Development and morphology of the clock-gene-expreasing lateral neurons of Drosophila melanogaster

Journal of Comparative Neurology

Volumn 500, Issue 1, 2007, Pages 47-70

  Helfrich Förster, Charlotte ^a   Shafer, Orie T ^b   Wülbeck, Corinna ^a   Grieshaber, Eva ^a   Rieger, Dirk ^a   Taghert, Paul ^b  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Accessory medulla; Circadian clock; Immunohistochemistry; PDF; PER

Indexed keywords

ACCESSORY NERVE; ARTICLE; CELL MIGRATION; CIRCADIAN RHYTHM; CLOCK GENE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE; GENE EXPRESSION; INSECT DEVELOPMENT; LOCOMOTION; MEDULLA OBLONGATA; METAMORPHOSIS; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROPIL; NONHUMAN; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AGE FACTORS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BRAIN; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; NEURAL PATHWAYS; NEURONS; NEUROPEPTIDES; TRANSCRIPTION FACTORS;

EID: 33845397569     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21146     Document Type: Article

References (95)

1. Blanchardon E, Grima B, Klarsfeld A, Chelot E, Hardin PE, Preat T, Rouyer F. 2001. Defining the role of Drosophila lateral neurons in the control of circadian rhythms in motor activity and eclosion by targeted genetic ablation and PERIOD protein overexpression. Eur J Neurosci 13:871-888.
2. Dircksen H. 1992. Fine structure of the neurohemal sinus gland of the shore crab, Carcinus maenas, and immuno-electron-microscopic identification of neurosecretory endings according to their neuropeptide contents. Cell Tissue Res 269:249-266.
3. Dircksen H, Zahnow CA, Gaus G, Keller R, Rao KR, Riehm JP. 1987. The ultrastructure of nerve endings containing pigment-dispersing hormone (PDH) in crustacean sinus glands: identification by an antiserum against a synthetic PDH. Cell Tissue Res 250:377-387.
4. Emery P, Stanewsky R, Helfrich-Förster C, Emery-Le M, Hall JC, Rosbash M. 2000. Drosophila CRY is a deep brain circadian photoreceptor. Neuron 26:493-504.
5. Estes PS, Ho GL, Narayanan R, Ramaswami M. 2000. Synaptic localization and restricted diffusion of a Drosophila neuronal synaptobrevin-green fluorescent protein chimera in vivo. J Neurogenet 13:233-255.
6. 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.
7. Fingerman SW, Fingerman M. 1977. Circadian variation in the levels of red pigment-dispersing hormone and 5-hydroxytryptamine in the eye-stalks of the fiddler crab, Uca pugilator. Comp Biochem Physiol C56:5-8.
8. Fischbach K-F, Heisenberg M. 1984. Neurogenetics and behaviour in insects. J Exp Biol 112:65-93.
9. Freeman M. 1996. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87:651-660.
10. 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.
11. Grima B, Chelot 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.
12. Hall JC. 2005. Systems approaches to biological rhythms in Drosophila. Methods Enzymol 393:61-185.
13. Hamanaka Y, Yasuyama K, Numata H, Shiga S. 2005. Synaptic connections between pigment-dispersing factor-immunoreactive neurons and neurons in the pars lateralis of the blow fly Protophormia terraenovae. J Comp Neurol 491:390-399.
14. Hamasaka Y, Nässel DR. 2006. Mapping of serotonin, dopamine, and histamine in relation to different clock neurons in the brain of Drosophila. J Comp Neurol 494:314-330.
15. B receptors and decreases in calcium. J Neurobiol 65:225-240.
16. Hardin PE. 2004. Transcription regulation within the circadian clock: the E-box and beyond. J Biol Rhythms 19:348-360.
17. Hardin PE. 2005. The circadian timekeeping system of Drosophila. Curr Biol 15:R714-R722.
18. Heilig JS, Freeman M, Laverty T, Lee KJ, Campos AR, Rubin GM, Steller H. 1991. Isolation and characterization of the disconnected gene of Drosophila melanogaster. EMBO J 10:809-815.
19. Helfrich C. 1986. Role of the optic lobes in the regulation of the locomotor activity rhythm of Drosophila melanogaster: behavioral analysis of neural mutants. J Neurogenet 3:321-343.
20. Helfrich-Förster C. 1997. Development of pigment-dispersing hormone-immunoreactive neurons in the nervous system of Drosophila melanogaster. J Comp Neurol 380:335-354.
21. 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 A182:435-453.
22. Helfrich-Förster C. 2003. The neuroarchitecture of the circadian clock in the brain of Drosophila melanogaster. Microsc Res Techniq 62:94-102.
23. Helfrich-Förster C. 2004. The circadian clock in the brain: a structural and functional comparison between mammals and insects. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:601-613.
24. Helfrich-Förster C. 2005. Neurobiology of the fruit fly's circadian clock. Genes Brain Behav 4:65-76.
25. Helfrich-Förster C. 2006. Immunohistochemistry in Drosophila, sections and whole mount. In: Rosato E, editors. Methods in molecular biology. Totowa, NJ: Humana Press Inc. (in press).
26. Helfrich-Förster C, Homberg U. 1993. Pigment-dispersing hormone-immunoreactive neurons in the nervous system of wild-type Drosophila melanogaster and of several mutants with altered circadian rhythmicity. J Comp Neurol 337:177-190.
27. 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.
28. Helfrich-Förster C, Edwards T, Yasuyama K, Wisotzki B, Schneuwly S, Stanewsky R, Meinertzhagen IA, Hofbauer A. 2002. The extraretinal eyelet of Drosophila: development, ultrastructure, and putative circadian function. J Neurosci 22:9255-9266.
29. Hewes RS, Schaefer AM, Taghert PH. 2000. The cryptocephal gene (ATF4) encodes multiple basic-leucine zipper proteins controlling molting and metamorphosis in Drosophila. Genetics 155:1711-23.
30. Hinton CW. 1955. The behavior of an unstable ring chromosome of Drosophila melanogaster. Genetics 40:951-961.
31. Hofbauer A. 1991. Eine Bibliothek monoclonaler Antikörper gegen das Gehirn von Drosophila melanogaster. Habilitation thesis, University of Würzburg, Würzburg, Germany.
32. Homberg U, Reischig T, Stengl M. 2003. Neural organization of the circadian system of the cockroach Leucophaea maderae. Chronobiol Int 20:577-591.
33. Hyun S, Lee Y, Hong ST, Bang S, Paik D, Kang J, Shin J, Lee J, Jeon K, Hwang S, Bae E, Kim J. 2005. Drosophila GPCR Han is a receptor for the circadian clock neuropeptide PDF. Neuron 48:267-278.
34. Ito K, Suzuki K, Estes P, Ramaswami M, Yamamoto D, Strausfeld NJ. 1998. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem 5:52-77.
35. 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.
36. 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.
37. Kaneko M, Park JH, Cheng Y, Hardin PE, Hall JC. 2000. Disruption of synaptic transmission or clock-gene-product oscillations in circadian pacemaker cells of Drosophila cause abnormal behavioral rhythms. J Neurobiol 43:207-233.
38. Klarsfeld A, Malpel S, Michard-Vanhee C, Picot M, Chelot E, Rouyer F. 2004. Novel features of cryptochrome-mediated photoreception in the brain circadian clock of Drosophila. J Neurosci 24:1468-1477.
39. Lear BC, Merrill CE, Lin JM, Schroeder A, Zhang L, Allada R. 2005. A G protein-coupled receptor, groom-of-PDF, is required for PDF neuron action in circadian behavior. Neuron 48:221-227.
40. Lee KJ, Freeman M, Steller H. 1991. Expression of the disconnected gene during development of Drosophila melanogaster. EMBO J 10:817-826.
41. 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.
42. Linial M. 1997. SNARE proteins - why so many, why so few? J Neurochem 69:1781-1792.
43. Malpel S, Klarsfeld A, Rouyer F. 2002. Larval optic nerve and adult extra-retinal photoreceptors sequentially associate with clock neurons during Drosophila brain development. Development 129:1443-1453.
44. Mazzoni EO, Desplan C, Blau J. 2005. Circadian pacemaker neurons transmit and modulate visual information to control a rapid behavioral response. Neuron 45:293-300.
45. 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.
46. Meinertzhagen IA, Pyza E. 1999. Neurotransmitter regulation of circadian structural changes in the fly's visual system. Microsc Res Tech 45:96-105.
47. Mertens I, Vandingenen A, Johnson EC, Shafer OT, Li W, Trigg JS, De Loof A, Schoofs L, Taghert PH. 2005. PDF receptor signaling in Drosophila contributes to both circadian and geotactic behaviors. Neuron 48:213-219.
48. Miskiewicz K, Pyza E, Schürmann FW. 2004. Ultrastructural characteristics of circadian pacemaker neurones, immunoreactive to an antibody against a pigment-dispersing hormone in the fly's brain. Neurosci Lett 363:73-77.
49. Moore RY, Speh JC, Leak RK. 2002. Suprachiasmatic nucleus organization. Cell Tissue Res 309:89-98.
50. Morales J, Hiesinger PR, Schroeder AJ, Kume K, Verstreken P, Jackson FR, Nelson DL, Hassan BA. 2002. Drosophila fragile X protein, DFXR, regulates neuronal morphology and function in the brain. Neuron 34:961-972.
51. Nitabach MN, Blau J, Holmes TC. 2002. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109:485-495.
52. Page TL. 1978. Interactions between bilaterally paired components of the cockroach circadian system. J Comp Physiol 124:225-236.
53. Page TL, Caldarola PC, Pittendrigh CS. 1977. Mutual entrainment of bilaterally distributed circadian pacemaker. Proc Natl Acad Sci U S A 74:1277-1281.
54. Park D, Griffith LC. 2006. Electrophysiological and anatomical characterization of PDF-positive clock neurons in the intact adult Drosophila brain. J Neurophysiol 95:3955-3960.
55. 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 U S A 97:3608-3613.
56. Peng Y, Stoleru D, Levine JD, Hall JC, Rosbash M. 2003. Drosophila free-running rhythms require intercellular communication. PLoS Biol 1:E13.
57. Petri B, Stengl M. 1997. Pigment-dispersing hormone shifts the phase of the circadian pacemaker of the cockroach Leucophaea maderae. J Neurosci 17:4087-4093.
58. Petri B, Stengl M, Würden S, Homberg U. 1995. Immunocytochemical characterization of the accessory medulla in the cockroach Leucophaea maderae. Cell Tissue Res 282:3-19.
59. Pyza E. 2002. Dynamic structural changes of synaptic contacts in the visual system of insects. Microsc Res Techniq 58:335-344.
60. Pyza E, Meinertzhagen IA. 1993. Daily and circadian rhythms of synaptic frequency in the first visual neuropile of the housefly's (Musca domestica L.) optic lobe. Proc Biol Sci 254:97-105.
61. Pyza E, Meinertzhagen IA. 1995. Monopolar cell axons in the first optic neuropil of the housefly, Musca domestica L., undergo daily fluctuations in diameter that have a circadian basis. J Neurosci 15:407-418.
62. Pyza E, Meinertzhagen IA. 1997a. Circadian rhythms in screening pigment and invaginating organelles in photoreceptor terminals of the housefly's first optic neuropile. J Neurobiol 32:517-529.
63. Pyza E, Meinertzhagen IA. 1997b. Neurites of period-expressing PDH cells in the fly's optic lobe exhibit circadian oscillations in morphology. Eur J Neurosci 9:1784-1788.
64. Pyza E, Meinertzhagen IA. 1998. Neurotransmitters alter the numbers of synapses and organelles in photoreceptor terminals in the lamina of the housefly, Musca domestica. J Comp Physiol A183:719-727.
65. Pyza E, Meinertzhagen IA. 1999. Daily rhythmic changes of cell size and shape in the first optic neuropil in Drosophila melanogaster. J Neurobiol 40:77-88.
66. Rao KR. 1992. Crustacean pigment-dispersing hormones: chemistry, distribution and actions. Pigment Cell Res Suppl 2:266-270.
67. Reischig T, Stengl M. 1996. Morphology and pigment-dispersing hormone immunocytochemistry of the accessory medulla, the presumptive circadian pacemaker of the cockroach Leucophaea maderae: a light- and electron-microscopic study. Cell Tissue Res 285:305-319.
68. Reischig T, Stengl M. 2003. Ultrastructure of pigment-dispersing hormone-immunoreactive neurons in a three-dimensional model of the accessory medulla of the cockroach Leucophaea maderae. Cell Tissue Res 314:421-435.
69. Reischig T, Petri B, Stengl M. 2004. Pigment-dispersing hormone (PDH)-immunoreactive neurons form a direct coupling pathway between the bilaterally symmetric circadian pacemakers of the cockroach Leucophaea maderae. Cell Tissue Res 318:553-564.
70. Renden R, Berwin B, Davis W, Ann K, Chin CT, Kreber R, Ganetzky B, Martin TF, Broadie K. 2001. Drosophila CAPS is an essential gene that regulates dense-core vesicle release and synaptic vesicle fusion. Neuron 31:421-437.
71. 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.
72. Richmond JE, Broadie KS. 2002. The synaptic vesicle cycle: exocytosis and endocytosis in Drosophila and C. elegans. Curr Opin Neurobiol 12:499-507.
73. Rieger D, Shafer OT, Tomioka K, Helfrich-Förster C. 2006. Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 26:2531-2543.
74. Robertson LK, Bowling DB, Mahaffey JP, Imiolczyk B, Mahaffey JW. 2004. An interactive network of zinc-finger proteins contributes to regionalization of the Drosophila embryo and establishes the domains of HOM-C protein function. Development 131:2781-2789.
75. Schneider NL, Stengl M. 2005. Pigment-dispersing factor and GABA synchronize cells of the isolated circadian clock of the cockroach Leucophaea maderae. J Neurosci 25:5138-5147.
76. Schürmann FW, Sandeman R, Sandeman D. 1991. Dense-core vesicles and non-synaptic exocytosis in the central body of the crayfish brain. Cell Tissue Res 265:493-501.
77. 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.
78. Shafer OT, Helfrich-Förster C, Renn SCP, Taghert PH. 2006. Reevaluation of Drosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes. J Comp Neurol 498:180-193.
79. Shiga S. 2003. Anatomy and functions of brain neurosecretory cells in Diptera. Microsc Res Techniq 62:114-131.
80. Stanewsky R, Frisch B, Brandes C, Hamblen-Coyle MJ, Rosbash M, Hall JC. 1997. 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.
81. b mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95:681-692.
82. Steller H, Fischbach KF, Rubin GM. 1987. Disconnected: a locus required for neuronal pathway formation in the visual system of Drosophila. Cell 50:1139-1153.
83. Stoleru D, Peng Y, Agosto J, Rosbash M. 2004. Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431:862-868.
84. Strausfeld NJ. 1976. An atlas of an insect brain. New York: Springer.
85. Taghert PH, Roberts ME, Renn SC, Jacobs PS. 2000. Metamorphosis of tangential visual system neurons in Drosophila. Dev Biol 222:471-485.
86. Taghert PH, Hewes RS, Park JH, O'Brien MA, Han M, Peck ME. 2001. Multiple amidated neuropeptides are required for normal circadian locomotor rhythms in Drosophila. J Neurosci 21:6673-6686.
87. Tsai LT, Bainton RJ, Blau J, Heberlein U. 2004. Lmo mutants reveal a novel role for circadian pacemaker neurons in cocaine-induced behaviors. PLoS Biol 2:e408.
88. Thureson-Klein AK, Klein RL. 1990. Exocytosis from neuronal large densecore vesicles. Int Rev Cytol 121:67-126.
89. 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.
90. Voets T, Toonen RF, Brian EC, de Wit H, Moser T, Rettig J, Südhof TC, Neher E, Verhage M. 2001. Munc18-1 promotes large dense-core vesicle docking. Neuron 31:581-591.
91. Yang Z, Sehgal A. 2001. Role of molecular oscillations in generating behavioral rhythms in Drosophila. Neuron 29:453-467.
92. Yasuyama K, Okada Y, Hamanaka Y, Shiga S. 2006. Synaptic connections between eyelet photoreceptors and pigment dispersing factor-immunoreactive neurons of the blowfly Protophormia terraenovae. J Comp Neurol 494:331-344.
93. Yuan Q, Lin F, Zheng X, Sehgal A. 2005. Serotonin modulates circadian entrainment in Drosophila. Neuron 47:115-127.
94. Zeng H, Qian Z, Myers MP, Rosbash M. 1996. A light-entrainment mechanism for the Drosophila circadian clock. Nature 380:129-135.
95. Zhao J, Kilman VL, Keegan KP, Peng Y, Emery P, Rosbash M, Allada R. 2003. Drosophila clock can generate ectopic circadian clocks. Cell 113:755-766.