Circadian expression of the presynaptic active zone protein bruchpilot in the lamina of Drosophila melanogaster

Developmental Neurobiology

Volumn 73, Issue 1, 2013, Pages 14-26

  Górska Andrzejak, Jolanta ^a   Makuch, Renata ^a   Stefan, Joanna ^a   Görlich, Alicja ^a   Semik, Danuta ^a   Pyza, Elzbieta ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Circadian clock; Glial cells; Synaptic plasticity; Tetrad synapses; Visual system

Indexed keywords

BRUCHPILOT PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FLUORESCENCE; GENE EXPRESSION; GLIA CELL; IMMUNOREACTIVITY; NEUROPIL; NONHUMAN; PHOTORECEPTOR; PHOTOTRANSDUCTION; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SYNAPSE; VISUAL SYSTEM;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASEMENT MEMBRANE; BRAIN; CIRCADIAN RHYTHM; CIRCADIAN RHYTHM SIGNALING PEPTIDES AND PROTEINS; DARKNESS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; NEUROPIL; PHOTORECEPTOR CELLS, VERTEBRATE; RNA INTERFERENCE;

EID: 84870734584     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22032     Document Type: Article

References (56)

1. Balys M, Pyza E. 2001. Localization of the clock controlling circadian rhythms in the first neuropile of the optic lobe in the housefly. J Exp Biol 204: 3303-3310.
2. Bloomquist BT, Shortridge RD, Schneuwly S, Perdew M, Montell C, Steller H, Rubin G, et al. 1988. Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 54: 723-733.
3. Burkhardt W, Braintenberg V. 1976. Some peculiar synaptic complexes in the first visual ganglion of the fly, Musca domestica. Cell Tissue Res 173: 287-308.
4. Cheng Y, Hardin PE, 1998. Drosophila photoreceptors contain an autonomous circadian oscillator that can function without period mRNA cycling. J Neurosci 18: 741-750.
5. Collins B, Mazzoni EO, Stanewsky R, Blau J. 2006. Drosophila CRYPTOCHROME is a circadian transcriptional repressor. Curr Biol 16: 441-449.
6. Cyran SA, Buchsbaum AM, Reddy KL, Lin MC, Glossop NR, Hardin PE, Young MW, et al. 2003. Vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 112: 329-341.
7. Damulewicz M, Pyza E. 2011. The clock input to the first optic neuropil of Drosophila melanogaster expressing neuronal circadian plasticity. PLoS One 6: e21258.
8. Dolezelova E, Dolezel D, Hall JC. 2007. Rhythms defects caused by newly engineered null mutations in Drosophila's cryptochrome gene. Genetics 177: 329-345.
9. 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.
10. 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.
11. Hardie RC. 1987. Is histamine a neurotransmitter in insect photoreceptors? J Comp Physiol A161: 201-213.
12. Hardin PE. 2005. The circadian timekeeping system of Drosophila. Curr Biol 15: 714-722.
13. Heisenberg M, Heusippet M, Wanke C. 1995. Structural plasticity in the Drosophila brain. J Neurosci 15: 1951-1960.
14. 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 182: 435-453.
15. Helfrich-Förster C. 2000. Differential control of morning and evening components in the activity rhythm of Drosophila melanogaster-Sex-specific differences suggest a different quality of activity. J Biol Rhythms 15: 135-154.
16. Helfrich-Förster C, Shafer OT, Wülbeck C, Grieshaber E, Rieger D, Taghert P. 2007. Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J Comp Neurol 500: 47-70.
17. Holtmaat A, Svoboda K. 2009. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Neurosci 6: 854-662.
18. Im SH, Taghert PH. 2010. PDF receptor expression reveals direct interaction between circadian oscillators in Drosophila. J Comp Neurol 518: 1925-1945.
19. Ivanchenko M, Stanewsky R, Giebultowicz JM. 2001. Circadian photoreception in Drosophila: functions of cryptochrome in peripheral and central clocks. J Biol Rhythms 16: 205-215.
20. Jasinska M, Siucinska E, Cybulska-Klosowicz A, Pyza E, Furness DN, Kossut M, Glazewski S. 2010. Rapid, learning-induced synaptogenesis in murine barrel field. J Neurosci 30: 1176-1184.
21. Kadener S, Stoleru D, McDonald M, Nawathean P, Rosbash M. 2007. Clockwork orange is a transcriptional repressor and a new Drosophila circadian pacemaker component. Genes Dev 21: 1675-1686.
22. Kittel RJ, Wichmann C, Rasse TM, Fouquet W, Schmidt M, Schmid A, Wagh DA, et al. 2006. Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 312: 1051-1054.
23. Krishnan B, Levine JD, Lynch MK, Dowse HB, Funes P, Hall J, Hardin PD, et al. 2001. A new role for cryptochrome in a Drosophila circadian oscillator. Nature 411: 313-317.
24. Kula E, Pyza E. 2007. Effects of locomotor stimulation and protein synthesis inhibition on circadian rhythms in size changes of L1 and L2 interneurons in the fly's visual system. Dev Neurobiol 67: 1433-1442.
25. Lin FJ, Song W, Meyer-Bernstein E, Naidoo N, Sehgal A. 2001. Photic signaling by cryptochrome in the Drosophila circadian system. Mol Cell Biol 21: 7287-7294.
26. Martin SJ, Grimwood PD, Morris RG. 2000. Synaptic plasticity and memory: An evaluation of the hypothesis. Annu Rev Neurosci 23: 649-711.
27. Matsumoto A, Ukai-Tadenuma M, Yamada RG, Houl J, Uno KD, Kasukawa T, Dauwalder B, et al. 2007. A functional genomics strategy reveals clockwork orange as a transcriptional regulator in the Drosophila circadian clock. Genes Dev 21: 1687-1700.
28. Meinertzhagen IA, O'Neil SD. 1991. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J Comp Neurol 305: 232-263.
29. Meinertzhagen IA, Sorra KE. 2001. Synaptic organization in the fly's optic lamina: Few cells, many synapses and divergent microcircuits. Prog Brain Res 13: 53-69.
30. Naidoo N, Song W, Hunter-Ensor M, Sehgal A. 1999. A role for the proteasome in the light response of the timeless clock protein. Science 285: 1737-1741.
31. Nicol D, Meinertzhagen IA. 1982. An analysis of the number and composition of the synaptic population formed by photoreceptors of the fly. J Comp Neurol 207: 29-44.
32. Pyza E. 2010. Circadian rhythms in the fly's visual system. In: Darlene AD, editor. Encyclopedia of the Eye, Vol. 1. Oxford: Academic Press, pp 302-311.
33. 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.
34. 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.
35. 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.
36. 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 A 183: 719-727.
37. 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.
38. Pyza E, Górska-Andrzejak J. 2004. Involvement of glial cells in rhythmic size changes in neurons of the housefly's visual system. J Neurobiol 59: 205-215.
39. Rieger D, Shafer OT, Tomioka K, Helfrich-Förster C. 2006. Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 26: 2531-2543.
40. Rosato E, Codd V, Mazzotta G, Piccin A, Zordan M, Costa R, Kyriacou CP. 2001. Light-dependent interaction between Drosophila CRY and the clock protein PER mediated by the carboxy terminus of CRY. Curr Biol 11: 909-917.
41. Schmid A, Hallermann S, Kittel RJ, Khorramshahi O, Frölich AM, Quentin C, Rasse TM, et al. 2008. Activity-dependent site-specific changes of glutamate receptor composition in vivo. Nat Neurosci 11: 659-666.
42. Shafer OT, Helfrich-Förster C, Renn SC, Taghert PH. 2006. Reevaluation of Drosophila melanogaster's neuronal circadian pacemakers reveal new neuronal classes. J Comp Neurol 498: 180-193.
43. Sheeba V, Fogle KJ, Holmes TC. 2010. Persistence of morning anticipation behavior and high amplitude morning startle response following functional loss of small ventral lateral neurons in Drosophila. PLoS One 5: e11628.
44. Sigg D, Thompson CM, Mercer AR. 1997. Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera (L.). J Neurosci 17: 7148-7156.
45. Spiwoks-Becker I, Glas M, Lasarzik I, Vollrath L. 2004. Mouse photoreceptor synaptic ribbons lose and regain material in response to illumination changes. Eur J Neurosci 19: 1559-1571.
46. b mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95: 681-692.
47. Stoleru D, Peng Y, Agosto J, Rosbash M. 2004. Coupled oscillators control morning and evening locomotor behavior of Drosophila. Nature 431: 862-868.
48. Strausfeld NJ, Campos-Ortega JA. 1977. Vision in insects: Pathways possibly underlying neural adaptation and lateral inhibition. Science 195: 894-897.
49. Tanoue S, Krishnan P, Krishnan B, Dryer SE, Hardin PE. 2004. Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr Biol 14: 638-649.
50. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Dürrbeck H, Buchner S, et al. 2006. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49: 833-844.
51. Weber P, Kula-Eversole E, Pyza E. 2009. Circadian control of dendrite morphology in the visual system of Drosophila melanogaster. PLoS One 4: e4290.
52. Weyhersmüller A, Hallermann S, Wagner N, Eilers J. 2011. Rapid active zone remodeling during synaptic plasticity. J Neurosci 31: 6041-6052.
53. 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.
54. Yoshii T, Todo T, Wülbeck C, Stanewsky R, Helfrich-Förster C. 2008. Cryptochrome is present in the compound eyes and a subset of Drosophila's clock neurons. J Comp Neurol 508: 952-966.
55. Zhang Y, Liu Y, Bilodeau-Wentworth D, Hardin PE, Emery P. 2010. Light and temperature control the contribution of specific DN1 neurons to Drosophila circadian behavior. Curr Biol 20: 600-605.
56. Zheng L, de Polavieja GG, Wolfram V, Asyali MH, Hardie RC, Juusola M. 2006. Feedback network controls photoreceptor output at the layer of the first synapses in Drosophila. J Gen Physiol 127: 495-510.