Reevaluation of Drosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes

Journal of Comparative Neurology

Volumn 498, Issue 2, 2006, Pages 180-193

  Shafer, Orie Thomas ^a   Helfrich Förster, Charlotte ^b   Renn, Susan Christine Portia ^a,c   Taghert, Paul H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c HARVARD UNIVERSITY   (United States)

Author keywords

Circadian clock; Drosophila; Glass; IPNamide; Neuropeptides; nplp1; PDF receptor

Indexed keywords

BETA GALACTOSIDASE; ISOLEUCYLPROLYLASPARAGINAMIDE; NEUROPEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CELL SUBPOPULATION; CIRCADIAN RHYTHM; DROSOPHILA MELANOGASTER; NONHUMAN; NUCLEOTIDE SEQUENCE; PACEMAKER NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE;

ANIMALS; BIOLOGICAL CLOCKS; BIOLOGICAL MARKERS; CIRCADIAN RHYTHM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENES, REPORTER; MEDULLA OBLONGATA; NEURAL PATHWAYS; NEURONS; NEUROPEPTIDES; NUCLEAR PROTEINS; PERIOD CIRCADIAN PROTEINS;

EID: 33746818002     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21021     Document Type: Article

References (39)

1. Baggerman G, Cerstiaens A, De Loof A, Schoofs L. 2002. Peptidomics of the larval Drosophila melanogaster central nervous system. J Biol Chem 277:40368-40374.
2. Cyran SA, Buchsbaum AM, Reddy KL, Lin MC, Glossop MR, Hardin PE, Young MW, Storti RV, Blau J. 2003. vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 112:329-341.
3. Dunlap JC. 1999. Molecular bases for circadian clocks. Cell 96:271-790.
4. Ewer J, Frisch B, Hamblen-Coyle MJ, Rosbash M, Hall JC. 1992. Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells' influence on circadian behavioral rhythms. J Neurosci 12:3321-3349.
5. Frisch B, Hardin PE, Hamblen-Coyle MJ, Rosbash M, Hall JC. 1994. A promoterless period gene mediates behavioral rhythmicity and cyclical per expression in a restricted subset of the Drosophila nervous system. Neuron 12:555-570.
6. Gríma B, Chélot E, Xia R, Rouyer F. 2004. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431:869-873.
7. Hall JC. 2005. Systems approaches to biological rhythms in Drosophila. Methods Enzymol 393:61-185.
8. Hardin PE. 2004. Transcription regulation within the circadian clock: the E-box and beyond. J Biol Rhythms 19:348-360.
9. Helfrich-Förster C. 1998. Robust circadian rhythmicity of Drosophila melanogaster requires the presence of lateral neurons: a brain-behavioral study of disconnected mutants. J Comp Physiol A 182:435-453.
10. Helfrich-Förster C. 2003. The neuroarchitecture of the circadian clock in the brain of Drosophila melanogaster. Microsc Res Techn 62:94-102.
11. Helfrich-Förster C. 2005. Techniques that revealed the network of the circadian clock of Drosophila. Methods Enzymol 393:439-451.
12. Helfrich-Förster C, Winter C, Hofbauer A, Hall JC, Stanewsky R. 2001. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30:249-261.
13. Kaneko M, Hall JC. 2000. Neuroanatomy of cells expressing clock genes in Drosophila: transgeneic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections. J Comp Neurol 422:66-94.
14. Klarsfeld A, Malpel S, Michard-Vanhée C, Picot M, Chélot E, Rouyer F. 2004. Novel features of cryptochrome-mediated photoreception in the brain circadian clock of Drosophila. J Neurosci 24:1468-1477.
15. Leak RK, Moore RY. 2000. Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol 433:312-334.
16. Lin Y, Stormo GD, Taghert PH. 2004. The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J Neurosci 24:7951-7957.
17. Lindsley DL, Zimm GG. 1992. Genetic variations of Drosophila melanogaster. San Diego: Academic Press.
18. Liu X, Zwiebel LJ, Hinton D, Benzer S, Hall JC, Rosbash M. 1992. The period gene encodes a predominantly nuclear protein in adult Drosophila. J Neurosci 12:2735-2744.
19. Moses K, Rubin GM. 1991. Glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes Dev 5:583-593.
20. Moses K, Ellis MC, Rubin RM. 1989. The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells. Nature 340:531-536.
21. Nitabach MN, Blau J, Holmes TC. 2002. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109:485-495.
22. O'Neill EM, Rebay I, Tijan R, Rubin GM. 1994. The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78:137-147.
23. Park JH, Helfrich-Forster C, Lee G, Liu L, Rosbash M, 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.
24. Peng Y, Stoleru D, Levine JD, Hall JC, Rosbash M. 2003. Drosophila free-running rhythms rquire intercellular communication. Pub Lib Sci Biol 1:32-40.
25. Renn SCP, Park JH, Rosbash M, Hall JC, Taghert PH. 1999. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99:971-802.
26. Samson ML, Lisbin MJ, White K. 1995. Two distinct temperature-sensitive alleles at the elav locus of Drosophila are suppressed nonsense mutations of the same tryptophan codon. Genetics 141:1101-1111.
27. Schneider LE, Roberts MS, Taghert PH. 1993. Cell type-specific transcriptional regulation of the Drosophila FMRFamide neuropeptide gene. Neuron 10:279-291.
28. Schöning JC, Staiger D. 2005. At the pulse of time: protein interactions determine the pace of circadian clocks. FEBS Lett 579:3246-3252.
29. Sepp KJ, Auld VJ. 1999. Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151:1093-1101.
30. Shafer OT, Rosbash M, 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.
31. Stoleru D, Ping Y, Agosto J, Rosbash M. 2004. Coupled oscillators control morning and evening locomotor behavior in Drosophila. Nature 431:862-868.
32. Suh GS, Wong AM, Hergarden AC, Wang JW, Simon AF, Benzer S, Axel R, Anderson DJ. 2004. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431:854-8599.
33. Taghert PH, Lin Y. 2005. Tick-talk: the cellular and molecular biology of Drosophila circadian rhythms. In: Gilbert LI, Iatrou K, Gill SS, editors. Comprehensive molecular insect science. Amsterdam: Elsevier, p 357-395.
34. Taghert PH, Hewes RS, Park JH, O'Brien MA, Han M, Peck ME. 2001. Multiple amidated neuropeptides are required for normal circadian rhythmicity in Drosophila. J Neurosci 21:6673-6686.
35. Veleri S, Brandes C, Helfrich-Förster C, Hall JC, Stanewsky R. 2003. A self-sustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr Biol 13:1758-1767.
36. Verleyen P, Baggerman G, Wiehart W, Schoeters E, Van Lommel A, De Loof A, Schoofs L. 2004. Expression of a novel neuropeptide, NVGT-LARDFQLPIPNamide, in the larval and adult brain of Drosophila melanogaster. J Neurochem 88:311-319.
37. Yang Z, Sehgal A. 2001. Role of molecular oscillations in generating behavioral rhythms in Drosophila. Neuron 29:453-467.
38. Yoshii T, Heshiki Y, Ibuki-Ishibashi T, Matsumoto A, Tanimura T, Tomioka K. 2005. Temperature cycles drive Drosophila circadian oscillation in constant light that otherwise induces behavioural arrhythmicity. Eur J Neurosci 22:1176-1184.
39. Zhao J, Kilman VL, Keegan KP, Peng Y, Emery P, Rosbash M, Allada R. 2003. Drosophila Clock can generate ectopic circadian clocks. Cell 13:755-766.