Surprising gene expression patterns within and between PDF-containing circadian neurons in Drosophila

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 30, 2010, Pages 13497-13502

  Kula Eversole, Elzbieta ^a,b   Nagoshi, Emi ^a,c   Shang, Yuhua ^a   Rodriguez, Joseph ^a   Allada, Ravi ^b   Rosbash, Michael ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

Cycling mRNAs; Microarrays; PDF neurons

Indexed keywords

MESSENGER RNA; OCTOPAMINE; DROSOPHILA PROTEIN; GREEN FLUORESCENT PROTEIN; NEUROPEPTIDE; NORSYNEPHRINE RECEPTOR; PDF PROTEIN, DROSOPHILA; RECEPTOR;

ARTICLE; CIRCADIAN RHYTHM; DROSOPHILA; GENE EXPRESSION; IN VITRO STUDY; NONHUMAN; OSCILLATION; PACEMAKER NERVE CELL; PRIORITY JOURNAL; PURIFICATION; ANIMAL; BIOLOGICAL RHYTHM; CYTOLOGY; DNA MICROARRAY; DROSOPHILA MELANOGASTER; FEMALE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION PROFILING; GENETICS; MALE; METABOLISM; NERVE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THALAMUS VENTRAL NUCLEUS;

ANIMALS; BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION PROFILING; GREEN FLUORESCENT PROTEINS; MALE; MICROSCOPY, FLUORESCENCE; NEURONS; NEUROPEPTIDES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, BIOGENIC AMINE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VENTRAL THALAMIC NUCLEI;

EID: 77955829612     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1002081107     Document Type: Article

References (47)

1. Hardin PE (2004) Transcription regulation within the circadian clock: The E-box and beyond. J Biol Rhythms 19:348-360.
2. Rosbash M, et al. (2007) Transcriptional feedback and definition of the circadian pacemaker in Drosophila and animals. Cold Spring Harb Symp Quant Biol 72:75-83.
3. Rosbash M (2009) The implications of multiple circadian clock origins. PLoS Biol 7:e62.
4. So WV, Rosbash M (1997) Post-transcriptional regulation contributes to Drosophila clock gene mRNA cycling. EMBO J 16:7146-7155.
5. Price JL, et al. (1998) double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell 94:83-95.
6. Martinek S, Inonog S, Manoukian AS, Young MW (2001) A role for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 105:769-779.
7. Lin JM, et al. (2002) A role for casein kinase 2alpha in the Drosophila circadian clock. Nature 420:816-820.
8. Akten B, et al. (2003) A role for CK2 in the Drosophila circadian oscillator. Nat Neurosci 6:251-257.
9. Helfrich-Förster C (2005) Neurobiology of the fruit fly's circadian clock. Genes Brain Behav 4:65-76.
10. Nitabach MN, Taghert PH (2008) Organization of the Drosophila circadian control circuit. Curr Biol 18:R84-R93.
11. Nagoshi E, et al. (2010) Dissecting differential gene expression within the circadian neuronal circuit of Drosophila. Nat Neurosci 13:60-68.
12. Shafer OT, et al. (2008) Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 58:223-237.
13. Helfrich-Förster C (1995) 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.
14. Kaneko M, Hall JC (2000) Neuroanatomy of cells expressing clock genes in Drosophila: Transgenic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections. J Comp Neurol 422:66-94.
15. Stoleru D, Peng Y, Agosto J, Rosbash M (2004) Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431:862-868.
16. Grima 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.
17. Shang Y, Griffith LC, Rosbash M (2008) Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc Natl Acad Sci USA 105:19587-19594.
18. Parisky KM, et al. (2008) PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60:672-682.
19. Sheeba V, et al. (2008) Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr Biol 18:1537-1545.
20. Sheeba V, Gu H, Sharma VK, O'Dowd DK, Holmes TC (2008) Circadian- and light-dependent regulation of resting membrane potential and spontaneous action potential firing of Drosophila circadian pacemaker neurons. J Neurophysiol 99:976-988.
21. Nelson SB, Sugino K, Hempel CM (2006) The problem of neuronal cell types: A physiological genomics approach. Trends Neurosci 29:339-345.
22. Helfrich-Förster C (1997) Development of pigment-dispersing hormone-immunoreactive neurons in the nervous system of Drosophilamelanogaster. J Comp Neurol 380:335-354.
23. Renn SC, 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 99:791-802.
24. Bae K, Lee C, Hardin PE, Edery I (2000) dCLOCK is present in limiting amounts and likely mediates daily interactions between the dCLOCK-CYC transcription factor and the PER-TIM complex. J Neurosci 20:1746-1753.
25. Kilman VL, Allada R (2009) Genetic analysis of ectopic circadian clock induction in Drosophila. J Biol Rhythms 24:368-378.
26. Houl JH, Yu W, Dudek SM, Hardin PE (2006) Drosophila CLOCK is constitutively expressed in circadian oscillator and non-oscillator cells. J Biol Rhythms 21:93-103.
27. Zhao J, et al. (2003) Drosophila clock can generate ectopic circadian clocks. Cell 113:755-766.
28. Lear BC, Zhang L, Allada R (2009) The neuropeptide PDF acts directly on evening pacemaker neurons to regulate multiple features of circadian behavior. PLoS Biol 7:e1000154.
29. Johard HA, et al. (2009) Peptidergic clock neurons in Drosophila: Ion transport peptide and short neuropeptide F in subsets of dorsal and ventral lateral neurons. J Comp Neurol 516:59-73.
30. Hewes RS, Park D, Gauthier SA, Schaefer AM, Taghert PH (2003) The bHLH protein Dimmed controls neuroendocrine cell differentiation in Drosophila. Development 130:1771-1781.
31. Park D, Taghert PH (2009) Peptidergic neurosecretory cells in insects: Organization and control by the bHLH protein DIMMED. Gen Comp Endocrinol 162:2-7.
32. Farooqui T (2007) Octopamine-mediated neuromodulation of insect senses. Neurochem Res 32:1511-1529.
33. Crocker A, Sehgal A (2008) Octopamine regulates sleep in drosophila through protein kinase A-dependent mechanisms. J Neurosci 28:9377-9385.
34. Sehgal A, et al. (1995) Rhythmic expression of timeless: A basis for promoting circadian cycles in period gene autoregulation. Science 270:808-810.
35. McDonald MJ, Rosbash M (2001) Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107:567-578.
36. Lee C, Bae K, Edery I (1998) The Drosophila CLOCK protein undergoes daily rhythms in abundance, phosphorylation, and interactions with the PER-TIM complex. Neuron 21:857-867.
37. Darlington TK, et al. (1998) Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science 280:1599-1603.
38. Claridge-Chang A, et al. (2001) Circadian regulation of gene expression systems in the Drosophila head. Neuron 32:657-671.
39. Ceriani MF, et al. (2002) Genome-wide expression analysis in Drosophila reveals genes controlling circadian behavior. J Neurosci 22:9305-9319.
40. Lin Y, et al. (2002) Influence of the period-dependent circadian clock on diurnal, circadian, and aperiodic gene expression in Drosophila melanogaster. Proc Natl Acad Sci USA 99:9562-9567.
41. Ueda HR, et al. (2002) Genome-wide transcriptional orchestration of circadian rhythms in Drosophila. J Biol Chem 277:14048-14052.
42. Keegan KP, Pradhan S, Wang JP, Allada R (2007) Meta-analysis of Drosophila circadian microarray studies identifies a novel set of rhythmically expressed genes. PLOS Comput Biol 3:e208.
43. Wijnen H, Naef F, Boothroyd C, Claridge-Chang A, Young MW (2006) Control of daily transcript oscillations in Drosophila by light and the circadian clock. PLoS Genet 2:e39.
44. Storch KF, et al. (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417:78-83.
45. Hughes ME, et al. (2009) Harmonics of circadian gene transcription in mammals. PLoS Genet 5:e1000442.
46. Yang S, Wang K, Valladares O, Hannenhalli S, Bucan M (2007) Genome-wide expression profiling and bioinformatics analysis of diurnally regulated genes in the mouse prefrontal cortex. Genome Biol 8:R247.
47. Kadener S, et al. (2006) Neurotoxic protein expression reveals connections between the circadian clock and mating behavior in Drosophila. Proc Natl Acad Sci USA 103:13537-13542.