Disruption of synaptic transmission or clock-gene-product oscillations in circadian pacemaker cells of Drosophila cause abnormal behavioral rhythms

Journal of Neurobiology

Volumn 43, Issue 3, 2000, Pages 207-233

  Kaneko, Maki ^a,b   Park, Jae H ^a,c   Cheng, Yuzhong ^b,d   Hardin, Paul E ^b   Hall, Jeffrey C ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b University of Houston   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Brain neurons; Clock genes; Locomotor behavior; Luciferase reporting; Neuropeptide; Tetanus toxin

Indexed keywords

LUCIFERASE; NEUROPEPTIDE; TETANUS TOXIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOLUMINESCENCE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DROSOPHILA; FEEDBACK SYSTEM; GENE DISRUPTION; GENE SEQUENCE; LIGHT DARK CYCLE; NONHUMAN; OSCILLATION; PACEMAKER NERVE CELL; PRIORITY JOURNAL; PROMOTER REGION; SYNAPTIC TRANSMISSION;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL CLOCKS; BRAIN; CELL CYCLE; CIRCADIAN RHYTHM; DROSOPHILA; DROSOPHILA PROTEINS; IMMUNOHISTOCHEMISTRY; INSECT PROTEINS; METALLOENDOPEPTIDASES; MOTOR ACTIVITY; NEURONS; NEUROPEPTIDES; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); SYNAPTIC TRANSMISSION; TETANUS TOXIN; TIME FACTORS;

EID: 0034608506     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(20000605)43:3<207::AID-NEU1>3.0.CO;2-0     Document Type: Article

References (89)

1. Allen MJ, Shan X, Caruccio P, Froggett SJ, Moffat KG, Murphey RK. 1999. Targeted expression of truncated Glued disrupts giant fiber synapse formation in Drosophila. J Neurosci 19:9374-9384.
2. Aronson BD, Johnson KA, Loros JJ, Dunlap JC. 1994. Negative feedback defining a circadian clock: autoregulation of the clock gene frequency. Science 263:1578-1584.
3. Bae K, Lee C, Sidote D, Chuang K-Y, Edery I. 1998. Circadian regulation of a Drosophila homolog of the mammalian Clock gene: PER and TIM function as positive regulators. Mol Cell Biol 18:6142-6151.
4. Baines RA, Robinson SG, Fujioka M, Jaynes JB, Bate M. 1999. Postsynaptic expression of tetanus toxin light chain blocks synaptogenesis in Drosophila. Curr Biol 9:1267-1270.
5. Batschelet E. 1965. Statistical Methods for the Analysis of Problems in Animal Orientation and Certain Biological Rhythms. An AIBS Monograph. Washington, DC: The American Institute of Biological Sciences. 57 p.
6. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
7. Cagan RL, Ready DF. 1989. The emergence of order in the Drosophila pupal retina. Dev Biol 136:346-362.
8. Cheng Y, Gvakharia B, Hardin PE. 1998. Two alternatively spliced transcripts from the Drosophila period gene rescue rhythms having different molecular and behavioral characteristics. Mol Cell Biol 18:6505-6514.
9. Cheng Y, Hardin PE. 1998. Drosophila photoreceptors contain an autonomous circadian oscillator that can function without period mRNA cycling. J Neurosci 18:741-750.
10. Citri Y, Colot HV, Jacquier AC, Yu Q, Hall JC, Baltimore D, Rosbash M. 1987. A family of unusually spliced biologically active transcripts encoded by a Drosophila clock gene. Nature 326:42-47.
11. Darlington TK, Wager-Smith K, Ceriani MF, Staknis D, Gekakis N, Steeves TDL, Weitz CJ, Takahashi JS, Kay SA. 1998. Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science 280:1599-1603.
12. Dayanithi G, Stecher B, Höhne-Zell B, Yamasaki S, Binz T, Weller U, Niemann H, Gratzl M. 1994. Exploring the functional domain and the target of the tetanus toxin light chain in neurohypophysial terminals. Neuroscience 58: 423-431.
13. deBelle JS, Heisenberg M. 1994. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692-695.
14. Dunlap JC. 1999. Molecular bases for circadian clocks. Cell 96:271-290.
15. Dunlap JC, Loros JJ, Liu Y, Crosthwaite SK. 1999. Eukaryotic circadian systems: cycles in common. Genes Cells 4:1-10.
16. Dushay MS, Rosbash M, Hall JC. 1989. The disconnected visual system mutations in Drosophila melanogaster drastically disrupt circadian rhythms. J Biol Rhythms 4:1-27.
17. Emery P, So WV, Kaneko M, Hall JC, 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.
18. 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.
19. Fisher NI. 1993. Statistical Analysis of Circular Data. Cambridge: Cambridge University Press. 277 p.
20. 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.
21. Giebultovicz JM, Stanewsky R, Hall JC, Hege DM. 2000. Transplanted Drosophila excretory tubules maintain circadian clock cycling out of phase with the host. Curr Biol 10:107-110.
22. Glossop NRJ, Lyons LC, Hardin PE. 1999. Interlocked feedback loops within the Drosophila circadian oscillator. Science 286:766-768.
23. Hall JC. 1995. Tripping along the trail to the molecular mechanisms of biological clocks. Trends Neurosci 18: 230-240.
24. - mutants. J Neurogenet 3:249-291.
25. Hamblen MJ, White NE, Emery PTJ, Kaiser K, Hall JC. 1998. Molecular and behavioral analysis of four period mutants in Drosophila melanogaster encompassing extreme short, novel long, and unorthodox arrhythmic types. Genetics 149:165-178.
26. Hamblen-Coyle M, Konopka RJ, Zwiebel LJ, Colot HV, Dowse HB, Rosbash M, Hall JC. 1989. A new mutation at the period locus of Drosophila melanogaster with some novel effects on circadian rhythms. J Neurogenet 5:229-256.
27. Hamblen-Coyle MJ, Wheeler DA, Rutila JE, Rosbash M, Hall JC. 1992. Behavior of period-altered circadian rhythm mutants of Drosophila in light: dark cycles. J Insect Behav 5:417-446.
28. Handler AM, Konopka RJ. 1979. Transplantation of a circadian pacemaker in Drosophila. Nature 279:236-238.
29. Hardin PE. 1998. Activating inhibitors and inhibiting activators: a day in the life of a fly. Curr Opin Neurobiol 8:642-647.
30. Hardin PE, Hall JC, Rosbash M. 1990. Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343:536-540.
31. Hardin PE, Hall JC, Rosbash M. 1992. Behavioral and molecular analyses suggest that circadian output is disrupted by disconnected mutants in D. melanogaster. EMBO J 11:1-6.
32. Hardin P, Siwicki KK. 1995. The multiple roles of per in the Drosophila circadian clock. Semin Neurosci 7:15-25.
33. Heimbeck G, Bugnon V, Gendre N, Häberlin C, Stocker RF. 1999. Smell and taste perception in Drosophila melanogaster larva: toxin expression studies in chemosensory neurons. J Neurosci 19:6599-6609.
34. 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.
35. Helfrich-Förster C. 1996. Drosophila rhythms: from brain to behavior. Semin Cell Dev Biol 7:791-802.
36. Helfrich-Förster C. 1998. Robust circadian rhythmicity of Drosophila melanogaster requires the presence of lateral neurons: brain-behavioral study of disconnected mutants. J Comp Physiol A 182:435-453.
37. Helfrich-Förster C, Stengl M, Homberg U. 1998. Organization of the circadian system in insects. Chronobiol Internat 15:567-594.
38. Hidalgo A, Urban J, Brand AH. 1995. Targeted ablation of glia disrupts axon tract formation in the Drosophila CNS. Development 121:3703-3712.
39. Hiesinger PR, Reiter C, Schau H, Fischbach K-F. 1999. Neuopil pattern formation and regulation of cell adhesion molecules in Drosophila optic lobe development depend on synapobrevin. J Neurosci 19:7448-7556.
40. Hunter-Ensor M, Ousley A, Sehgal A. 1996. Regulation of the Drosophila protein timeless suggests a mechanism for resetting the circadian clock by light. Cell 84:677-685.
41. Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D. 1997. The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124:761-771.
42. Johnson RL, Grenier JK, Scott MP. 1995. patched overexpression alters wing disc size and pattern: transcriptional and post-transcriptional effects on hedgehog targets. Development 121:4161-4170.
43. Kaiser K. 1993. Second generation enhancer traps. Curr Biol 3:560-562.
44. Kalb JM, DiBenetto AJ, Wolfner MF. 1993. Probing the function of Drosophila melanogaster accessory glands by directed cell ablation. Proc Natl Acad Sci USA 90:8093-8097.
45. Kaneko M. 1998. Neural substrates of Drosophila rhythms revealed by mutants and molecular manipulations. Curr Opin Neurobiol 8:652-658.
46. 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.
47. Short mutation on phase shifts induced by light pulses delivered to Drosophila larvae. J Biol Rhythms 15:43-60.
48. Kaneko M, Helfrich-Förster C, Hall JC. 1997. 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.
49. Kuwada J, Goodman CS. 1985. Neuronal determination during embryonic development of the grasshopper nervous system. Dev Biol 110:114-126.
50. 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.
51. Liu X, Lorenz L, Yu Q, Hall JC, Rosbash M. 1988. Spatial and temporal expression of the period gene in Drosophila melanogasler. Genes Dev 2:228-238.
52. Martin J-R, Ernest R, Heisenberg M. 1998. Mushroom bodies suppress locomotor activity in Drosophila melanogaster. Learn Mem 5:179-191.
53. Martin J-R, Raabe T, Heisenberg M. 1999. Central complex substructures are required for the maintenance of locomotor activity in Drosophila melanogaster. J Comp Physiol A 185:277-288.
54. Martin TFJ. 1994. The molecular machinery for fast and slow neurosecretion. Curr Opin Neurobiol 4:626-632.
55. ril lengthens circadian period in a temperature-dependent manner through suppression of PERIOD protein cycling and nuclear localization. Mol Cell Biol 19:4343-4354.
56. McNabb SL, Baker JD, Agapite J, Steller H, Roddiford LM, Truman JW. 1997. Disruption of a behavioral sequence by targeted death of peptidergic neurons in Drosophila. Neuron 19:813-823.
57. Morimura S, Maves L, Chen Y, Hoffmann FM. 1996. dicapentaplegic overexpression affects Drosophila wing and leg imaginal disc development and wingless expression. Dev Biol 177:136-151.
58. Myers MP, Wager-Smith K, Rothenfluh-Hilfiker A, Young MW. 1996. Light-induced degradation of TIMELESS and entrainment of the Drosophila circadian clock. Science 271:1736-1740.
59. Park JH, Hall JC. 1998. Isolation and chronobiological analysis of a neuropeptide pigment-dispersing factor gene in Drosophila melanogaster. J Biol Rhythms 13:219-228.
60. Park JH, Helfrich-Förster 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 USA 97:3608-3613.
61. Plautz JD, Kaneko M, Hall JC, Kay SA. 1997a. Independent photoreceptive circadian clocks throughout Drosophila. Science 278:1632-1635.
62. Plautz JD, Straume M, Stanewsky R, Jamison CF, Brandes C, Dowse HB, Hall JC, Kay SA. 1997b. Quantitative analysis of Drosophila period gene transcription in living animals. J Biol Rhythms 12:204-217.
63. Reddy S, Jin P, Trimarchi J, Caruccio P, Phillis R, Murphey RK. 1997. Mutant molecular motors disrupt neural circuits in Drosophila. J Neurobiol 33:711-723.
64. 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 99:791-802.
65. Saez L, Young MW. 1988. In situ localization of the per clock protein during development of Drosophila melanogaster. Mol Cell Biol 8:5378-5385.
66. Siwicki KK, Eastman C, Petersen G, Rosbash M, Hall JC. 1988. Antibodies to the period gene product of Drosophila reveal diverse tissue distribution and rhythmic changes in the visual system. Neuron 1:141-150.
67. Smith H. 1989. Pattern regulation during the development of the ventral abdomen in the flesh fly Sarcophaga agryostoma. Development 105:335-342.
68. Smith RF, Konopka RJ. 1982. Effects of dosage alterations at the per locus on the period of the circadian clock of Drosophila. Mol Gen Genet 185:30-36.
69. Sokal RR, Rohlf FJ. 1995. Biometry. 3rd ed. New York: W. H. Freeman and Co. 887 p.
70. Sokolove PG, Bushnell WN. 1978. The chi square periodogram: its utility for analysis of circadian rhythms. J Theor Biol 72:131-160.
71. Stanewsky R, Frisch B, Brandes C, Hamblen-Coyle MJ, Rosbash M, Hall JC. 1997a. Temporal and spatial expression patterns of transgenes containing increasing amounts of the Drosophila clock gene period and a lacZ reporter: mapping elements of the PER protein involved in circadian cycling. J Neurosci 17:676-696.
72. Stanewsky R, Jamison CF, Plautz JD, Kay SA, Hall JC. 1997b. Multiple circadian-regulated elements contribute to cycling period gene expression in Drosophila. EMBO J 16:5006-5018.
73. b mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95:681-692.
74. Strauss R, Heisenberg M. 1993. A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13:1852-1861.
75. Stoker RF, Heimbeck G, Gendre N, de Belle JS. 1997. Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J Neurobiol 32:443-456.
76. Sweeny ST, Broadie K, Keane J, Niemann H, O'Kane CJ. 1995. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14:341-351.
77. Tissot M, Gendre N, Stocker RF. 1998. Drosophila P[Gal4] lines reveal that motor neurons involved in feeding persist through metamorphosis. J Neurobiol 37:237-250.
78. Watson GS. 1983. Statistics on Spheres. New York: Wiley. 238 p.
79. Wheeler DA, Hamblen-Coyle MJ, Dushay MS, Hall JC. 1993. Behavior in light-dark cycles of Drosophila mutants that are arrhythmic, blind, or both. J Biol Rhythms 8:67-94.
80. Whim MD, Niemann H, Kaczmarek LK. 1997. The secretion of classical and peptide cotransmitters from a single presynaptic neuron involves a synaptobrevin-like molecule. J Neurosci 17:2338-2347.
81. White K, Tahaoglu E, Steller H. 1996. Cell killing by the Drosophila gene reaper. Science 271:805-807.
82. Whitmore D, Sassone-Corsi P, Foulkes NS. 1998. PASting together the mammalian clock. Curr Opin Neurobiol 8:635-641.
83. Wilsbacher LD, Takahashi JS. 1998. Circadian rhythms: molecular basis of the clock. Curr Opin Genet Dev 8:595-602.
84. Wilson C, Bellen HJ, Gehring WJ. 1990. Position effects on eukaryotic gene expression. Annu Rev Cell Biol 6:679-714.
85. Young MW. 1998. The molecular control of circadian behavioral rhythms and their entrainment in Drosophila. Annu Rev Biochem 67:135-152.
86. Zeng H, Hardin PE, Rosbash M. 1994. Constitutive overexpression of the Drosophila period protein inhibits period mRNA cycling. EMBO J 13:3590-3598.
87. Zeng H, Qian Z, Myers MP, Rosbash M. 1996. A light-entrainment mechanism for the Drosophila circadian clock. Nature 380:129-135.
88. Zerr DM, Hall JC, Rosbash M, Siwicki KK. 1990. Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J Neurosci 10:2749-2762.
89. Zhou L, Schnitzler A, Agapite J, Schwartz LM, Steller H, Nambu JR. 1997. Cooperative functions of the reaper and head involution defective genes in the programmed cell death of Drosophila central nervous system midline cells. Proc Natl Acad Sci USA 94:5131-5136.