A One-day Journey to the Suburbs: Circadian Clock in the Drosophila Visual System

Overview

Journal FEBS J

Specialty Biochemistry

Date 2024 Nov 1

PMID 39484992

Authors

Milena Damulewicz

Gabriella M Mazzotta

Affiliations

Soon will be listed here.

Abstract

Living organisms, which are constantly exposed to cyclical variations in their environment, need a high degree of plasticity in their visual system to respond to daily and seasonal fluctuations in lighting conditions. In Drosophila melanogaster, the visual system is a complex tissue comprising different photoreception structures that exhibit daily rhythms in gene expression, cell morphology, and synaptic plasticity, regulated by both the central and peripheral clocks. In this review, we briefly summarize the structure of the circadian clock and the visual system in Drosophila and comprehensively describe circadian oscillations in visual structures, from molecules to behaviors, which are fundamental for the fine-tuning of visual sensitivity. We also compare some features of the rhythmicity in the visual system with that of the central pacemaker and hypothesize about the differences in the regulatory signals and mechanisms that control these two clocks.

References

Rieger D, Stanewsky R, Helfrich-Forster C . Cryptochrome, compound eyes, Hofbauer-Buchner eyelets, and ocelli play different roles in the entrainment and masking pathway of the locomotor activity rhythm in the fruit fly Drosophila melanogaster. J Biol Rhythms. 2003; 18(5):377-91. DOI: 10.1177/0748730403256997. View

Milena D, Elzbieta P . Determination of DNA Damage in the Retina Photoreceptors . Bio Protoc. 2021; 8(3):e2708. PMC: 8203978. DOI: 10.21769/BioProtoc.2708. View

Fan J, Agyekum B, Venkatesan A, Hall D, Keightley A, Bjes E . Noncanonical FK506-binding protein BDBT binds DBT to enhance its circadian function and forms foci at night. Neuron. 2013; 80(4):984-96. PMC: 3869642. DOI: 10.1016/j.neuron.2013.08.004. View

Richardt A, Rybak J, Stortkuhl K, Meinertzhagen I, Hovemann B . Ebony protein in the Drosophila nervous system: optic neuropile expression in glial cells. J Comp Neurol. 2002; 452(1):93-102. DOI: 10.1002/cne.10360. View

Schnell B, Joesch M, Forstner F, Raghu S, Otsuna H, Ito K . Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. J Neurophysiol. 2010; 103(3):1646-57. DOI: 10.1152/jn.00950.2009. View

Weber P, Kula-Eversole E, Pyza E . Circadian control of dendrite morphology in the visual system of Drosophila melanogaster. PLoS One. 2009; 4(1):e4290. PMC: 2628732. DOI: 10.1371/journal.pone.0004290. View

Jean-Guillaume C, Kumar J . Development of the ocellar visual system in Drosophila melanogaster. FEBS J. 2022; 289(23):7411-7427. PMC: 9805374. DOI: 10.1111/febs.16468. View

Singh S, Giesecke A, Damulewicz M, Fexova S, Mazzotta G, Stanewsky R . New Circadian Clock Mutants Affecting Temperature Compensation Induced by Targeted Mutagenesis of . Front Physiol. 2019; 10:1442. PMC: 6901700. DOI: 10.3389/fphys.2019.01442. View

OReilly L, Zhang X, Smithgall T . Individual Src-family tyrosine kinases direct the degradation or protection of the clock protein Timeless via differential ubiquitylation. Cell Signal. 2012; 25(4):860-6. PMC: 3595377. DOI: 10.1016/j.cellsig.2012.12.009. View

10.

Xiao N, Xu S, Li Z, Tang M, Mao R, Yang T . A single photoreceptor splits perception and entrainment by cotransmission. Nature. 2023; 623(7987):562-570. PMC: 10651484. DOI: 10.1038/s41586-023-06681-6. View

11.

Helfrich-Forster C, Edwards T, Yasuyama K, Wisotzki B, Schneuwly S, Stanewsky R . The extraretinal eyelet of Drosophila: development, ultrastructure, and putative circadian function. J Neurosci. 2002; 22(21):9255-66. PMC: 6758046. View

12.

Zuker C, Cowman A, Rubin G . Isolation and structure of a rhodopsin gene from D. melanogaster. Cell. 1985; 40(4):851-8. DOI: 10.1016/0092-8674(85)90344-7. View

13.

Naidoo N, Song W, Sehgal A . A role for the proteasome in the light response of the timeless clock protein. Science. 1999; 285(5434):1737-41. DOI: 10.1126/science.285.5434.1737. View

14.

Pyza E . Dynamic structural changes of synaptic contacts in the visual system of insects. Microsc Res Tech. 2002; 58(4):335-44. DOI: 10.1002/jemt.10141. View

15.

Shafer O, Gutierrez G, Li K, Mildenhall A, Spira D, Marty J . Connectomic analysis of the lateral neuron clock cells reveals the synaptic basis of functional pacemaker classes. Elife. 2022; 11. PMC: 9365390. DOI: 10.7554/eLife.79139. View

16.

Doktor B, Damulewicz M, Krzeptowski W, Bednarczyk B, Pyza E . Effects of PINK1 mutation on synapses and behavior in the brain of Drosophila melanogaster. Acta Neurobiol Exp (Wars). 2018; 78(3):231-241. View

17.

Kolodziejczyk A, Sun X, Meinertzhagen I, Nassel D . Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system. PLoS One. 2008; 3(5):e2110. PMC: 2373871. DOI: 10.1371/journal.pone.0002110. View

18.

Grima B, Chelot E, Xia R, Rouyer F . Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature. 2004; 431(7010):869-73. DOI: 10.1038/nature02935. View

19.

Lin J, Kilman V, Keegan K, Paddock B, Emery-Le M, Rosbash M . A role for casein kinase 2alpha in the Drosophila circadian clock. Nature. 2002; 420(6917):816-20. DOI: 10.1038/nature01235. View

20.

Gorska-Andrzejak J, Salvaterra P, Meinertzhagen I, Krzeptowski W, Gorlich A, Pyza E . Cyclical expression of Na+/K+-ATPase in the visual system of Drosophila melanogaster. J Insect Physiol. 2009; 55(5):459-68. PMC: 2721802. DOI: 10.1016/j.jinsphys.2009.02.003. View