The blue-light photoreceptor CRYPTOCHROME is expressed in a subset of circadian oscillator neurons in the Drosophila CNS

Journal of Biological Rhythms

Volumn 23, Issue 4, 2008, Pages 296-307

  Benito, Juliana ^b,c   Houl, Jerry H ^a,b   Roman, Gregg W ^b   Hardin, Paul E ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF HOUSTON   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

Behavior; Circadian clock; Cryptochrome; Drosophila; Immunolocalization; Mutant

Indexed keywords

CRYPTOCHROME; TRANSCRIPTION FACTOR;

ARTICLE; BLUE LIGHT; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CIRCADIAN RHYTHM; DROSOPHILA MELANOGASTER; LIGHT DARK CYCLE; NERVE CELL; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOLOGICAL CLOCKS; CELL NUCLEUS; CENTRAL NERVOUS SYSTEM; CYTOPLASM; DROSOPHILA; DROSOPHILA PROTEINS; EYE PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE, DIRECT; GENE DELETION; NEURONS; PHOTORECEPTORS, INVERTEBRATE; RECEPTORS, G-PROTEIN-COUPLED;

DROSOPHILA MELANOGASTER;

EID: 47549086116     PISSN: 07487304     EISSN: 15524531     Source Type: Journal    
DOI: 10.1177/0748730408318588     Document Type: Article

References (51)

1. Bell-Pedersen D., Cassone VM, Earnest DJ, Golden SS, Hardin PE, Thomas TL, and Zoran MJ (2005) Circadian rhythms from multiple oscillators: Lessons from diverse organisms. Nat Rev Genet 6: 544-556.
2. Busza A., Emery-Le M., Rosbash M., and Emery P. (2004) Roles of the two Drosophila CRYPTOCHROME structural domains in circadian photoreception. Science 304: 1503-1506.
3. Cashmore AR, Jarillo JA, Wu YJ, and Liu D. (1999) Cryptochromes: Blue light receptors for plants and animals. Science 284: 760-765.
4. Ceriani MF, Darlington TK, Staknis D., Mas P., Petti AA, Weitz CJ, and Kay SA (1999) Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science 285: 553-556.
5. Cheng Y. and Hardin PE (1998) Drosophila photoreceptors contain an autonomous circadian oscillator that can function without period mRNA cycling. J Neurosci 18: 741-750.
6. Collins B, Mazzoni EO, Stanewsky R, and Blau J (2006) Drosophila CRYPTOCHROME is a circadian transcriptional repressor. Curr Biol 16: 441-449.
7. de Velasco B., Erclik T., Shy D., Sclafani J., Lipshitz H., McInnes R., and Hartenstein V. (2007) Specification and development of the pars intercerebralis and pars lateralis, neuroendocrine command centers in the Drosophila brain. Dev Biol 302: 309-323.
8. Dolezelova E., Dolezel D., and Hall JC (2007) Rhythm defects caused by newly engineered null mutations in Drosophila's cryptochrome gene. Genetics 177: 329-345.
9. Egan ES, Franklin TM, Hilderbrand-Chae MJ, McNeil GP, Roberts MA, Schroeder AJ, Zhang X., and Jackson FR (1999) An extraretinally expressed insect cryptochrome with similarity to the blue light photoreceptors of mammals and plants. J Neurosci 19: 3665-3673.
10. Emery P., So WV, Kaneko M., Hall JC, and Rosbash M. (1998) CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95: 669-679.
11. Emery P, Stanewsky R, Hall JC, and Rosbash M (2000 a) A unique circadian-rhythm photoreceptor. Nature 404: 456-457.
12. Emery P, Stanewsky R, Helfrich-Forster C, Emery-Le M, Hall JC, and Rosbash M (2000 b) Drosophila CRY is a deep brain circadian photoreceptor. Neuron 26: 493-504.
13. Greenspan RJ (2004) Fly Pushing: The Theory and Practice of Drosophila Genetics. Cold Spring Harbor: Cold Spring Harbor Press.
14. Grima B., Chelot E., Xia R., and Rouyer F. (2004) Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431: 869-873.
15. Hall JC (2003) Genetics and molecular biology of rhythms in Drosophila and other insects. Adv Genet 48: 1-280.
16. Hardin PE (2005) The circadian timekeeping system of Drosophila. Curr Biol 15: R714-722.
17. Hazelrigg T., Levis R., and Rubin GM (1984) Transformation of white locus DNA in Drosophila: dosage compensation, zeste interaction, and position effects. Cell 36: 469-481.
18. Helfrich-Forster C. (2005) Neurobiology of the fruit fly's circadian clock. Genes Brain Behav 4: 65-76.
19. Helfrich-Forster C., Shafer OT, Wulbeck C., Grieshaber E., Rieger D., and Taghert P. (2007) Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J Comp Neurol 500: 47-70.
20. Helfrich-Forster C, Winter C, Hofbauer A, Hall JC, and Stanewsky R (2001) The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30: 249-261.
21. Houl JH, Yu W., Dudek SM, and Hardin PE (2006) Drosophila CLOCK is constitutively expressed in circadian oscillator and non-oscillator cells. J Biol Rhythms 21: 93-103.
22. Hunter-Ensor M., Ousley A., and Sehgal A. (1996) Regulation of the Drosophila protein timeless suggests a mechanism for resetting the circadian clock by light. Cell 84: 677-685.
23. Ivanchenko M, Stanewsky R, and Giebultowicz JM (2001) Circadian photoreception in Drosophila: Functions of cryptochrome in peripheral and central clocks. J Biol Rhythms 16: 205-215.
24. Klarsfeld A., Malpel S., Michard-Vanhee C., Picot M., Chelot E., and Rouyer F. (2004) Novel features of cryptochrome-mediated photoreception in the brain circadian clock of Drosophila. J Neurosci 24: 1468-1477.
25. Koh K., Zheng X., and Sehgal A. (2006) JETLAG resets the Drosophila circadian clock by promoting light-induced degradation of TIMELESS. Science 312: 1809-1812.
26. Konopka RJ and Benzer S. (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 68: 2112-2116.
27. Krishnan B., Dryer SE, and Hardin PE (1999) Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature 400: 375-378.
28. Krishnan B., Levine JD, Lynch MK, Dowse HB, Funes P., Hall JC, Hardin PE, and Dryer SE (2001) A new role for cryptochrome in a Drosophila circadian oscillator. Nature 411: 313-317.
29. Kume K., Zylka MJ, Sriram S., Shearman LP, Weaver DR, Jin X., Maywood ES, Hastings MH, and Reppert SM (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98: 193-205.
30. Levine JD, Funes P., Dowse HB, and Hall JC (2002) Advanced analysis of a cryptochrome mutation's effects on the robustness and phase of molecular cycles in isolated peripheral tissues of Drosophila. BMC Neurosci 3: 5.
31. Lin FJ, Song W., Meyer-Bernstein E., Naidoo N., and Sehgal A. (2001) Photic signaling by cryptochrome in the Drosophila circadian system. Mol Cell Biol 21: 7287-7294.
32. Meyer P., Saez L., and Young MW (2006) PER-TIM interactions in living Drosophila cells: An interval timer for the circadian clock. Science 311: 226-229.
33. Myers MP, Wager-Smith K., Rothenfluh-Hilfiker A., and Young MW (1996) Light-induced degradation of TIMELESS and entrainment of the Drosophila circadian clock. Science 271: 1736-1740.
34. Park JH, Helfrich-Forster C., Lee G., Liu L., Rosbash M., and Hall JC (2000) Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Natl Acad Sci U S A 97: 3608-3613.
35. Peschel N, Veleri S, and Stanewsky R (2006) Veela defines a molecular link between Cryptochrome and Timeless in the light-input pathway to Drosophila's circadian clock. Proc Natl Acad Sci U S A 103: 17313-17318.
36. Rieger D., Shafer OT, Tomioka K., and Helfrich-Forster C. (2006) Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 26: 2531-2543.
37. Rieger D, Stanewsky R, and Helfrich-Forster C (2003) 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 18: 377-391.
38. Rutila JE, Suri V., Le M., So WV, Rosbash M., and Hall JC (1998) CYCLE is a second bHLH-PAS clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell 93: 805-814.
39. Shafer OT, Helfrich-Forster C., Renn SC, and Taghert PH (2006) Reevaluation of Drosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes. J Comp Neurol 498: 180-193.
40. Shafer OT, Rosbash M., and Truman JW (2002) Sequential nuclear accumulation of the clock proteins period and timeless in the pacemaker neurons of Drosophila melanogaster. J Neurosci 22: 5946-5954.
41. Stanewsky R, Kaneko M, Emery P, Beretta B, Wager-Smith K, Kay SA, Rosbash M, and Hall JC (1998) The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95: 681-692.
42. Stoleru D., Peng Y., Agosto J., and Rosbash M. (2004) Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431: 862-868.
43. Stoleru D., Peng Y., Nawathean P., and Rosbash M. (2005) A resetting signal between Drosophila pacemakers synchronizes morning and evening activity. Nature 438: 238-242.
44. Tanoue S., Krishnan P., Krishnan B., Dryer SE, and Hardin PE (2004) Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr Biol 14: 638-649.
45. Veleri S, Brandes C, Helfrich-Forster C, Hall JC, and Stanewsky R (2003) A self-sustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr Biol 13: 1758-1767.
46. Veleri S, Rieger D, Helfrich-Forster C, and Stanewsky R (2007) Hofbauer-Buchner eyelet affects circadian photosensitivity and coordinates TIM and PER expression in Drosophila clock neurons. J Biol Rhythms 22: 29-42.
47. Wilson RJ, Goodman JL, and Strelets VB (2008) FlyBase: Integration and improvements to query tools. Nucleic Acids Res 36: D588-593.
48. Yang Z. and Sehgal A. (2001) Role of molecular oscillations in generating behavioral rhythms in Drosophila. Neuron 29: 453-467.
49. Zeng H., Qian Z., Myers MP, and Rosbash M. (1996) A light-entrainment mechanism for the Drosophila circadian clock. Nature 380: 129-135.
50. Zhao J., Kilman VL, Keegan KP, Peng Y., Emery P., Rosbash M., and Allada R. (2003) Drosophila Clock can generate ectopic circadian clocks. Cell 113: 755-766.
51. Zheng H., Ng F., Liu Y., and Hardin PE (2008) Spatial and circadian regulation of cry in Drosophila. J Biol Rhythms 23: 283-295.