Cryptochrome Mediates Light-Dependent Magnetosensitivity of Drosophila's Circadian Clock
Open accessAbstract
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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
That cryptochromes might mediate magnetic responses in animals has been documented for the case of fruit flies.
“That cryptochromes might mediate magnetic responses in animals has also been documented for the case of fruit flies [101,102].”
From The future of quantum biology (2018) · cites this paper as [102]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor
Ahmad, M., & Cashmore, A. R. (1993) · Nature · doi:10.1038/366162a0 · Cited by 1,270 · see citing works
Self-citationA Model for Photoreceptor-Based Magnetoreception in Birds
Ritz, T., Adem, S., & Schulten, K. (2000) · Biophysical Journal · doi:10.1016/s0006-3495(00)76629-x · Cited by 1,176 · cited 3× · see citing works
“[10] calculated the yield of the triplet products in relation to the strength of the magnetic field and the angle of the field with respect to the alignment of the radical pair in space.”
BackgroundCryptochromes: Blue Light Receptors for Plants and Animals
Cashmore, A. R., Jarillo, J. A., Wu, Y., & Liu, D. (1999) · Science · doi:10.1126/science.284.5415.760 · Cited by 1,027 · see citing works
The chi square periodogram: Its utility for analysis of circadian rhythms
Sokolove, P. G., & Bushell, W. N. (1978) · Journal of Theoretical Biology · doi:10.1016/0022-5193(78)90022-x · Cited by 972 · see citing works
The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila
Stanewsky, R., Kaneko, M., Emery, P., Beretta, B., Wager-Smith, K., Kay, S. A., Rosbash, M., & Hall, J. C. (1998) · Cell · doi:10.1016/s0092-8674(00)81638-4 · Cited by 968 · see citing works
Emery, P., So, W. V., Kaneko, M., Hall, J. C., & Rosbash, M. (1998) · Cell · doi:10.1016/s0092-8674(00)81637-2 · Cited by 912 · see citing works
Magnetic Compass of European Robins
Wiltschko, W., & Wiltschko, R. (1972) · Science · doi:10.1126/science.176.4030.62 · Cited by 752 · see citing works
Light-Dependent Sequestration of TIMELESS by CRYPTOCHROME
Ceriani, M. F., Darlington, T. K., Staknis, D., Más, P., Petti, A. A., Weitz, C. J., & Kay, S. A. (1999) · Science · doi:10.1126/science.285.5427.553 · Cited by 565 · see citing works
Chemical magnetoreception in birds: The radical pair mechanism
Rodgers, C. T., & Hore, P. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711968106 · Cited by 542 · see citing works
Chemical compass model of avian magnetoreception
Maeda, K., Henbest, K. B., Cintolesi, F., Kuprov, I., Rodgers, C. T., Liddell, P. A., Gust, D., Timmel, C. R., & Hore, P. J. (2008) · Nature · doi:10.1038/nature06834 · Cited by 496 · see citing works
Cycling vrille Expression Is Required for a Functional Drosophila Clock
Blau, J., & Young, M. W. (1999) · Cell · doi:10.1016/s0092-8674(00)81554-8 · Cited by 439 · see citing works
A Biomagnetic Sensory Mechanism Based on Magnetic Field Modulated Coherent Electron Spin Motion
Schulten, K., Swenberg, C. E., & Weller, A. (1978) · Zeitschrift für Physikalische Chemie · doi:10.1524/zpch.1978.111.1.001 · Cited by 430 · see citing works
Cryptochrome mediates light-dependent magnetosensitivity in Drosophila
Gegear, R. J., Casselman, A., Waddell, S., & Reppert, S. M. (2008) · Nature · doi:10.1038/nature07183 · Cited by 421 · see citing works
Miyamoto, Y., & Sancar, A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.11.6097 · Cited by 406 · see citing works
Zhu, H., Šauman, I., Yuan, Q., Casselman, A. L., Emery-Le, M., Emery, P., & Reppert, S. M. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060004 · Cited by 321 · see citing works
Red light disrupts magnetic orientation of migratory birds
Wiltschko, W., Munro, U. H., FORD, H. A., & Wiltschko, R. (1993) · Nature · doi:10.1038/364525a0 · Cited by 314 · see citing works
Mouritsen, H., Janssen‐Bienhold, U., Liedvogel, M., Feenders, G., Stalleicken, J., Dirks, P., & Weiler, R. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405968101 · Cited by 304 · see citing works
Helfrich‐Förster, C. (1998) · Journal of Comparative Physiology A · doi:10.1007/s003590050192 · Cited by 298 · see citing works
Self-citationRoles of the Two Drosophila CRYPTOCHROME Structural Domains in Circadian Photoreception
Busza, A. C., Emery-Le, M., Rosbash, M., & Emery, P. (2004) · Science · doi:10.1126/science.1096973 · Cited by 292 · see citing works
Light-induced electron transfer in a cryptochrome blue-light photoreceptor
Giovani, B., Byrdin, M., Ahmad, M., & Brettel, K. (2003) · Nature Structural & Molecular Biology · doi:10.1038/nsb933 · Cited by 274 · see citing works
Self-citationCryptochrome: The Second Photoactive Pigment in the Eye and Its Role in Circadian Photoreception
Sancar, A. (2000) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.69.1.31 · Cited by 263 · see citing works
Rhodopsin: Insights from Recent Structural Studies
Sakmar, T. P., Menon, S. T., Marin, E. P., & Awad, E. S. (2002) · Annual Review of Biophysics and Biomolecular Structure · doi:10.1146/annurev.biophys.31.082901.134348 · Cited by 240 · see citing works
Konopka, R. J., Pittendrigh, C. S., & Orr, D. (1989) · Journal of Neurogenetics · doi:10.3109/01677068909107096 · Cited by 235 · see citing works
The Extraretinal Eyelet ofDrosophila: Development, Ultrastructure, and Putative Circadian Function
Helfrich‐Förster, C., Edwards, T. N., Yasuyama, K., Wisotzki, B., Schneuwly, S., Stanewsky, R., Meinertzhagen, I. A., & Hofbauer, A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-21-09255.2002 · Cited by 230 · see citing works
Self-citationCryptochrome is present in the compound eyes and a subset of Drosophila's clock neurons
Yoshii, T., Todo, T., Wülbeck, C., Stanewsky, R., & Helfrich‐Förster, C. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21702 · Cited by 226 · see citing works
Self-citationPrimary Reactions of the LOV2 Domain of Phototropin, a Plant Blue-Light Photoreceptor
Kennis, J. T. M., Crosson, S., Gauden, M., van Stokkum, I. H. M., Moffat, K., & van Grondelle, R. (2003) · Biochemistry · doi:10.1021/bi034022k · Cited by 221 · see citing works
Lateralization of magnetic compass orientation in a migratory bird
Wiltschko, W., Traudt, J., Güntürkün, O., Prior, H., & Wiltschko, R. (2002) · Nature · doi:10.1038/nature00958 · Cited by 217 · see citing works
A Novel Photoreaction Mechanism for the Circadian Blue Light Photoreceptor Drosophila Cryptochrome
Berndt, A., Kottke, T., Breitkreuz, H., Dvorský, R., Hennig, S., Alexander, M., & Wolf, E. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m608872200 · Cited by 212 · see citing works
Helfrich‐Förster, C. (2000) · Journal of Biological Rhythms · doi:10.1177/074873040001500208 · Cited by 209 · see citing works
Self-citationMagnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana
Ahmad, M., Galland, P., Ritz, T., Wiltschko, R., & Wiltschko, W. (2006) · Planta · doi:10.1007/s00425-006-0383-0 · Cited by 194 · see citing works
Self-citationMagnetic field effects on photosynthetic reactions
Hoff, A. J. (1981) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583500002481 · Cited by 176 · see citing works
Möller, A., Sagasser, S., Wiltschko, W., & Schierwater, B. (2004) · Naturwissenschaften · doi:10.1007/s00114-004-0578-9 · Cited by 173 · see citing works
Human and Drosophila Cryptochromes Are Light Activated by Flavin Photoreduction in Living Cells
Hoang, N., Schleicher, E., Kacprzak, S., Bouly, J., Picot, M., Wu, W., Berndt, A., Wolf, E., Bittl, R., & Ahmad, M. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060160 · Cited by 162 · see citing works
Self-citationWiltschko, W., & Wiltschko, R. (1995) · Journal of Comparative Physiology A · doi:10.1007/bf00192425 · Cited by 155 · see citing works
Rhythm Defects Caused by Newly Engineered Null Mutations in Drosophila's cryptochrome Gene
Doleželová, E., Doležel, D., & Hall, J. C. (2007) · Genetics · doi:10.1534/genetics.107.076513 · Cited by 154 · see citing works
Muheim, R., Bäckman, J., & Åkesson, S. (2002) · Journal of Experimental Biology · doi:10.1242/jeb.205.24.3845 · Cited by 151 · see citing works
Boxer, S. G., Chidsey, C. E. D., & Roelofs, M. G. (1983) · Annual Review of Physical Chemistry · doi:10.1146/annurev.pc.34.100183.002133 · Cited by 130 · see citing works
Response to Pervasive Geophysical Factors and the Biological Clock ProblemPreprint
Brown, F. A. (1960) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1960.025.01.007 · Cited by 125 · see citing works
Model for a Physiological Magnetic Compass
Schulten, K. J., & Windemuth, A. (1986) · Springer proceedings in physics · doi:10.1007/978-3-642-71526-6_16 · Cited by 115 · see citing works
Rieger, D., Fraunholz, C., Popp, J., Bichler, D., Dittmann, R., & Helfrich‐Förster, C. (2007) · Journal of Biological Rhythms · doi:10.1177/0748730407306198 · Cited by 112 · see citing works
Self-citationProbing the Relative Importance of Molecular Oscillations in the Circadian Clock
Zheng, X., & Sehgal, A. (2008) · Genetics · doi:10.1534/genetics.107.088658 · Cited by 112 · see citing works
Einflu� schwacher elektro-magnetischer Felder auf die circadiane Periodik des Menschen
Wever, R. A. (1968) · Die Naturwissenschaften · doi:10.1007/bf00593403 · Cited by 111 · see citing works
Benito, J., Houl, J. H., Roman, G., & Hardin, P. E. (2008) · Journal of Biological Rhythms · doi:10.1177/0748730408318588 · Cited by 104 · see citing works
Wavelength-dependent effects of light on magnetic compass orientation in Drosophila melanogaster
Phillips, J. B., & Sayeed, O. (1993) · Journal of Comparative Physiology A · doi:10.1007/bf00216612 · Cited by 100 · see citing works
Chains of single-domain magnetite particles in chinook salmon,Oncorhynchus tshawytscha
Kirschvink, J. L., Walker, M. M., Chang, S., Dizon, A. E., & Peterson, K. A. (1985) · Journal of Comparative Physiology A · doi:10.1007/bf00618127 · Cited by 96 · see citing works
Circadian activity rhythm influenced by near zero magnetic field
BLISS, V. L., & HEPPNER, F. H. (1976) · Nature · doi:10.1038/261411a0 · Cited by 96 · see citing works
Expression of mCLOCK and Other Circadian Clock‐Relevant Proteins in the Mouse Suprachiasmatic Nuclei
Maywood, E. S., O’Brien, J., & Hastings, M. H. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.00971.x · Cited by 91 · see citing works
Cryptochromes: sensory reception, transduction, and clock functions subserving circadian systems
Hall, J. C. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00117-3 · Cited by 89 · see citing works
Byrdin, M., Sartor, V., Eker, A. P. M., Vos, M. H., Aubert, C., Brettel, K., & Mathis, P. (2003) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2003.07.001 · Cited by 88 · see citing works
Shedding Light on Vertebrate Magnetoreception
Ritz, T., Dommer, D. H., & Phillips, J. B. (2002) · Neuron · doi:10.1016/s0896-6273(02)00707-9 · Cited by 87 · see citing works
Visual lateralization and homing in pigeons
Prior, H., Wiltschko, R., Stapput, K., Güntürkün, O., & Wiltschko, W. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.02.018 · Cited by 80 · see citing works
Action Spectrum of Drosophila Cryptochrome
VanVickle-Chavez, S. J., & Gelder, R. N. V. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m609314200 · Cited by 69 · see citing works
Perception of the geomagnetic field in the flyDrosophila melanogaster
Wehner, R., & Labhart, T. (1970) · Cellular and Molecular Life Sciences · doi:10.1007/bf02114135 · Cited by 46 · see citing works
Entrainment of Circadian Activity Rhythms in Mice by Electrostatic Fields
Dowse, H. B., & Palmer, J. D. (1969) · Nature · doi:10.1038/222564a0 · Cited by 40 · see citing works
TheDrosophilaCircadian Pacemaker Circuit: Pas de Deux or Tarantella?
Sheeba, V., Kaneko, M. A. N., Sharma, V. K., & Holmes, T. C. (2008) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409230701829128 · Cited by 36 · see citing works
Magnetic compass orientation by larval Drosophila melanogaster
Dommer, D. H., Gazzolo, P. J., Painter, M. S., & Phillips, J. B. (2008) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2008.02.001 · Cited by 33 · see citing works
Hardin, P. E., & Glossop, N. R. J. (1999) · Science · doi:10.1126/science.286.5449.2460 · Cited by 30 · see citing works
Engelmann, W., Hellrung, W., & Johnsson, A. (1996) · Bioelectromagnetics · doi:10.1002/(sici)1521-186x(1996)17:2 · Cited by 19 · see citing works
Radical pair state in photosystem II
Rutherford, A. W., & Thurnauer, M. C. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.23.7283 · Cited by 12 · see citing works
Die Bagdadbahn und ihre Kulturbedeutung
Frech, F. (1913) · Die Naturwissenschaften · doi:10.1007/bf01494410 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The cryptochromes: blue light photoreceptors in plants and animals
Chaves, I., Pokorny, R., Byrdin, M., Hoang, N., Ritz, T., Brettel, K., Essen, L.-O., van der Horst, G. T. J., Batschauer, A., & Ahmad, M. (2011) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042110-103759 · Cited by 845 · see citing works
Self-citationThe Radical-Pair Mechanism of Magnetoreception
Hore, P. J., & Mouritsen, H. (2016) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-032116-094545 · Cited by 813 · see citing works
Mechanisms and Mitochondrial Redox Signaling in Photobiomodulation
Hamblin, M. R. (2017) · Photochemistry and Photobiology · doi:10.1111/php.12864 · Cited by 854 · see citing works
Phototransduction Motifs and Variations
Yau, K., & Hardie, R. (2009) · Cell · doi:10.1016/j.cell.2009.09.029 · Cited by 488 · see citing works
Sustained Quantum Coherence and Entanglement in the Avian Compass
Gauger, E. M., Rieper, E., Morton, J. J. L., Benjamin, S. C., & Vedral, V. (2011) · Physical Review Letters · doi:10.1103/physrevlett.106.040503 · Cited by 357 · see citing works
Qin, S., Yin, H. H., Yang, C., Dou, Y., Liu, Z., Zhang, P., He, Y. H., Huang, Y., Feng, J., Hao, J., et al. (2015) · Nature Materials · doi:10.1038/nmat4484 · Cited by 350 · see citing works
The Cryptochrome Blue Light Receptors
Yu, X., Liu, H., John Klejnot, B., & Lin, C. (2010) · The Arabidopsis Book · doi:10.1199/tab.0135 · Cited by 337 · see citing works
Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism
Gegear, R. J., Foley, L. E., Casselman, A. L., & Reppert, S. M. (2010) · Nature · doi:10.1038/nature08719 · Cited by 289 · see citing works
Marais, A., Adams, B., Ringsmuth, A. K., Ferretti, M., Gruber, J. M., Hendrikx, R., Schuld, M., Smith, S. L., Sinayskiy, I., Krüger, T. P. J., et al. (2018) · Journal of The Royal Society Interface · doi:10.1098/rsif.2018.0640 · Cited by 274 · see citing works
Cryptochromes—a potential magnetoreceptor: what do we know and what do we want to know?
Liedvogel, M., & Mouritsen, H. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0411.focus · Cited by 231 · see citing works
Navigational mechanisms of migrating monarch butterflies
Reppert, S. M., Gegear, R. J., & Merlin, C. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.04.004 · Cited by 230 · see citing works
Setting the clock – by nature: Circadian rhythm in the fruitfly Drosophila melanogaster
Peschel, N., & Helfrich‐Förster, C. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.02.028 · Cited by 222 · see citing works
Self-citationHuman cryptochrome exhibits light-dependent magnetosensitivity
Foley, L. E., Gegear, R. J., & Reppert, S. M. (2011) · Nature Communications · doi:10.1038/ncomms1364 · Cited by 214 · see citing works
CRYPTOCHROME Is a Blue-Light Sensor That Regulates Neuronal Firing Rate
Fogle, K. J., Parson, K. G., Dahm, N. A., & Holmes, T. C. (2011) · Science · doi:10.1126/science.1199702 · Cited by 197 · see citing works
Magnetic field effects in biology from the perspective of the radical pair mechanism
Zadeh-Haghighi, H., & Simon, C. (2022) · Journal of The Royal Society Interface · doi:10.1098/rsif.2022.0325 · Cited by 197 · see citing works
Müller, P., & Ahmad, M. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.228940 · Cited by 190 · see citing works
Self-citationAvian Ultraviolet/Violet Cones Identified as Probable Magnetoreceptors
Nießner, C., Denzau, S., Gross, J. C., Peichl, L., Bischof, H., Fleissner, G., Wiltschko, W., & Wiltschko, R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020091 · Cited by 184 · see citing works
Chemical and structural analysis of a photoactive vertebrate cryptochrome from pigeon
Zoltowski, B. D., Chelliah, Y., Wickramaratne, A. C., Jarocha, L. E., Karki, N., Xu, W., Mouritsen, H., Hore, P. J., Hibbs, R. E., Green, C. B., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907875116 · Cited by 164 · see citing works
Structure of full-length Drosophila cryptochrome
Zoltowski, B. D., Vaidya, A. T., Top, D., Widom, J. M., Young, M. W., & Crane, B. R. (2011) · Nature · doi:10.1038/nature10618 · Cited by 162 · see citing works
Ritz, T., Ahmad, M., Mouritsen, H., Wiltschko, R., & Wiltschko, W. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0456.focus · Cited by 135 · see citing works
Self-citationGehring, W. J. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.96 · Cited by 128 · see citing works
Electron spin relaxation in cryptochrome-based magnetoreception
Kattnig, D. R., Solov’yov, I. A., & Hore, P. J. (2016) · Physical Chemistry Chemical Physics · doi:10.1039/c5cp06731f · Cited by 129 · see citing works
A radical sense of direction: signalling and mechanism in cryptochrome magnetoreception
Dodson, C. A., Hore, P. J., & Wallace, M. I. (2013) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2013.07.002 · Cited by 129 · see citing works
Decrypting Cryptochrome: Revealing the Molecular Identity of the Photoactivation Reaction
Solov’yov, I. A., Domratcheva, T. M., Shahi, A. R. M., & Schulten, K. J. (2012) · Journal of the American Chemical Society · doi:10.1021/ja3074819 · Cited by 121 · see citing works
Hogben, H. J., Efimova, O., Wagner-Rundell, N., Timmel, C. R., & Hore, P. J. (2009) · Chemical Physics Letters · doi:10.1016/j.cplett.2009.08.051 · Cited by 114 · see citing works
Chemical amplification of magnetic field effects relevant to avian magnetoreception
Kattnig, D. R., Evans, E. W., Déjean, V., Dodson, C. A., Wallace, M. I., Mackenzie, S. R., Timmel, C. R., & Hore, P. J. (2016) · Nature Chemistry · doi:10.1038/nchem.2447 · Cited by 114 · see citing works
An electromagnetic field disrupts negative geotaxis in Drosophila via a CRY-dependent pathway
Fedele, G., Green, E. W., Rosato, E., & Kyriacou, C. P. (2014) · Nature Communications · doi:10.1038/ncomms5391 · Cited by 113 · see citing works
Cryptochrome 2 mediates directional magnetoreception in cockroaches
Bazalová, O., Kvíčalová, M., Válková, T., Slabý, P., Bartoš, P., Netušil, R., Tomanová, K., Braeunig, P., Lee, H., Šauman, I., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1518622113 · Cited by 112 · see citing works
Pooam, M., Arthaut, L.-D., Burdick, D., Link, J. J., Martino, C. F., & Ahmad, M. (2018) · Planta · doi:10.1007/s00425-018-3002-y · Cited by 109 · see citing works
Self-citationPhillips, J. B., Jorge, P. E., & Muheim, R. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0459.focus · Cited by 110 · see citing works
Cryptochrome 1 mediates light-dependent inclination magnetosensing in monarch butterflies
Wan, G., Hayden, A. N., Iiams, S. E., & Merlin, C. (2021) · Nature Communications · doi:10.1038/s41467-021-21002-z · Cited by 110 · see citing works
The Role of Clock Genes in Pharmacology
Paschos, G. K., Baggs, J. E., Hogenesch, J. B., & FitzGerald, G. A. (2010) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.010909.105621 · Cited by 105 · see citing works
Millitesla magnetic field effects on the photocycle of an animal cryptochrome
Sheppard, D. M. W., Li, J., Henbest, K. B., Neil, S. R. T., Maeda, K., Storey, J. G., Schleicher, E., Biskup, T., Rodriguez, R., Weber, S., et al. (2017) · Scientific Reports · doi:10.1038/srep42228 · Cited by 100 · see citing works
Fedele, G., Edwards, M. D., Bhavnani, S., Hares, J. M., Murbach, M., Green, E. W., Dissel, S., Hastings, M. H., Rosato, E., & Kyriacou, C. P. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004804 · Cited by 98 · see citing works
Lüdemann, G., Solov’yov, I. A., Kubař, T., & Elstner, M. (2014) · Journal of the American Chemical Society · doi:10.1021/ja510550g · Cited by 95 · see citing works
Phillips, J. B., Muheim, R., & Jorge, P. E. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.020792 · Cited by 94 · see citing works
Anthropogenic radiofrequency electromagnetic fields as an emerging threat to wildlife orientation
Balmorí, A. (2015) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2015.02.077 · Cited by 90 · see citing works
Martel, J., Chang, S.-H., Chevalier, G., Ojcius, D. M., & Young, J. D. (2023) · Biomedical Journal · doi:10.1016/j.bj.2023.01.003 · Cited by 101 · see citing works
Circadian oscillator proteins across the kingdoms of life: structural aspects
Saini, R. V., Jaskólski, M., & Davis, S. J. (2019) · BMC Biology · doi:10.1186/s12915-018-0623-3 · Cited by 88 · see citing works
Inner retinal circadian clocks and non-visual photoreceptors: Novel players in the circadian system
Guido, M. E., Garbarino‐Pico, E., Contin, M. A., Valdez, D. J., Nieto, P. S., Verra, D. M., Acosta-Rodríguez, V. A., de Zavalía, N., & Rosenstein, R. E. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.08.005 · Cited by 83 · see citing works
Dufor, T., Grehl, S., Tang, A. D., Doulazmi, M., Traoré, M., Debray, N., Dubacq, C., Deng, Z., Mariani, J., Lohof, A. M., et al. (2019) · Science Advances · doi:10.1126/sciadv.aav9847 · Cited by 80 · see citing works
Pinzon-Rodriguez, A., Bensch, S., & Muheim, R. (2018) · Journal of The Royal Society Interface · doi:10.1098/rsif.2018.0058 · Cited by 75 · see citing works
Cryptochrome magnetoreception: four tryptophans could be better than three
Wong, S. Y., Wei, Y., Mouritsen, H., Solov’yov, I. A., & Hore, P. J. (2021) · Journal of The Royal Society Interface · doi:10.1098/rsif.2021.0601 · Cited by 76 · see citing works
Cryptochrome-dependent magnetic field effect on seizure response in Drosophila larvae
Marley, R., Giachello, C. N., Scrutton, N. S., Baines, R., & Jones, A. R. (2014) · Scientific Reports · doi:10.1038/srep05799 · Cited by 73 · see citing works
Jing, D., Shen, G., Huang, J., Xie, K., Cai, J., Xu, Q., Wu, X., & Luo, E. (2009) · Bone · doi:10.1016/j.bone.2009.09.021 · Cited by 71 · see citing works
Molecular evolution and functional divergence of zebrafish (Danio rerio) cryptochrome genes
Liu, C., Hu, J. M., Qu, C., Wang, L., Huang, G., Niu, P., Zhong, Z., Hong, F., Wang, G., Postlethwait, J. H., et al. (2015) · Scientific Reports · doi:10.1038/srep08113 · Cited by 71 · see citing works
A Mechanosensory Pathway to the Drosophila Circadian Clock
Simoni, A., Wolfgang, W., Topping, M. P., Kavlie, R. G., Stanewsky, R., & Albert, J. T. (2014) · Science · doi:10.1126/science.1245710 · Cited by 68 · see citing works
Kattnig, D. R., & Hore, P. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-09914-7 · Cited by 70 · see citing works
Quantum effects in biology: Bird navigation
Ritz, T. (2011) · Procedia Chemistry · doi:10.1016/j.proche.2011.08.034 · Cited by 67 · see citing works
Loss of Timeless Underlies an Evolutionary Transition within the Circadian Clock
Kotwica‐Rolinska, J., Chodáková, L., Smýkal, V., Damulewicz, M., Provazník, J., Wu, B. C.-H., Hejníková, M., Chvalová, D., & Doležel, D. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab346 · Cited by 63 · see citing works
Roberts, L., Leise, T., Noguchi, T., Galschiodt, A. M., Houl, J. H., Welsh, D. K., & Holmes, T. C. (2015) · Current Biology · doi:10.1016/j.cub.2015.01.056 · Cited by 62 · see citing works
Hammad, M., Albaqami, M., Pooam, M., Kernevez, E., Witczak, J., Ritz, T., Martino, C. F., & Ahmad, M. (2020) · Photochemical & Photobiological Sciences · doi:10.1039/c9pp00469f · Cited by 62 · see citing works
Self-citationMagnetic Fields Modulate Blue-Light-Dependent Regulation of Neuronal Firing by Cryptochrome
Giachello, C. N., Scrutton, N. S., Jones, A. R., & Baines, R. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2140-16.2016 · Cited by 58 · see citing works
Magnetocarcinogenesis: is there a mechanism for carcinogenic effects of weak magnetic fields?
Juutilainen, J., Herrala, M., Luukkonen, J., Naarala, J., & Hore, P. J. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2018.0590 · Cited by 62 · see citing works
Rhythms of behavior: are the times changin’?
Häfker, N. S., & Tessmar‐Raible, K. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.10.005 · Cited by 58 · see citing works
Photoactivation of the cryptochrome/photolyase superfamily
Wang, J., Du, X., Pan, W., Wang, X., & Wu, W. (2014) · Journal of Photochemistry and Photobiology C Photochemistry Reviews · doi:10.1016/j.jphotochemrev.2014.12.001 · Cited by 56 · see citing works
Wan, G., Jiang, S., Zhao, Z., Xu, J., Tao, X., Sword, G. A., Gao, Y., Pan, W., & Chen, F. (2014) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2014.06.016 · Cited by 52 · see citing works
Lau, J. C. S., Rodgers, C. T., & Hore, P. J. (2012) · Journal of The Royal Society Interface · doi:10.1098/rsif.2012.0374 · Cited by 52 · see citing works
Positive geotactic behaviors induced by geomagnetic field in Drosophila
Bae, J.-E., Bang, S., Min, S., Lee, S., Kwon, S., Lee, Y., Lee, Y., Chung, J., & Chae, K. S. (2016) · Molecular Brain · doi:10.1186/s13041-016-0235-1 · Cited by 53 · see citing works
No evidence for magnetic field effects on the behaviour of Drosophila
Bassetto, M., Reichl, T., Kobylkov, D., Kattnig, D. R., Michael Winklhofer, A., Hore, P. J., & Mouritsen, H. (2023) · Nature · doi:10.1038/s41586-023-06397-7 · Cited by 53 · see citing works
Mechanism of Photosignaling by Drosophila Cryptochrome
Öztürk, N., Selby, C. P., Zhong, D., & Sancar, A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.542498 · Cited by 54 · see citing works
Cellular metabolites modulate in vivo signaling of Arabidopsis cryptochrome-1
El-Esawi, M. A., Glascoe, A., Engle, D., Ritz, T., Link, J. J., & Ahmad, M. (2015) · Plant Signaling & Behavior · doi:10.1080/15592324.2015.1063758 · Cited by 51 · see citing works
Self-citationAre stress responses to geomagnetic storms mediated by the cryptochrome compass system?
Close, J. (2012) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2012.0324 · Cited by 49 · see citing works
Biological effects related to geomagnetic activity and possible mechanisms
Крылов, В. В. (2017) · Bioelectromagnetics · doi:10.1002/bem.22062 · Cited by 50 · see citing works
Circadian clocks: an overview on its adaptive significance
Krittika, S., & Yadav, P. (2020) · Biological Rhythm Research · doi:10.1080/09291016.2019.1581480 · Cited by 50 · see citing works
Light Might Directly Affect Retinal Ganglion Cell Mitochondria to Potentially Influence Function†
del Olmo‐Aguado, S., Manso, A. G., & Osborne, N. N. (2012) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2012.01120.x · Cited by 49 · see citing works
A light-dependent magnetoreception mechanism insensitive to light intensity and polarization
Worster, S. B., Mouritsen, H., & Hore, P. J. (2017) · Journal of The Royal Society Interface · doi:10.1098/rsif.2017.0405 · Cited by 46 · see citing works
Cryptochromes: Photochemical and structural insight into magnetoreception
Karki, N., Vergish, S., & Zoltowski, B. D. (2021) · Protein Science · doi:10.1002/pro.4124 · Cited by 45 · see citing works
Cryptochrome: A photoreceptor with the properties of a magnetoreceptor?
Ritz, T., Yoshii, T., Foerster, C., & Ahmad, M. (2010) · Communicative & Integrative Biology · doi:10.4161/cib.3.1.9865 · Cited by 45 · see citing works
Self-citationAnti-aging effects of long-term space missions, estimated by heart rate variability
Otsuka, K., Cornelissen, G., Kubo, Y., Shibata, K., Mizuno, K., Ohshima, H., Furukawa, S., & Mukai, C. (2019) · Scientific Reports · doi:10.1038/s41598-019-45387-6 · Cited by 45 · see citing works
Magnetic field effects in proteins
Jones, A. R. (2016) · Molecular Physics · doi:10.1080/00268976.2016.1149631 · Cited by 42 · see citing works
Can disordered radical pair systems provide a basis for a magnetic compass in animals?
Hill, E. M., & Ritz, T. (2009) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0378.focus · Cited by 38 · see citing works
One Actor, Multiple Roles: The Performances of Cryptochrome in Drosophila
Damulewicz, M., & Mazzotta, G. M. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00099 · Cited by 37 · see citing works
Rishabh, R., Zadeh‐Haghighi, H., Salahub, D. R., & Simon, C. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1010198 · Cited by 38 · see citing works
Biological Effects of Space Hypomagnetic Environment on Circadian Rhythm
Xue, X., Ali, Y. F., Luo, W., Liu, C., Zhou, G., & Liu, N. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.643943 · Cited by 37 · see citing works
Light-dependent magnetic compass in Iberian green frog tadpoles
Diego‐Rasilla, F. J., Luengo, R. M., & Phillips, J. B. (2010) · Die Naturwissenschaften · doi:10.1007/s00114-010-0730-7 · Cited by 34 · see citing works
Wan, G., Wang, W., Xu, J., Yang, Q., Dai, M.-J., Zhang, F., Sword, G. A., Pan, W., & Chen, F. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132966 · Cited by 33 · see citing works
Painter, M. S., Dommer, D. H., Altizer, W. W., Muheim, R., & Phillips, J. B. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.077404 · Cited by 34 · see citing works
Agliassa, C., & Maffei, M. E. (2018) · Journal of Plant Physiology · doi:10.1016/j.jplph.2018.11.008 · Cited by 33 · see citing works
Arabidopsis cryptochrome is responsive to Radiofrequency (RF) electromagnetic fields
Albaqami, M., Hammad, M., Pooam, M., Procopio, M., Sameti, M., Ritz, T., Ahmad, M., & Martino, C. F. (2020) · Scientific Reports · doi:10.1038/s41598-020-67165-5 · Cited by 31 · see citing works
Self-citationLandscape Analysis of Drone Congregation Areas of the Honey Bee,Apis mellifera
Galindo‐Cardona, A., Monmany-Garzia, A. C., Moreno-Jackson, R., Rivera-Rivera, C. J., Huertas-Dones, C., Caicedo-Quiroga, L., & Giray, T. (2012) · Journal of insect science/Journal of Insect Science · doi:10.1673/031.012.12201 · Cited by 31 · see citing works
van Belkum, S. M., Bosker, F. J., Kortekaas, R., Beersma, D. G. M., & Schoevers, R. A. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.07.006 · Cited by 29 · see citing works
Weak radiofrequency fields affect the insect circadian clock
Bartoš, P., Netušil, R., Slabý, P., Doležel, D., Ritz, T., & Vácha, M. (2019) · Journal of The Royal Society Interface · doi:10.1098/rsif.2019.0285 · Cited by 29 · see citing works
Friedmann, H., Lipovsky, A., Nitzan, Y., & Lubart, R. (2009) · LASER THERAPY · doi:10.5978/islsm.18.137 · Cited by 28 · see citing works
How do honeybees use their magnetic compass? Can they see the North?
Válková, T., & Vácha, M. (2012) · Bulletin of Entomological Research · doi:10.1017/s0007485311000824 · Cited by 28 · see citing works
Helfrich‐Förster, C. (2017) · Springer eBooks · doi:10.1007/978-81-322-3688-7_6 · Cited by 27 · see citing works
Self-citationRadical pairs can explain magnetic field and lithium effects on the circadian clock
Zadeh‐Haghighi, H., & Simon, C. (2022) · Scientific Reports · doi:10.1038/s41598-021-04334-0 · Cited by 27 · see citing works
Nimpf, S., & Keays, D. A. (2022) · iScience · doi:10.1016/j.isci.2022.104454 · Cited by 28 · see citing works
An open quantum system approach to the radical pair mechanism
Adams, B., Sinayskiy, I., & Petruccione, F. (2018) · Scientific Reports · doi:10.1038/s41598-018-34007-4 · Cited by 26 · see citing works
Drosophila Cryptochrome: Variations in Blue
Foley, L. E., & Emery, P. (2019) · Journal of Biological Rhythms · doi:10.1177/0748730419878290 · Cited by 25 · see citing works
Höytö, A., Herrala, M., Luukkonen, J., Juutilainen, J., & Naarala, J. (2017) · International Journal of Radiation Biology · doi:10.1080/09553002.2017.1294275 · Cited by 26 · see citing works
Roles of peripheral clocks: lessons from the fly
Yildirim, E., Curtis, R., & Hwangbo, D. (2021) · FEBS Letters · doi:10.1002/1873-3468.14251 · Cited by 25 · see citing works
Honey bees possess a polarity-sensitive magnetoreceptor
Lambinet, V., Hayden, M. E., Reid, C., & Gries, G. (2017) · Journal of Comparative Physiology A · doi:10.1007/s00359-017-1214-4 · Cited by 25 · see citing works
Friis, I., Sjulstok, E., & Solov’yov, I. A. (2017) · Scientific Reports · doi:10.1038/s41598-017-13258-7 · Cited by 25 · see citing works
Impact of Static Magnetic Field (SMF) on Microorganisms, Plants and Animals
Zhang, X., Yarema, K. J., & Xu, A. (2017) · Springer eBooks · doi:10.1007/978-981-10-3579-1_5 · Cited by 24 · see citing works
The circadian activity rhythm is reset by nanowatt pulses of ultraviolet light
Negelspach, D., Kaladchibachi, S., & Fernandez, F. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2018.1288 · Cited by 24 · see citing works
Li, S., Huang, A., Jiang, T., Gu, H., Zeng, F., Wang, X., & Zhang, S. (2023) · Journal of Molecular Liquids · doi:10.1016/j.molliq.2023.121391 · Cited by 24 · see citing works
Netušil, R., Tomanová, K., Chodáková, L., Chvalová, D., Doležel, D., Ritz, T., & Vácha, M. (2021) · Journal of Experimental Biology · doi:10.1242/jeb.243000 · Cited by 23 · see citing works
Magnetoreception Regulates Male Courtship Activity in Drosophila
Wu, C., Fu, T., Chiang, M.-H., Chang, Y.-W., Her, J.-L., & Wu, T. (2016) · PLoS ONE · doi:10.1371/journal.pone.0155942 · Cited by 22 · see citing works
Wan, G.-J., Yuan, R., Wang, W.-J., Fu, K., Zhao, J., Jiang, S., Pan, W., Sword, G. A., & Chen, F. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.08.024 · Cited by 22 · see citing works
- Authors
- Yoshii, T., Ahmad, M., & Helfrich-Förster, C.
- Affiliations
- University of Regensburg (DE)
- Université Pierre-et-Marie-Curie (FR)
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2009-04-07
- Volume
- 7
- Issue
- 4
- Pages
- e1000086
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC2667543
- OpenAlex
- W1981618051
- Cited by
- 232
- References
- 60
- Citations by year
- 2026: 10 · 2025: 8 · 2024: 11 · 2023: 9 · 2022: 14 · 2021: 14 · 2020: 9 · 2019: 23 · 2018: 17 · 2017: 19 · 2016: 17 · 2015: 10 · 2014: 13 · 2013: 7 · 2012: 12
- FWCI
- 7.63
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Electromagnetic Fields and Biological Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Magnetic and Electromagnetic Effects
- Keywords
- cryptochrome, magnetic field sensitivity, circadian clock, Drosophila, radical pair mechanism, clock neurons, blue light, magnetic compass, bird migration
- MeSH terms
- Animals, Biological Clocks, Circadian Rhythm, Drosophila melanogaster, Flavoproteins, Light, Locomotion, Magnetics, Photoreceptor Cells, Invertebrate, Drosophila Proteins, Cryptochromes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review