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Cryptochrome mediates light-dependent magnetosensitivity of Drosophila's circadian clock.

Yoshii T, Ahmad M, Helfrich-Förster C - PLoS Biol. (2009)

Bottom Line: We tested the effect of applied static magnetic fields on the circadian clock and found that flies exposed to these fields indeed showed enhanced slowing of clock rhythms.This effect was maximal at 300 muT, and reduced at both higher and lower field strengths.We conclude that Drosophila's circadian clock is sensitive to magnetic fields and that this sensitivity depends on light activation of CRY and on the applied field strength, consistent with the radical pair mechanism.

View Article: PubMed Central - PubMed

Affiliation: University of Regensburg, Institute of Zoology, Regensburg, Germany.

ABSTRACT
Since 1960, magnetic fields have been discussed as Zeitgebers for circadian clocks, but the mechanism by which clocks perceive and process magnetic information has remained unknown. Recently, the radical-pair model involving light-activated photoreceptors as magnetic field sensors has gained considerable support, and the blue-light photoreceptor cryptochrome (CRY) has been proposed as a suitable molecule to mediate such magnetosensitivity. Since CRY is expressed in the circadian clock neurons and acts as a critical photoreceptor of Drosophila's clock, we aimed to test the role of CRY in magnetosensitivity of the circadian clock. In response to light, CRY causes slowing of the clock, ultimately leading to arrhythmic behavior. We expected that in the presence of applied magnetic fields, the impact of CRY on clock rhythmicity should be altered. Furthermore, according to the radical-pair hypothesis this response should be dependent on wavelength and on the field strength applied. We tested the effect of applied static magnetic fields on the circadian clock and found that flies exposed to these fields indeed showed enhanced slowing of clock rhythms. This effect was maximal at 300 muT, and reduced at both higher and lower field strengths. Clock response to magnetic fields was present in blue light, but absent under red-light illumination, which does not activate CRY. Furthermore, cry(b) and cry(OUT) mutants did not show any response, and flies overexpressing CRY in the clock neurons exhibited an enhanced response to the field. We conclude that Drosophila's circadian clock is sensitive to magnetic fields and that this sensitivity depends on light activation of CRY and on the applied field strength, consistent with the radical pair mechanism. CRY is widespread throughout biological systems and has been suggested as receptor for magnetic compass orientation in migratory birds. The present data establish the circadian clock of Drosophila as a model system for CRY-dependent magnetic sensitivity. Furthermore, given that CRY occurs in multiple tissues of Drosophila, including those potentially implicated in fly orientation, future studies may yield insights that could be applicable to the magnetic compass of migratory birds and even to potential magnetic field effects in humans.

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Representative Free-Running Locomotor Rhythms before and during the Exposure to a Magnetic FieldActograms of two wild-type flies (A and B), one cryb mutant (C) and one CRY-overexpressing fly (tim-gal4;uas-cry) (D) are depicted. All flies were exposed to blue light of 0.18 μW/cm2 throughout the experiment and to a magnetic field of 300 μT during the second half of the experiment (indicated by gray areas). The free-running periods of 40% of wild-type flies lengthened (A) and 12% shortened (B) during exposure to the magnetic field. These effects were not observed in the majority of cryb mutant flies (C). More than 60% of CRY-overexpressing flies exhibited arrhythmicity after the magnetic field (D).
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pbio-1000086-g002: Representative Free-Running Locomotor Rhythms before and during the Exposure to a Magnetic FieldActograms of two wild-type flies (A and B), one cryb mutant (C) and one CRY-overexpressing fly (tim-gal4;uas-cry) (D) are depicted. All flies were exposed to blue light of 0.18 μW/cm2 throughout the experiment and to a magnetic field of 300 μT during the second half of the experiment (indicated by gray areas). The free-running periods of 40% of wild-type flies lengthened (A) and 12% shortened (B) during exposure to the magnetic field. These effects were not observed in the majority of cryb mutant flies (C). More than 60% of CRY-overexpressing flies exhibited arrhythmicity after the magnetic field (D).

Mentions: In a first experiment we tested the influence of magnetic fields of different intensities (Figure 1). The radical-pair mechanism predicts that there should be an optimal magnetic strength and that the effects would be smaller under too low or too high magnetic fields [9]. To enable comparison with previous experiments [37] we chose static magnetic fields of 0 μT, 150 μT, 300 μT, and 500 μT; excepting the control of 0 μT these are, respectively, 3, 6, and 10 times stronger than natural magnetic fields. The free-running periods of the flies were determined before and during the application of the constant magnetic fields and the changes in period were calculated (independent of their direction). We found that even flies without exposure to a magnetic field exhibited period changes over the recording time, but that these changes were significantly smaller than those occurring under the influence of a magnetic field of 300 μT (Figures 2A, 2B and 3A). ANOVA revealed that the period changes depended significantly on the strength of the magnetic field (Figure 3A). Most flies lengthened their periods in response to the magnetic field (Figure 2A); but there are also some flies with shortened periods (Figure 2B). To quantify the number of flies with shortened and lengthened periods we defined the following categories (Table 1): Flies exhibiting period changes smaller than 0.5 h (as most wild-type flies did) were defined as flies showing no effects. Flies with shortened or lengthened periods by 0.5 h or more were defined as flies showing period shortening or lengthening, respectively. The third category consisted of flies in which periodogram analysis could not detect any significant period. These were defined as arrhythmic. χ2 analysis revealed that the number of flies with lengthened periods was significantly higher when a magnetic field of 300 μT was applied (Table 1).


Cryptochrome mediates light-dependent magnetosensitivity of Drosophila's circadian clock.

Yoshii T, Ahmad M, Helfrich-Förster C - PLoS Biol. (2009)

Representative Free-Running Locomotor Rhythms before and during the Exposure to a Magnetic FieldActograms of two wild-type flies (A and B), one cryb mutant (C) and one CRY-overexpressing fly (tim-gal4;uas-cry) (D) are depicted. All flies were exposed to blue light of 0.18 μW/cm2 throughout the experiment and to a magnetic field of 300 μT during the second half of the experiment (indicated by gray areas). The free-running periods of 40% of wild-type flies lengthened (A) and 12% shortened (B) during exposure to the magnetic field. These effects were not observed in the majority of cryb mutant flies (C). More than 60% of CRY-overexpressing flies exhibited arrhythmicity after the magnetic field (D).
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2667543&req=5

pbio-1000086-g002: Representative Free-Running Locomotor Rhythms before and during the Exposure to a Magnetic FieldActograms of two wild-type flies (A and B), one cryb mutant (C) and one CRY-overexpressing fly (tim-gal4;uas-cry) (D) are depicted. All flies were exposed to blue light of 0.18 μW/cm2 throughout the experiment and to a magnetic field of 300 μT during the second half of the experiment (indicated by gray areas). The free-running periods of 40% of wild-type flies lengthened (A) and 12% shortened (B) during exposure to the magnetic field. These effects were not observed in the majority of cryb mutant flies (C). More than 60% of CRY-overexpressing flies exhibited arrhythmicity after the magnetic field (D).
Mentions: In a first experiment we tested the influence of magnetic fields of different intensities (Figure 1). The radical-pair mechanism predicts that there should be an optimal magnetic strength and that the effects would be smaller under too low or too high magnetic fields [9]. To enable comparison with previous experiments [37] we chose static magnetic fields of 0 μT, 150 μT, 300 μT, and 500 μT; excepting the control of 0 μT these are, respectively, 3, 6, and 10 times stronger than natural magnetic fields. The free-running periods of the flies were determined before and during the application of the constant magnetic fields and the changes in period were calculated (independent of their direction). We found that even flies without exposure to a magnetic field exhibited period changes over the recording time, but that these changes were significantly smaller than those occurring under the influence of a magnetic field of 300 μT (Figures 2A, 2B and 3A). ANOVA revealed that the period changes depended significantly on the strength of the magnetic field (Figure 3A). Most flies lengthened their periods in response to the magnetic field (Figure 2A); but there are also some flies with shortened periods (Figure 2B). To quantify the number of flies with shortened and lengthened periods we defined the following categories (Table 1): Flies exhibiting period changes smaller than 0.5 h (as most wild-type flies did) were defined as flies showing no effects. Flies with shortened or lengthened periods by 0.5 h or more were defined as flies showing period shortening or lengthening, respectively. The third category consisted of flies in which periodogram analysis could not detect any significant period. These were defined as arrhythmic. χ2 analysis revealed that the number of flies with lengthened periods was significantly higher when a magnetic field of 300 μT was applied (Table 1).

Bottom Line: We tested the effect of applied static magnetic fields on the circadian clock and found that flies exposed to these fields indeed showed enhanced slowing of clock rhythms.This effect was maximal at 300 muT, and reduced at both higher and lower field strengths.We conclude that Drosophila's circadian clock is sensitive to magnetic fields and that this sensitivity depends on light activation of CRY and on the applied field strength, consistent with the radical pair mechanism.

View Article: PubMed Central - PubMed

Affiliation: University of Regensburg, Institute of Zoology, Regensburg, Germany.

ABSTRACT
Since 1960, magnetic fields have been discussed as Zeitgebers for circadian clocks, but the mechanism by which clocks perceive and process magnetic information has remained unknown. Recently, the radical-pair model involving light-activated photoreceptors as magnetic field sensors has gained considerable support, and the blue-light photoreceptor cryptochrome (CRY) has been proposed as a suitable molecule to mediate such magnetosensitivity. Since CRY is expressed in the circadian clock neurons and acts as a critical photoreceptor of Drosophila's clock, we aimed to test the role of CRY in magnetosensitivity of the circadian clock. In response to light, CRY causes slowing of the clock, ultimately leading to arrhythmic behavior. We expected that in the presence of applied magnetic fields, the impact of CRY on clock rhythmicity should be altered. Furthermore, according to the radical-pair hypothesis this response should be dependent on wavelength and on the field strength applied. We tested the effect of applied static magnetic fields on the circadian clock and found that flies exposed to these fields indeed showed enhanced slowing of clock rhythms. This effect was maximal at 300 muT, and reduced at both higher and lower field strengths. Clock response to magnetic fields was present in blue light, but absent under red-light illumination, which does not activate CRY. Furthermore, cry(b) and cry(OUT) mutants did not show any response, and flies overexpressing CRY in the clock neurons exhibited an enhanced response to the field. We conclude that Drosophila's circadian clock is sensitive to magnetic fields and that this sensitivity depends on light activation of CRY and on the applied field strength, consistent with the radical pair mechanism. CRY is widespread throughout biological systems and has been suggested as receptor for magnetic compass orientation in migratory birds. The present data establish the circadian clock of Drosophila as a model system for CRY-dependent magnetic sensitivity. Furthermore, given that CRY occurs in multiple tissues of Drosophila, including those potentially implicated in fly orientation, future studies may yield insights that could be applicable to the magnetic compass of migratory birds and even to potential magnetic field effects in humans.

Show MeSH
Related in: MedlinePlus