neuron 48, 267-278 (2005).
27. Lear, B.C. et al. A G protein-coupled receptor, groom-of-PDF, is required for PDF neuron action in circadian behavior. Neuron 48, 221-227 (2005). (Pubitemid 41476356)
28. Mertens, I. et al. PDF receptor signaling in Drosophila contributes to both circadian and geotactic behaviors. Neuron 48, 213-219 (2005). (Pubitemid 41476355)
29. Wu, Y., Cao, G. & Nitabach, M.N. Electrical silencing of PDF neurons advances the phase of non-PDF clock neurons in Drosophila. J. Biol. Rhythms 23, 117-128 (2008). (Pubitemid 351393171)
30. Peng, Y., Stoleru, D., Levine, J.D., Hall, J.C. & Rosbash, M. Drosophila free-running rhythms require intercellular communication. PLoS Biol. 1, e13 (2003).
31. Lin, Y., Stormo, G.D. & Taghert, P.H. The neuropeptide PDF coordinates pacemaker interactions in the Drosophila circadian system. J. Neurosci. 24, 7951-7957 (2004). (Pubitemid 39215701)
32. Shafer, O.T. et al. Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 58, 223-237 (2008). (Pubitemid 351539003)
33. Wülbeck, C., Grieshaber, E. & Helfrich-Forster, C. Pigment-dispersing factor (PDF) has different effects on Drosophila's circadian clocks in the accessory medulla and in the dorsal brain. J. Biol. Rhythms 23, 409-424 (2008).
34. Yoshii, T. et al. The neuropeptide pigment-dispersing factor adjusts period and phase of Drosophila's clock. J. Neurosci. 29, 2597-2610 (2009).
35. Hanai, S. & Ishida, N. Entrainment of Drosophila circadian clock to green and yellow light by Rh1, Rh5, Rh6 and CRY. Neuroreport 20, 755-758 (2009).
36. 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 92, 612-616 (1995).
37. Park, J.H. et al. Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc. Natl. Acad. Sci. USA 97, 3608-3613 (2000). (Pubitemid 30183350)
38. Taghert, P.H. et al. Multiple amidated neuropeptides are required for normal circadian locomotor rhythms in Drosophila. J. Neurosci. 21, 6673-6686 (2001). (Pubitemid 32781112)
39. Kaneko, M., Helfrich-Förster, C. & Hall, J.C. Spatial and temporal expression of the period and timeless genes in the developing nervous system of Drosophila: newly identified pacemaker candidates and novel features of clock gene product cycling. J. Neurosci. 17, 6745-6760 (1997). (Pubitemid 27366626)
40. Picot, M., Klarsfeld, A., Chélot, E., Malpel, S. & Rouyer, F. A role for blind DN2 clock neurons in temperature entrainment of the Drosophila larval brain. J. Neurosci. 29, 8312-8320 (2009).
41. Sheeba, V. et al. Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr. Biol. 18, 1537-1545 (2008).
42. Emery, P., So, W.V., Kaneko, M., Hall, J.C. & Rosbash, M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95, 669-679 (1998). (Pubitemid 28544128)
43. Fernández, M.P., Berni, J. & Ceriani, M.F. Circadian remodeling of neuronal circuits involved in rhythmic behavior. PLoS Biol. 6, e69 (2008).
44. Sheeba, V., Gu, H., Sharma, V.K., O'Dowd, D.K. & Holmes, T.C. Circadian- and light-dependent regulation of resting membrane potential and spontaneous action potential firing of Drosophila circadian pacemaker neurons. J. Neurophysiol. 99, 976-988 (2008). (Pubitemid 351253250)
45. Mrosovsky, N. & Hattar, S. Diurnal mice (Mus musculus) and other examples of temporal niche switching. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 191, 1011-1024 (2005). (Pubitemid 41586772)
46. Doyle, S.E., Yoshikawa, T., Hillson, H. & Menaker, M. Retinal pathways influence temporal niche. Proc. Natl. Acad. Sci. USA 105, 13133-13138 (2008).
47. Aton, S.J., Colwell, C.S., Harmar, A.J., Waschek, J. & Herzog, E.D. Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat. Neurosci. 8, 476-483 (2005). (Pubitemid 41007565)
48. Blanchardon, E. et al. Defining the role of Drosophila lateral neurons in the control of circadian activity and eclosion rhythms by targeted genetic ablation and PERIOD protein overexpression. Eur. J. Neurosci. 13, 871-888 (2001). (Pubitemid 32226139)
49. Bergmann, A., Agapite, J., McCall, K. & Steller, H. The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95, 331-341 (1998). (Pubitemid 28507322)
50. Hamblen, M. et al. Germ-line transformation involving DNA from the period locus in Drosophila melanogaster: overlapping genomic fragments that restore circadian and ultradian rhythmicity to per0 and per- mutants. J. Neurogenet. 3, 249-291 (1986). (Pubitemid 16019622)