Drosophila rhythms: From brain to behavior

Seminars in Cell and Developmental Biology

Volumn 7, Issue 6, 1996, Pages 791-802

  Helfrich Forster, Charlotte ^a  

^a Botanisches Institut   (Germany)

Author keywords

Activity; Eclosion; Insects; Period gene; Pigment dispersing hormone; Timeless gene

Indexed keywords

ARTHROPODA; DROSOPHILA MELANOGASTER; HEXAPODA; MELANOGASTER;

EID: 0001376796     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1006/scdb.1996.0097     Document Type: Article

References (110)

1. Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci USA 68:2112-2116
2. Hall JC (1995) Tripping along the trail to the molecular mechanisms of biological clocks. Trends Neurosci 18:230-240
3. Hardin P, Siwicki KK (1995) The multiple roles of per in the Drosophila circadian clock. Semin Neurosci 7:15-25
4. Goldbeter A (1995) A model for circadian oscillations in the Drosophila period protein (per). Proc R Soc Lond B: 261:319-324
5. Sehgal A, Price JL, Man B, Young MW (1994) Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science 263:1603-1606
6. Vosshall LB, Price JL, Seghal A, Saez L, Young MW (1994) Nuclear localization of period protein by a second clock mutation, timeless. Science 263:1606-1609
7. Myers MP, Wagner-Smith K, Wesley CS, Young MW, Sehgal S (1995) Positional cloning and sequence analysis of the Drosophila clock gene, timeless. Science 270:805-808
8. Price JL, Dembinska ME, Young MW, Rosbash M (1995) Suppression of period protein abundance and circadian cycling by the Drosophila clock mutation timeless. EMBO J 14:1044-1049
9. 1. Science 270:811-815
10. Seghal A, Rothenfluh-Hilfiker A, Hunter-Ensor M, Chen Y, Myers MP, Young MW (1995) Rhythmic expression of timeless: a basis for promoting circadian cycles in period gene autoregulation. Science 270:808-810
11. Seghal A (1995) Genetic dissection of the circadian clock: a timeless story. Semin Neurosci 7:27-35
12. Reppert SM, Sauman I (1995) period and timeless tango: a dance of two clock genes. Neuron 15:983-986
13. Hunter-Ensor M. Ousley A, Seghal A (1996) Regulation of the Drosophila protein timeless suggests a mechanism for resetting the circadian clock by light. Cell 84:677-685
14. Myers PM, Wagner-Smith K, Rothenfluh-Hilfiker A, Young MW (1996) Light-induced degradation of timeless and entrainment of the Drosophila circadian clock. Science 271:1736-1740
15. Lee C, Parikh V, Itsukaichi T, Bae K, Edery I (1996) Resetting the Drosophila clock by photic regulation of per and a per-tim complex. Science 271:1740-1744
16. Zeng H, Qian Z, Myers MP, Rosbash M (1996) A light-entrainment mechanism for the Drosophila circadian clock. Nature 380:129-135
17. Brandes C, Plautz JD, Stanewsky R, Jamison CF, Straume M, Wood KV, Kay SA, Hall JC (1996) Novel features of Drosophila period transcription revealed by real-time luciferase reporting. Neuron 16:687-692
18. Zeng H, Hardin PE, Rosbash M (1994) Constitutive overexpression of the Drosophila period protein inhibits period mRNA cycling. EMBO J 13: 3590-3598
19. 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
20. Siwicki KK, Hom EF, Bug B, Folwell MG, Noveral J (1995) The cellular rhythms of a Drosophila clock protein, in Nervous Systems and Behavior. Proc 4th Int Cong Neuroethology (Burrows M, Matheson T, Newland PL, Schuppe J, eds) p. 130. Thieme, Stuttgart
21. Hall JC, Kyriacou CP (1990) Genetics of biological rhythms in Drosophila. Adv Insect Physiol 22:221-298
22. Chen D-M, Christianson JS, Sapp RJ, Stark WS (1992) Visual receptor cycle in normal and period mutant Drosophila: microspectrophotometry, electrophysiology, and ultrastructural morphometry. Vis Neurosci 9:125-135
23. Meinertzhagen IA, Pyza E (1996) Daily rhythms in cells of the fly's optic lobe: taking time out from the circadian clock. Trends Neurosci 19:285-291
24. Allemand R (1976) Les rhythmes de vitellogenèse et d'ovulation en photopériode LD 12:12 de Drosophila melanogaster. J Insect Physiol 22:1031-1035
25. McCabe CJ, Birley AJ, Morgan E (1993) Oviposition in period mutants of Drosophila melanogaster. J Interdiscipl Cycle Res 24:224
26. Page TL (1985) Clocks and circadian rhythms. Comp Insect Physiol Biochem Pharmacol 6:557-653
27. Dowse HB, Hall JC, Ringo JM (1987) Circadian and ultradian rhythms in period mutants of Drosophila melanogaster. Behav Genet 17:19-35
28. Saunders DS, Heinrich VC, Gilbert LI (1989) Induction of diapause in Drosophila melanogaster. photoperiodic regulation and the impact of arrhythmic clock mutations on time measurement. Proc Natl Acad Sci USA 86:3748-3752
29. 0 mutant of Drosophila melanogaster. Z Naturforsch C 42:1335-1338
30. 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
31. Kimura Y, Masaki S (1993) Hourglass and oscillator expression of photoperiodic diapause response in the cabbage moth Mamestra brassicae. Physiol Entomol 18:240-246
32. Klein DC, Moore RY, Reppert SM (1991) Suprachiasmatic Nucleus. Oxford University Press, New York, Oxford
33. Siwicki KK, Eastman C, Petersen G, Rosbash M, Hall JC (1988) Antibodies to the period gene product of Drosophila reveal diverse distribution and rhythmic changes in the visual system. Neuron 1:141-150
34. Hardin PE (1994) Analysis of period mRNA cycling in Drosophila head and body tissues indicates that body oscillators behave differently than head oscillators. Molec Cell Biol 14:7211-7218
35. Konopka RJ, Kyriacou CP, Hall JC (1996) Mosaic analysis in the Drosophila CNS of circadian and courtship-song rhythms affected by a period clock mutation. J Neurogenet, in press
36. Konopka RJ, Wells S, Lee T (1983) Mosaic analysis of a Drosophila clock mutant. Molec Gen Genet 190:284-288
37. Cahill GM, Beharse JC (1995) Circadian rhythmicity in vertebrate retinas: regulation by a photoreceptor oscillator. Prog Retinal Res 14:267-291
38. Weber F (1995) Cyclic layer deposition in the cockroach (Blaberus craniifer) endocuticle: a circadian rhythm in leg pieces cultured in vitro. J Insect Physiol 41:153-161
39. Giebultowicz JM, Rieman JG, Raina AK, Ridgway RL (1989) Circadian system controlling release of sperm in the insect testes. Science 245:1098-1100
40. Giebultowicz JM, Hege D, Stanewsky R, Hall JC (1996) Rhythm of period protein expression in the malpighian tubules of Drosophila melanogaster; evidence for head-independent circadian clock. 5th meeting Soc Res Biol Rhythms: 87
41. Emery I, Noveral J, Jamison C, Siwicki KK (1996) The clock protein, period, cycles in prothoracic glands cultured in vitro, 5th meeting SRBR: 30
42. Helfrich C, Engelmann W (1983) Circadian rhythms of the locomotor activity rhythm in Drosophila melanogaster and its mutants 'sine oculis' and 'small optic lobes'. Physiol Entomol 8:257-272
43. Helfrich C (1986) Role of optic lobes in the regulation of locomotor activity rhythm in Drosophila melanogaster. behavioral analysis of neural mutants. J Neurogenet 3:321-343
44. 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
45. 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
46. Frisch B, Hardin PE, Hamblen-Coyle MJ, Rosbash MR, 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
47. Vosshall LB, Young MW (1995) Circadian rhythms in Drosophila can be driven by period expression in a restricted group of central brain cells. Neuron 15:345-360
48. Handler AM, Konopka RJ (1979) Transplantation of a circadian pacemaker in Drosophila. Nature 279:236-238
49. Konopka RJ, Wells S (1980) Drosophila clock mutations affect the morphology of a brain neurosecretory cell group. J Neurobiol 11:411-415
50. Helfrich C (1985) Untersuchungen über das circadiane System von Fliegen. PhD Thesis, Tübingen, Germany
51. Helfrich-Förster C (1991) Are neurosecretory cells involved in the circadian control of locomotor activity? In Chronobiology and Chronomedicine (Gutenbrunner C, Hildebrandt G, Moog R, eds) pp 134-140. Peter Lang, Frankfurt
52. 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
53. Helfrich-Förster C (1995) The period clock gene is expressed in CNS 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
54. Helfrich-Förster C, Homberg U (1993) Pigment-dispersing-hormone immunoreactive neurons in the nervous system of wildtype Drosophila melanogaster and of several mutants with altered circadian rhythmicity. J Comp Neurol 337:177-190
55. Helfrich-Förster C, Engelmann W (1995) The occurrence of clear rhythmic locomotor activity in individual disconnected mutants of Drosophila melanogaster is accompanied by the presence of lateral neurons in these flies. The Physiologist 38:6.2
56. Bennett MR, Schwartz WJ (1994) Are glia among the cells that express immunoreactive c-fos in the suprachiasmatic nucleus? Neuroreport 5:1737-1740
57. Prosser RA, Edgar DM, Heller HC, Miller JD (1994) A possible glial role in the mammalian circadian clock. Brain Res 643:296-301
58. Strecker GJ, Bouskila Y, Dudek FE (1995) Neurotransmission and electrophysiological mechanisms in the suprachiasmatic nucleus. Semin Neurosci 7:43-51
59. Barres BA (1991) New roles for glia. J Neurosci 11:3685-3694
60. Hatton GI (1988) Pituicytes, glia and control of terminal secretion. J Exp Biol 139:67-79
61. Engelmann W, Mack W (1978) Different oscillators control the circadian rhythm of eclosion and activity in Drosophila. J Comp Physiol A 127:229-237
62. Newby LM, Jackson FR (1991) Drosophila ebony mutants have altered circadian activity rhythms but normal eclosion rhythms. J Neurogenet 7:85-101
63. Newby LM, Jackson FR (1993) A new biological rhythm mutant of Drosophila melanogaster that identifies a gene with an essential embryonic function. Genetics 135:1077-1090
64. Jackson FR (1993) Circadian rhythm mutants of Drosophila, in Molecular Genetics of Biological Rhythms (Young MW, ed) pp 91-121. Marcel Dekker Inc, New York, Basel, Hong Kong
65. Sawin EP, Dowse HB, Hamblen-Coyle MJ, Hall JC, Sokolowski MB (1994) A lack of locomotor activity rhythms in Drosophila melanogaster larvae (Diptera: Drosophilidae). J Insect Behav 7:349-262
66. Brett WJ (1955) Persistent diurnal rhythmicity in Drosophila emergence. Ann Entomol Soc America 48:119-131
67. Zimmerman WF, Ives D (1971) Some photophysiological aspects of circadian rhythmicity in Drosophila, in Proc Symp Biochronometry (Menaker M, ed.) pp 381-391. Natl Acad Sci, Washington
68. Seghal A, Price J, Young MW (1992) Ontogeny of a biological clock in Drosophila melanogaster. Proc Natl Acad Sci USA 89:1423-1427
69. Helfrich-Förster C (1995) Development of presumptive circadian pacemaker neurons in the brain of Drosophila melanogaster, in Göttingen Neurobiology Report, VoI II (Elsner N, Menzel R, eds) pp 596. Thieme, Stuttgart, New York
70. Engelmann W, Honegger HW (1966) Tagesperiodische Schlüpfrhythmik einer augenlosen Drosophila melanogaster Mutante. Naturwissenschaften 53:588
71. Truman JW (1976) Extraretinal photoreception in insects. Photochem Photobiol 23:215-225
72. Pollock JA, Benzer S (1988) Transcript localization of four opsin genes in the three visual organs of Drosophila; RH2 is ocellus specific. Nature 333:779-782
73. Truman JW (1972) Physiology of insect rhythms. II. The silkmoth brain as the location of the biological clock controlling eclosion. J Comp Physiol A 81:99-114
74. Hofbauer A, Buchner E (1989) Does Drosophila have seven eyes? Naturwissenschaften 76:335-336
75. Blaschke I, Lang P, Hofbauer A, Engelmann W, Helfrich-Förster C (1996) Preliminary action spectra suggest that the clock cells of Drosophila are synchronized to the external LD-cycle by the compound eyes plus extraretinal photoreceptors, in Brain and Evolution (Elsner N, Schnitzler H-U, eds) p 30. Thieme, Stuttgart, New York
76. Hagberg M (1986) Ultrastructure and central projections of extraocular photoreceptors in caddiesflies (Insecta:Trichoptera). Cell Tiss Res 245:643-648
77. Seifert P, Smola U, Schinko I (1987) Internal extraocular photoreceptors in a dipteran insect. Tissue Cell 19:111-118
78. Schulz W-D, Schlüter U, Seifert G (1984) Extraocular photoreceptors in the brain of Epilachna varivestis (Coleoptera, Coccinellidae). Cell Tissues Res 236:317-320
79. Fleissner G, Fleissner G, Frisch B (1993) A new type of putative non-visual photoreceptors in the optic lobe of beetles. Cell Tissue Res 273:435-445
80. Foster RG, Garcia-Fernandez JM, Provencio I, DeGrip WJ (1993) Opsin localization and chromophore retinoids identified within the basal brain of the lizard Anolis carolinensis. J Comp Physiol A 172:33-45
81. Garcia-Fernandez JM, Foster RG (1994) Immunocytochemical identification of photoreceptor proteins in hypothalamic cerebrospinal fluid-contacting neurons of the larval lamprey. Cell Tissue Res 275:319-326
82. Sandeman DC, Sandeman RE, de Couet HG (1990) Extraretinal photoreceptors in the brain of the crayfish Cherax destructor. J Neurobiol 21:619-629
83. Thompson KSJ, Bacon JP (1991) The vasopressin-like immunoreactive (VPLI) neurons of the locust, Locusta migratoria. II. Physiology. J Comp Physiol A 168:619-630
84. Cymborowski B, Korf H-W (1995) Immunocytochemical demonstration of S-antigen (arrestin) in the brain of the blowfly Calliphora vicina. Cell Tissue Res 279:109-114
85. Cymborowski B, Hong S-F, McWatters HG, Saunders DS (1996) S-antigen antibody partially blocks entrainment and the effects of constant light on the circadian rhythm of locomotor activity in the adult blow fly, Calliphora vicina. J Biol Rhythms 11:68-74
86. Van Gelder RN, Bae I, Palazzolo MJ, Krasnow MA (1995) Extent and character of circadian gene expression in Drosophila melanogaster. identification of twenty oscillating mRNAs in the fly head. Curr Biol 5: 1424-1436
87. Homberg U (1994) Distribution of neurotransmitters in the insect brain. Progress in Zoology Volume 40. Gustav Fischer, Stuttgart, Jena, New York
88. Nässel DR (1993) Neuropeptides in the insect brain: a review. Cell Tissue Res 273:1-29
89. Wulf J, de Belle JS, Helfrich-Förster C (1996) Do mushroom bodies mediate circadian locomotor activity rhythms in Drosophila? in Brain and Evolution (Elsner N, Schnitzler H-U, eds) p 29. Thieme, Stuttgart, New York
90. Silver R, LeSauter J (1993) Efferent signals of the suprachiasmatic nucleus. J Biol Rhythms 8:S89-S92
91. Pyza E, Meinertzhagen IA (1996) Neurotransmitters regulate rhythmic size changes amongst cells in the fly's optic lobe. J Comp Physiol A 178:33-45
92. Arechiga H, Fernández-Quirós F, de Miguel FF, Rodrìguez-Sosa L (1993) The circadian system of crustaceans. Chronobiol Int 10:1-19
93. Mangerich S, Keller R, Dircksen H, Rao KR, Riehm JP (1987) Immunocytochemical localization of pigment-dispersing hormone (PDH) and its coexistence with FMRFamide-immunoreactive material in the eyestalks of the decapod crustaceans Carcinus maenas and Orconectes limosus. Cell Tiss Res 250:365-375
94. Nußbaum T, Dircksen H (1995) Neuronal pathways of classical crustacean neurohormones in the central nervous system of the woodlouse, Oniscus asellus (L.). Phil Trans R Soc Lond B 347:139-154
95. Mangerich S, Keller R (1988) Localization of pigment-dispersing hormone (PDH) Immunoreactivity in the central nervous system of Carcinus maenas and Orconectes limosus (Crustacea), with reference to FMRFamide immunoreactivity in O. limosus. Cell Tiss Res 253:199-208
96. Fleissner G, Fleissner G (1988) Efferent control of visual sensitivity in arthropod eyes: With emphasis on circadian rhythms, in Information Processing in Animals, Vol 5 (Lindauer M, ed). Fischer, Stuttgart, New York
97. Kass L, Barlow RB (1992) A circadian clock in the Limulus brain transmits synchronous efferent signals to all eyes. Vis Neurosci 9:493-504
98. Homberg U, Würden S, Dircksen H, Rao KR (1991) Comparative anatomy of pigment-dispersing hormone-immunoreactive neurons in the brain of orthopteroid insects. Cell Tiss Res 266:343-357
99. Stengl M, Homberg U (1994) Pigment-dispersing hormone-immunoreactive neurons in the cockroach Leucophaea maderae share properties with circadian pacemaker neurons. J Comp Physiol A 175:203-213
100. Stengl M (1995) Pigment-dispersing hormone-immunoreactive fibers persist in crickets which remain rhythmic after bilateral transaction of the optic stalks. J Comp Physiol A:217-228
101. Petri B, Stengl M (1996) Is pigment-dispersing hormone a component of the circadian system of Leucophaea maderae? in Brain and Evolution (Elsner N, Schnitzler H-U, eds) p 28. Thieme, Stuttgart, New York
102. Fleissner G (1982) Isolation of a circadian clock. J Comp Physiol A 149:311-316
103. Frisch B, Fleissner G, Fleissner G, Brandes C, Hall JC (1996) Staining in the brain of Pachymorpha sexguttata mediated by an antibody against a Drosophila clock-gene product: labeling of cells with possible importance for the beetle's circadian system. Cell Tiss Res, in press
104. Fleissner G, Fleissner G (1991) Ein Konzept der circadianen Organisation von Arthropoden and Beispiel von Struktur und Funktion neuronaler Elemente im optischen System von Skorpion und Käfer. Verh Dtsch Zool Ges 85:109
105. Homberg U, Prakash N (1996) Development of pigment-dispersing-hormone-like immunoreactivity in the brain of the locust Schistocerca gregaria: comparison with immunostaining for urotensin I and Mas-allatotropin. Cell Tiss Res, in press
106. Reppert SM, Tsai T, Roca AL, Sauman I (1994) Cloning of a structural and functional homologue of the circadian clock gene period from the giant silkmoth Antheraea pernyi. Neuron 13:1167-1176
107. Levine JD, Sauman I, Imbalzano M, Reppert SM, Jackson FR (1995) Period protein from the giant silkmoth Antheraea pernyi functions as a circadian clock element in Drosophila melanogaster. Neuron 15:147-157
108. Homberg U, Davis NT, Hildebrand JG (1991) Peptide-immunocytochemistry of neurosecretory cells in the brain and retrocerebral complex of the sphinx moth Manduca sexta. J Comp Neurol 303:235-252
109. Helfrich C, Cymborowski B, Engelmann W (1985) Circadian activity rhythm of the house fly continues after optic tract severance and lobectomy. Chronobiol Int 2:19-32
110. Cymborowski B, Lewis RD, Hong S-F, Saunders DS (1994) Circadian locomotor activity rhythms and their entrainment to light-dark cycles continue in flies (Calliphora vicinia) surgically deprived of their optic lobes. J Insect Physiol 40:501-510