Exquisite Light Sensitivity of Cryptochrome

English version České info

Drosophila melanogaster shows exquisite light sensitivity for modulation of circadian functions in vivo, yet the activities of the Drosophila circadian photopigment cryptochrome (CRY) have only been observed at high light levels. We studied intensity/duration parameters for light pulse induced circadian phase shifts under dim light conditions in vivo. Flies show far greater light sensitivity than previously appreciated, and show a surprising sensitivity increase with pulse duration, implying a process of photic integration active up to at least 6 hours. The CRY target timeless (TIM) shows dim light dependent degradation in circadian pacemaker neurons that parallels phase shift amplitude, indicating that integration occurs at this step, with the strongest effect in a single identified pacemaker neuron. Our findings indicate that CRY compensates for limited light sensitivity in vivo by photon integration over extraordinarily long times, and point to select circadian pacemaker neurons as having important roles.

Vyšlo v časopise: Exquisite Light Sensitivity of Cryptochrome. PLoS Genet 9(7): e32767. doi:10.1371/journal.pgen.1003615
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003615

Souhrn

Zdroje

1. GolombekDA, RosensteinRE (2010) Physiology of circadian entrainment. Physiol Rev 90 : 1063–1102.

2. HardinPE (2011) Molecular genetic analysis of circadian timekeeping in Drosophila. Adv Genet 74 : 141–173.

3. PeschelN, Helfrich-ForsterC (2011) Setting the clock–by nature: circadian rhythm in the fruitfly Drosophila melanogaster. FEBS Lett 585 : 1435–1442.

4. Helfrich-ForsterC, WinterC, HofbauerA, HallJC, StanewskyR (2001) The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30 : 249–261.

5. WheelerDA, Hamblen-CoyleMJ, DushayMS, HallJC (1993) Behavior in light-dark cycles of Drosophila mutants that are arrhythmic, blind, or both. J Biol Rhythms 8 : 67–94.

6. SuriV, QianZ, HallJC, RosbashM (1998) Evidence that the TIM light response is relevant to light-induced phase shifts in Drosophila melanogaster. Neuron 21 : 225–234.

7. YangZ, EmersonM, SuHS, SehgalA (1998) Response of the timeless protein to light correlates with behavioral entrainment and suggests a nonvisual pathway for circadian photoreception. Neuron 21 : 215–223.

8. EmeryP, StanewskyR, HallJC, RosbashM (2000) A unique circadian-rhythm photoreceptor. Nature 404 : 456–457.

9. KlarsfeldA, MalpelS, Michard-VanheeC, PicotM, ChelotE, et al. (2004) Novel features of cryptochrome-mediated photoreception in the brain circadian clock of Drosophila. J Neurosci 24 : 1468–1477.

10. VeleriS, BrandesC, Helfrich-ForsterC, HallJC, StanewskyR (2003) A self-sustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr Biol 13 : 1758–1767.

11. LinFJ, SongW, Meyer-BernsteinE, NaidooN, SehgalA (2001) Photic signaling by cryptochrome in the Drosophila circadian system. Mol Cell Biol 21 : 7287–7294.

12. CollinsB, MazzoniEO, StanewskyR, BlauJ (2006) Drosophila CRYPTOCHROME is a circadian transcriptional repressor. Curr Biol 16 : 441–449.

13. IvanchenkoM, StanewskyR, GiebultowiczJM (2001) Circadian photoreception in Drosophila: functions of cryptochrome in peripheral and central clocks. J Biol Rhythms 16 : 205–215.

14. PeschelN, ChenKF, SzaboG, StanewskyR (2009) Light-dependent interactions between the Drosophila circadian clock factors cryptochrome, jetlag, and timeless. Curr Biol 19 : 241–247.

15. HirshJ, RiemenspergerT, CoulomH, IcheM, CouparJ, et al. (2010) Roles of dopamine in circadian rhythmicity and extreme light sensitivity of circadian entrainment. Curr Biol 20 : 209–214.

16. YuanQ, LinF, ZhengX, SehgalA (2005) Serotonin modulates circadian entrainment in Drosophila. Neuron 47 : 115–127.

17. EmeryP, StanewskyR, Helfrich-ForsterC, Emery-LeM, HallJC, et al. (2000) Drosophila CRY is a deep brain circadian photoreceptor. Neuron 26 : 493–504.

18. FrankKD, ZimmermanWF (1969) Action spectra for phase shifts of a circadian rhythm in Drosophila. Science 163 : 688–689.

19. OzturkN, SelbyCP, AnnayevY, ZhongD, SancarA (2011) Reaction mechanism of Drosophila cryptochrome. Proc Natl Acad Sci U S A 108 : 516–521.

20. FogleKJ, ParsonKG, DahmNA, HolmesTC (2011) CRYPTOCHROME is a blue-light sensor that regulates neuronal firing rate. Science 331 : 1409–1413.

21. BuszaA, Emery-LeM, RosbashM, EmeryP (2004) Roles of the two Drosophila CRYPTOCHROME structural domains in circadian photoreception. Science 304 : 1503–1506.

22. BloomquistBT, ShortridgeRD, SchneuwlyS, PerdewM, MontellC, et al. (1988) Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 54 : 723–733.

23. SzularJ, SehadovaH, GentileC, SzaboG, ChouWH, et al. (2012) Rhodopsin 5 -⁠ and Rhodopsin 6-mediated clock synchronization in Drosophila melanogaster is independent of retinal phospholipase C-beta signaling. J Biol Rhythms 27 : 25–36.

24. KistenpfennigC, HirshJ, YoshiiT, Helfrich-ForsterC (2012) Phase-Shifting the Fruit Fly Clock without Cryptochrome. J Biol Rhythms 27 : 117–125.

25. StanewskyR, KanekoM, EmeryP, BerettaB, Wager-SmithK, et al. (1998) The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95 : 681–692.

26. HardieRC (2001) Phototransduction in Drosophila melanogaster. J Exp Biol 204 : 3403–3409.

27. PariskyKM, AgostoJ, PulverSR, ShangY, KuklinE, et al. (2008) PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60 : 672–682.

28. SheebaV, FogleKJ, KanekoM, RashidS, ChouYT, et al. (2008) Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr Biol 18 : 1537–1545.

29. ShangY, GriffithLC, RosbashM (2008) Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc Natl Acad Sci U S A 105 : 19587–19594.

30. DoMT, KangSH, XueT, ZhongH, LiaoHW, et al. (2009) Photon capture and signalling by melanopsin retinal ganglion cells. Nature 457 : 281–287.

31. NelsonDE, TakahashiJS (1991) Sensitivity and integration in a visual pathway for circadian entrainment in the hamster (Mesocricetus auratus). J Physiol 439 : 115–145.

32. Van Den PolAN, CaoV, HellerHC (1998) Circadian system of mice integrates brief light stimuli. Am J Physiol 275: R654–657.

33. RiegerD, ShaferOT, TomiokaK, Helfrich-ForsterC (2006) Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 26 : 2531–2543.

34. YoshiiT, TodoT, WulbeckC, StanewskyR, Helfrich-ForsterC (2008) Cryptochrome is present in the compound eyes and a subset of Drosophila's clock neurons. J Comp Neurol 508 : 952–966.

35. BerndtA, KottkeT, BreitkreuzH, DvorskyR, HennigS, et al. (2007) A novel photoreaction mechanism for the circadian blue light photoreceptor Drosophila cryptochrome. J Biol Chem 282 : 13011–13021.

36. MyersMP, Wager-SmithK, Rothenfluh-HilfikerA, YoungMW (1996) Light-induced degradation of TIMELESS and entrainment of the Drosophila circadian clock. Science 271 : 1736–1740.

37. SathyanarayananS, ZhengX, KumarS, ChenCH, ChenD, et al. (2008) Identification of novel genes involved in light-dependent CRY degradation through a genome-wide RNAi screen. Genes Dev 22 : 1522–1533.

38. IshikawaT, MatsumotoA, KatoTJr, TogashiS, RyoH, et al. (1999) DCRY is a Drosophila photoreceptor protein implicated in light entrainment of circadian rhythm. Genes Cells 4 : 57–65.

39. DolezelovaE, DolezelD, HallJC (2007) Rhythm defects caused by newly engineered null mutations in Drosophila's cryptochrome gene. Genetics 177 : 329–345.

40. KohK, ZhengX, SehgalA (2006) JETLAG resets the Drosophila circadian clock by promoting light-induced degradation of TIMELESS. Science 312 : 1809–1812.

41. YoshiiT, VaninS, CostaR, Helfrich-ForsterC (2009) Synergic entrainment of Drosophila's circadian clock by light and temperature. J Biol Rhythms 24 : 452–464.