Loss of Drosophila melanogaster TRPA1 Function Affects "siesta" Behavior but Not Synchronization to Temperature Cycles

Journal of Biological Rhythms

Volumn 30, Issue 6, 2015, Pages 492-505

  Roessingh, Sanne ^a,b   Wolfgang, Werner ^b   Stanewsky, Ralf ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

circadian clocks; Drosophila melanogaster; sleep; temperature entrainment; thermo TRP channels; TRPA1

Indexed keywords

DROSOPHILA PROTEIN; TRANSCRIPTION FACTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPA1 PROTEIN, DROSOPHILA;

ANIMAL; ASSOCIATION; CIRCADIAN RHYTHM; DEFICIENCY; DROSOPHILA MELANOGASTER; GENETICS; METABOLISM; MOTOR ACTIVITY; MUTATION; NERVE CELL; PHYSIOLOGY; SLEEP; TEMPERATURE;

ANIMALS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CUES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MOTOR ACTIVITY; MUTATION; NEURONS; SLEEP; TEMPERATURE; TRANSCRIPTION FACTORS; TRPC CATION CHANNELS;

EID: 84947289412     PISSN: 07487304     EISSN: 15524531     Source Type: Journal    
DOI: 10.1177/0748730415605633     Document Type: Article

References (45)

1. Aschoff J, Tokura H, (1986) Circadian activity rhythm in squirrel monkeys: entrainment by temperature cycles. J Biol Rhythms 1 (2): 91-99.
2. Bushey D, Tononi G, Cirelli C, (2015) Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging. Proc Natl Acad Sci USA 112 (15): 4785-4790.
3. Busza A, Emery-Le M, Rosbash M, Emery P, (2004) Roles of the two Drosophila CRYPTOCHROME structural domains in circadian photoreception. Science 304: 1503-1506.
4. Busza A, Murad A, Emery P, (2007) Interactions between circadian neurons control temperature synchronization of Drosophila behavior. J Neurosci 27 (40): 10722-10733.
5. Cao W, Edery I, (2015) A novel pathway for sensory-mediated arousal involves splicing of an intron in the period clock gene. Sleep 38 (1): 41-51.
6. Collins BH, Rosato E, Kyriacou CP, (2004) Seasonal behavior in Drosophila melanogaster requires the photoreceptors, the circadian clock, and phospholipase C. Proc Natl Acad Sci USA 101 (7): 1945-1950.
7. 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.
8. Fowler MA, Montell C, (2013) Drosophila TRP channels and animal behavior. Life Sci 92: 394-403.
9. Gentile C, Sehadova H, Simoni A, Chen C, Stanewsky R, (2013) Cryptochrome antagonizes synchronization of Drosophila's circadian clock to temperature cycles. Curr Biol 23: 185-195.
10. Gilestro GF, Cirelli C, (2009) pySolo: a complete suite for sleep analysis in Drosophila. Bioinformatics 25 (11): 1466-1467.
11. Glaser FT, Stanewsky R, (2005) Temperature synchronization of the Drosophila circadian clock. Curr Biol 15: 1352-1363.
12. Green EW, O'Callaghan EK, Hansen CN, Bastianello S, Bhutani S, Vanin S, Armstrong JD, Costa R, Kyriacou CP, (2015) Drosophila circadian rhythms in seminatural environments: summer afternoon component is not an artifact and requires TrpA1 channels. Proc Nat Acad Sci USA 112 (28): 8702-8707.
13. Hamada FN, Rosenzweig M, Kang K, Pulver S, Ghezzi A, Jegla TJ, Garrity PA, (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454 (7201): 217-220.
14. Hamblen MJ, White NE, Emery PT, Kaiser K, Hall JC, (1998) Molecular and behavioural analysis of four period mutants in Drosophila melanogaster encompassing extreme short, novel long, and unorthodox arrhythmic types. Genetics 149 (1): 165-178.
15. 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.
16. Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, Sehgal A, Pack AI, (2000) Rest in Drosophila is a sleep-like state. Neuron 25: 129-138.
17. Kwon Y, Shim H-S, Wang X, Montell C, (2008) Control of thermotactic behaviour via coupling of a TRP channel to a phospholipase C signalling cascade. Nat Neurosci 11 (8): 871-873.
18. Lahiri K, Vallone D, Gondi SB, Santoriello C, Dickmeis T, Foulkes NS, (2005) Temperature regulates transcription in the zebrafish circadian clock. PLoS Biol 3 (11): e351.
19. Lee Y, (2013) Contribution of Drosophila TRPA1-expressing neurons to circadian locomotor activity patterns. PLoS One 8 (12): e85189.
20. Lee Y, Montell C, (2013) Drosophila TRPA1 functions in temperature control of circadian rhythm in pacemaker neurons. J Neurosci 33 (16): 6716-6725.
21. Levine JC, Funes P, Dowse HB, Hall JC, (2002) Signal analysis of behavioral and molecular cycles. BMC Neurosci 3: 1-25.
22. Liu C, Montell C, (2015) Forcing open TRP channels: Mechanical gating as a unifying activation mechanism. Biochem Biophys Res Commun 460: 22-25.
23. Low KH, Chen WF, Yildirim E, Edery I, (2012) Natural variation in the Drosophila melanogaster clock gene period modulates splicing of its 3'-terminal intron and mid-day siesta. PLoS One 7 (11): e49536.
24. Low KH, Lim C, Ko HW, Edery I, (2008) Natural variation in the splice site strength of a clock gene and species-specific thermal adaptation. Neuron 60 (6): 1054-1067.
25. Majercak J, Chen WF, Edery I, (2004) Splicing of the period gene 3′-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol Cell Biol 24 (8): 3359-3372.
26. Majercak J, Sidote D, Hardin PE, Edery I, (1999) How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 24 (1): 219-230.
27. Nitz DA, van Swinderen B, Nononi G, Greenspan RJ, (2002) Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr Biol 12: 1934-1940.
28. Peschel N, Helfrich-Förster C, (2011) Setting the clock-by nature: circadian rhythm in the fruitfly Drosophila melanogaster. FEBS Lett 585 (10): 1435-1442.
29. Peschel N, Veleri S, Stanewsky R, (2006) Veela defines a molecular link between Cryptochrome and Timeless in the light-input pathway to Drosophila' s circadian clock. Proc Nat Acad Sci USA 103 (46): 17313-17318.
30. Refinetti R, (2010) Entrainment of circadian rhythm by ambient temperature cycles in mice. J Biol Rhythms 25 (4): 247-256.
31. Ryder E, Ashburner M, Bautista-Llacer R, Drummond J, Webster J, Johnson G, Morley T, Sang Chan Y, Blows F, Coulson D, et al. (2007) The DrosDel deletion collection: a Drosophila genomewide chromosomal deficiency resource. Genetics 177 (1): 615-629.
32. Sandrelli F, Tauber E, Pegoraro M, Mazzotta G, Cisotto P, Landskron J, Stanewsky R, Piccin A, Rosato E, Zordan M, et al. (2007) A molecular basis for natural selection at the timeless locus in Drosophila melanogaster. Science 316: 1898-1900.
33. Sehadova H, Glaser FT, Gentile C, Simoni A, Giesecke A, Albert JT, Stanewsky R, (2009) Temperature entrainment of Drosophila 's circadian clock involves the gene nocte and signaling from peripheral sensory tissues to the brain. Neuron 64: 251-266.
34. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G, (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287 (5459): 1834-1837.
35. b mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95: 681-692.
36. Vanin S, Bhutani S, Montelli S, Menegazzi P, Green EW, Pegoraro M, Sandrelli F, Costa R, Kyriacou CP, (2012) Unexpected features of Drosophila circadian behavioural rhythms under natural conditions. Nature 484 (7394): 371-375.
37. Viswanath V, Story GM, Peier AM, Petrus MJ, Lee VM, Wook Hwang S, Patapoutian A, Jegla T, (2003) Ion channels: opposite thermosensor in fruitfly and mouse. Nature 423: 822-823.
38. 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.
39. Wolfgang W, Simoni A, Gentile C, Stanewsky R, (2013) The Pyrexia transient repector potential channel mediates circadian clock synchronization to low temperature cycles in Drosophila melanogaster. Proc Biol Sci 280 (1768):20130959
40. Yoshida T, Murayama Y, Ito H, Kageyama H, Kondo T, (2009) Nonparametric entrainment of the in vitro circadian phosphorylation rhythm of cyanobacterial KaiC by temperature cycle. Proc Natl Acad Sci USA 106 (5): 1648-1653.
41. Yoshii T, Hermann C, Helfrich-Förster C, (2010) Cryptochrome-positive and -negative clock neurons in Drosophila entrain differentially to light and temperature. J Biol Rhythms 25 (6): 387-398.
42. Yoshii T, Hermann-Luibl C, Kistenpfennig C, Schmid B, Tomioka K, Helfrich-Förster C, (2015) Cryptochrome-dependent and -independent circadian entrainment circuits in Drosophila. J Neurosci 35 (15): 6131-6141.
43. Yoshii T, Vanin S, Costa R, Helfrich-Förster C, (2009) Synergic entrainment of Drosophila's circadian clock by light and temperature. J Biol Rhythms 24 (6): 452-464.
44. Zhang 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 (7): 600-605.
45. Zhong L, Bellemer A, Yan H, Honjo K, Robertson J, Hwang RY, Pitt GS, Tracey WD, (2012) Thermosensory and non-thermosensory isoforms of Drosophila melanogaster TRPA1 reveal heat sensor domains of a thermoTRP channel. Cell Reports 1 (1): 43-55.