Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 13, 2012, Pages 4774-4779

  Maeda, Kiminori ^a   Robinson, Alexander J ^a   Henbest, Kevin B ^a   Hogben, Hannah J ^a   Biskup, Till ^a   Ahmad, Margaret ^b,c   Schleicher, Erik ^d   Weber, Stefan ^d   Timmel, Christiane R ^a   Hore, P J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b SORBONNE UNIVERSITÉ   (France)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Magnetic compass; Magnetoreception; Migratory birds; Quantum biology; Radical pair mechanism

Indexed keywords

CRYPTOCHROME; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; QUERCETIN; TRYPTOPHAN;

ABSORPTION SPECTROSCOPY; ACCELERATION; ARABIDOPSIS; ARTICLE; ATTENUATION; CHEMICAL REACTION; ELECTRON TRANSPORT; ESCHERICHIA COLI; KINETICS; LIGHT; MAGNETIC FIELD; MAGNETISM; MOLECULAR DYNAMICS; NONHUMAN; PHOTOCHEMISTRY; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTON TRANSPORT; QUANTUM YIELD; SIGNAL TRANSDUCTION;

ABSORPTION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CRYPTOCHROMES; ELECTRONS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLAVIN-ADENINE DINUCLEOTIDE; KINETICS; LIGHT; MAGNETIC FIELDS; MAGNETICS; PHOTOCHEMISTRY; RECEPTORS, CELL SURFACE; SPECTRUM ANALYSIS; TRYPTOPHAN;

AVES;

EID: 84859470589     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1118959109     Document Type: Article

References (48)

1. Ahmad M, Cashmore AR (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162-166.
2. Chaves I, et al. (2011) The cryptochromes: Blue light photoreceptors in plants and animals. Annu Rev Plant Biol 62:335-364.
3. Weber S (2005) Light-driven enzymatic catalysis of DNA repair: A review of recent biophysical studies on photolyase. Biochim Biophys Acta 1707:1-23.
4. Sancar A (2008) Structure and function of photolyase and in vivo enzymology: 50th anniversary. J Biol Chem 283:32153-32157.
5. Ritz T, Adem S, Schulten K (2000) A model for photoreceptor-based magnetoreception in birds. Biophys J 78:707-718.
6. Schulten K, Swenberg CE, Weller A (1978) A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Z Phys Chem NF 111:1-5.
7. Rodgers CT (2009) Magnetic field effects in chemical systems. Pure Appl Chem 81:19-43.
8. Gindt YM, et al. (1999) Origin of the transient electron paramagnetic resonance signals in DNA photolyase. Biochemistry 38:3857-3866.
9. Giovani B, Byrdin M, Ahmad M, Brettel K (2003) Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nat Struct Biol 10:489-490.
10. Zeugner A, et al. (2005) Light-induced electron transfer in Arabidopsis cryptochrome-1 correlates with in vivo function. J Biol Chem 280:19437-19440.
11. Biskup T, et al. (2009) Direct observation of a photoinduced radical-pair intermediate in a cryptochrome DASH blue-light photoreceptor. Angew Chem Int Ed 48:404-407.
12. Banerjee R, et al. (2007) The signaling state of Arabidopsis cryptochrome 2 contains flavin semiquinone. J Biol Chem 282:14916-14922.
13. Bouly JP, et al. (2007) Cryptochrome blue light photoreceptors are activated through interconversion of flavin redox states. J Biol Chem 282:9383-9391.
14. Rodgers CT, Hore PJ (2009) Chemical magnetoreception in birds: A radical pair mechanism. Proc Natl Acad Sci USA 106:353-360.
15. Liedvogel M, Mouritsen H (2010) Cryptochromes - a potential magnetoreceptor: What do we know and what do we want to know? J Roy Soc Interface 7:S147-S162.
16. Ahlbom A, et al. (2000) A pooled analysis of magnetic fields and childhood leukaemia. Brit J Cancer 83:692-698.
17. Greenland S, et al. (2000) A pooled analysis of magnetic fields, wire codes, and childhood leukemia. Epidemiology 11:624-634.
18. International Agency for Research on Cancer (2002) Static and extremely low-frequency (ELF) electric and magnetic fields. IARC monographs on the evaluation of carcinogenic risks to humans, vol. 80 (IARC, Lyon).
19. Advisory Group on Non-ionising Radiation (2001) AGNIR (2001) ELF electromagnetic fields and the risk of cancer. Report of an Advisory Group on Non-ionising Radiation. Documents of the NRPB, Vol. 12 (National Radiological Protection Board, Chilton, Oxon, UK).
20. Reddy AB, Wong GKY, O'Neill J, Maywood ES, Hastings MH (2005) Circadian clocks: Neural and peripheral pacemakers that impact upon the cell division cycle. Mutat Res 574:76-91.
21. Timmel CR, Till U, Brocklehurst B, McLauchlan KA, Hore PJ (1998) Effects of weak magnetic fields on free radical recombination reactions. Mol Phys 95:71-89.
22. Lagroye I, Percherancier Y, Juutilainen J, Poulletier De Gannes F, Veyret B (2011) ELF magnetic fields: Animal studies, mechanisms of action. Prog Biophys Mol Biol 107:369-373.
23. Henbest KB, et al. (2008) Magnetic-field effect on the photoactivation reaction of Escherichia coli DNA photolyase. Proc Natl Acad Sci USA 105:14395-14399.
24. Langenbacher T, Immeln D, Dick B, Kottke T (2009) Microsecond light-induced proton transfer to flavin in the blue light sensor plant cryptochrome. J Am Chem Soc 131:14274-14280.
25. Aubert C, Mathis P, Eker APM, Brettel K (1999) Intraprotein electron transfer between tyrosine and tryptophan in DNA photolyase from anacystis nidulans. Proc Natl Acad Sci USA 96:5423-5427.
26. Popović DM, Zmiric A, Zaric SD, Knapp EW (2002) Energetics of radical transfer in DNA photolyase. J Am Chem Soc 124:3775-3782.
27. Weber S, et al. (2002) Photoactivation of the flavin cofactor in Xenopus laevis (6-4) photolyase: Observation of a transient tyrosyl radical by time-resolved electron paramagnetic resonance. Proc Natl Acad Sci USA 99:1319-1322.
28. Li YF, Heelis PF, Sancar A (1991) Active-site of DNA photolyase - tryptophan-306 is the intrinsic hydrogen-atom donor essential for flavin radical photoreduction and DNA-repair in vitro. Biochemistry 30:6322-6329.
29. Brettel K, Byrdin M (2010) Reaction mechanisms of DNA photolyase. Curr Opin Struct Biol 20:693-701.
30. Byrdin M, et al. (2004) Intraprotein electron transfer and proton dynamics during photoactivation of DNA photolyase from E. coli: Review and new insights from an "inverse" deuterium isotope effect. Biochim Biophys Acta 1655:64-70.
31. Weller A, Nolting F, Staerk H (1983) A quantitative interpretation of the magnetic-field effect on hyperfine-coupling-induced triplet formation from radical ion-pairs. Chem Phys Lett 96:24-27.
32. Miura T, Maeda K, Arai T (2006) The spin mixing process of a radical pair in low magnetic field observed by transient absorption detected nanosecond pulsed magnetic field effect. J Phys Chem A 110:4151-4156.
33. Shushin AI (1991) The effect of the spin exchange interaction on SNP and RYDMR spectra of geminate radical pairs. Chem Phys Lett 181:274-278.
34. Woiczikowski PB, Steinbrecher T, Kubar T, Elstner M (2011) Nonadiabatic QM/MM simulations of fast charge transfer in Escherichia coli DNA photolyase. J Phys Chem B 115:9846-9863.
35. Krapf S, Koslowski T, Steinbrecher T (2010) The thermodynamics of charge transfer in DNA photolyase: Using thermodynamic integration calculations to analyse the kinetics of electron transfer reactions. Phys Chem Chem Phys 12:9516-9525.
36. Efimova O, Hore PJ (2008) Role of exchange and dipolar interactions in the radical pair model of the avian magnetic compass. Biophys J 94:1565-1574.
37. Brautigam CA, et al. (2004) Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana. Proc Natl Acad Sci USA 101:12142-12147.
38. Eveson RW, Timmel CR, Brocklehurst B, Hore PJ, McLauchlan KA (2000) The effects of weak magnetic fields on radical recombination reactions in micelles. Int J Radiat Biol 76:1509-1522.
39. Brocklehurst B (1976) Spin correlation in geminate recombination of radical ions in hydrocarbons. 1. Theory of magnetic-field effect. J Chem Soc Faraday Trans II 72:1869-1884.
40. Kirschvink JL, Winklhofer M, Walker MM (2010) Biophysics of magnetic orientation: Strengthening the interface between theory and experimental design. J R Soc Interface 7:S179-S191.
41. Zuo Z, Liu H, Liu B, Liu X, Lin C (2011) Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis. Curr Biol 21:841-847.
42. Liu B, Liu H, Zhong D, Lin C (2010) Searching for a photocycle of the cryptochrome photoreceptors. Curr Opin Plant Biol 13:578-586.
43. Partch CL, Sancar A (2005) Photochemistry and photobiology of cryptochrome blue-light photopigments: The search for a photocycle. Photochem Photobiol 81:1291-1304.
44. Bouly J, et al. (2003) Novel ATP-binding and autophosphorylation activity associated with Arabidopsis and human cryptochrome-1. Eur J Biochem 270:2921-2928.
45. Sang Y, et al. (2005) N-terminal domain-mediated homodimerization is required for photoreceptor activity of Arabidopsis cryptochrome 1. Plant Cell 17:1569-1584.
46. Kondoh M, et al. (2011) Light-induced conformational changes in full-length Arabidopsis thaliana cryptochrome. J Mol Biol 413:128-137.
47. Schleicher E, et al. (2005) Light-induced reactions of Escherichia coli DNA photolyase monitored by Fourier transform infrared spectroscopy. FEBS J 272:1855-1866.
48. Park H-W, Kim S-T, Sancar A, Deisenhofer J (1995) Crystal structure of DNA photolyase from Escherichia coli. Science 268:1866-1872.