An electromagnetic field disrupts negative geotaxis in Drosophila via a CRY-dependent pathway

Nature Communications

Volumn 5, Issue , 2014, Pages

  Fedele, Giorgio ^a   Green, Edward W ^a   Rosato, Ezio ^a   Kyriacou, Charalambos P ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME; FLAVINE ADENINE NUCLEOTIDE; DROSOPHILA PROTEIN;

ANTENNA (ORGAN); ARTICLE; BLUE LIGHT; CARBOXY TERMINAL SEQUENCE; CIRCADIAN RHYTHM; CLIMBING; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ELECTROMAGNETIC FIELD; ELECTRON; GENE DELETION; GENE MUTATION; GENOTYPE; LOCOMOTION; NEGATIVE GEOTAXIS; NERVE CELL; NONHUMAN; PHENOTYPE; PHOTOACTIVATION; PHOTORECEPTOR; SPECTRAL SENSITIVITY; ANIMAL; DROSOPHILA; METABOLISM;

ANIMALS; CRYPTOCHROMES; DROSOPHILA; DROSOPHILA PROTEINS; ELECTROMAGNETIC FIELDS; FLAVIN-ADENINE DINUCLEOTIDE;

EID: 84904489276     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5391     Document Type: Article

References (40)

1. Gould, J. L. Magnetoreception. Curr. Biol. 20, R431-R435 (2010).
2. Johnsen, S. & Lohmann, K. J. Magnetoreception in animals. Phys. Today 61, 29-35 (2008).
3. Ritz, T., Adem, S. & Schulten, K. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707-718 (2000). (Pubitemid 30211829)
4. Ritz, T., Ahmad, M., Mouritsen, H., Wiltschko, R. & Wiltschko, W. Photoreceptor-based magnetoreception: optimal design of receptor molecules, cells, and neuronal processing. J. R. Soc. Interface 7(Suppl 2): S135-S146 (2010).
5. Chaves, I. et al. The cryptochromes: blue light photoreceptors in plants and animals. Annu. Rev. Plant Biol. 62, 335-364 (2011).
6. Ruan, G. X., Zhang, D. Q., Zhou, T., Yamazaki, S. & McMahon, D. G. Circadian organization of the mammalian retina. Proc. Natl Acad. Sci. USA 103, 9703-9708 (2006). (Pubitemid 43955888)
7. Moller, A., Sagasser, S., Wiltschko, W. & Schierwater, B. Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. Naturwissenschaften 91, 585-588 (2004). (Pubitemid 40064608)
8. Niessner, C. et al. Magnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds. J. R. Soc. Interface 10, 20130638 (2013).
9. b mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95, 681-692 (1998). (Pubitemid 28544129)
10. Shearman, L. P. et al. Interacting molecular loops in the mammalian circadian clock. Science 288, 1013-1019 (2000). (Pubitemid 30324228)
11. Froy, O., Chang, D. C. & Reppert, S. M. Redox potential: differential roles in dCRY and mCRY1 functions. Curr. Biol. 12, 147-152 (2002). (Pubitemid 34099140)
12. Yuan, Q., Metterville, D., Briscoe, A. D. & Reppert, S. M. Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks. Mol. Biol. Evol. 24, 948-955 (2007). (Pubitemid 46536704)
13. Gegear, R. J., Casselman, A., Waddell, S. & Reppert, S. M. Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature 454, 1014-1018 (2008).
14. Yoshii, T., Ahmad, M. & Helfrich-Forster, C. Cryptochrome mediates light-dependent magnetosensitivity of Drosophila's circadian clock. PLoS Biol. 7, e1000086 (2009).
15. Phillips, J. B. & Sayeed, O. Wavelength-dependent effects of light on magnetic compass orientation in Drosophila melanogaster. J. Comp. Physiol. A 172, 303-308 (1993).
16. Wehner, R. & Labhart, T. Perception of the geomagnetic field in the fly Drosophila melanogaster. Experientia 26, 967-968 (1970).
17. Painter, M. S., Dommer, D. H., Altizer, W. W., Muheim, R. & Phillips, J. B. Spontaneous magnetic orientation in larval Drosophila shares properties with learned magnetic compass responses in adult flies and mice. J. Exp. Biol. 216, 1307-1316 (2013).
18. Gegear, R. J., Foley, L. E., Casselman, A. & Reppert, S. M. Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism. Nature 463, 804-807 (2010).
19. Foley, L. E., Gegear, R. J. & Reppert, S. M. Human cryptochrome exhibits light-dependent magnetosensitivity. Nat. Commun. 2, 356 (2011).
20. Dodson, C. A., Hore, P. J. & Wallace, M. I. A radical sense of direction: signalling and mechanism in cryptochrome magnetoreception. Trends Biochem. Sci. 38, 435-446 (2013).
21. Toma, D. P., White, K. P., Hirsch, J. & Greenspan, R. J. Identification of genes involved in Drosophila melanogaster geotaxis, a complex behavioral trait. Nat. Genet. 31, 349-353 (2002). (Pubitemid 35154442)
22. Rakshit, K. & Giebultowicz, J. M. Cryptochrome restores dampened circadian rhythms and promotes healthspan in aging Drosophila. Aging Cell 12, 752-762 (2013).
23. Yoshii, T., Todo, T., Wulbeck, C., Stanewsky, R. & Helfrich-Forster, C. Cryptochrome is present in the compound eyes and a subset of Drosophila's clock neurons. J. Comp. Neurol. 508, 952-966 (2008). (Pubitemid 351693553)
24. Grima, B., Chelot, E., Xia, R. & Rouyer, F. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431, 869-873 (2004). (Pubitemid 39434085)
25. Rosato, E. et al. Light-dependent interaction between Drosophila CRY and the clock protein PER mediated by the carboxy terminus of CRY. Curr. Biol. 11, 909-917 (2001). (Pubitemid 32589182)
26. Dissel, S. et al. A constitutively active cryptochrome in Drosophila melanogaster. Nat. Neurosci. 7, 834-840 (2004). (Pubitemid 38989506)
27. Biskup, T. et al. Variable electron transfer pathways in an amphibian cryptochrome: tryptophan versus tyrosine-based radical pairs. J. Biol. Chem. 288, 9249-9260 (2013).
28. Stoleru, D. et al. The Drosophila circadian network is a seasonal timer. Cell 129, 207-219 (2007). (Pubitemid 46507587)
29. Montell, C. Drosophila visual transduction. Trends Neurosci. 35, 356-363 (2012).
30. Szular, J. et al. 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 (2012).
31. Kamikouchi, A. et al. The neural basis of Drosophila gravity-sensing and hearing. Nature 458, 165-171 (2009).
32. Kamikouchi, A., Shimada, T. & Ito, K. Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J. Comp. Neurol. 499, 317-356 (2006). (Pubitemid 44571933)
33. Sun, Y. et al. TRPA channels distinguish gravity sensing from hearing in Johnston's organ. Proc. Natl Acad. Sci. USA 106, 13606-13611 (2009).
34. Reppert, S. M., Gegear, R. J. & Merlin, C. Navigational mechanisms of migrating monarch butterflies. Trends Neurosci. 33, 399-406 (2010).
35. Merlin, C., Gegear, R. J. & Reppert, S. M. Antennal circadian clocks coordinate sun compass orientation in migratory monarch butterflies. Science 325, 1700-1704 (2009).
36. de Oliveira, J. F. et al. Ant antennae: are they sites for magnetoreception? J. R. Soc. Interface 7, 143-152 (2010).
37. Emery, P., So, W. V., Kaneko, M., Hall, J. C. & Rosbash, M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95, 669-679 (1998). (Pubitemid 28544128)
38. Dolezelova, E., Dolezel, D. & Hall, J. C. Rhythm defects caused by newly engineered null mutations in Drosophila's cryptochrome gene. Genetics 177, 329-345 (2007). (Pubitemid 47555852)
39. Kirschvink, J. L. Uniform magnetic fields and double-wrapped coil systems: improved techniques for the design of bioelectromagnetic experiments. Bioelectromagnetics 13, 401-411 (1992).
40. Winer, B. J. in Statistical Principles in Experimental Design 2nd edn (McGraw-Hill, 1971).