New roles of flavoproteins in molecular cell biology: Blue-light active flavoproteins studied by electron paramagnetic resonance

FEBS Journal

Volumn 276, Issue 16, 2009, Pages 4290-4303

  Schleicher, Erik ^a   Bittl, Robert ^b   Weber, Stefan ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Cryptochrome; DNA repair; ENDOR; EPR; ESR; Flavoprotein; Paramagnetic intermediates; Photolyase; Photoreceptor; Radical pair

Indexed keywords

CRYPTOCHROME; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; FLAVOPROTEIN;

CATALYSIS; CIRCADIAN RHYTHM; CYTOLOGY; DNA DAMAGE; ELECTRON NUCLEAR DOUBLE RESONANCE; ELECTRON SPIN RESONANCE; INTERMETHOD COMPARISON; MOLECULAR BIOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN STRUCTURE; SHORT SURVEY; WILD TYPE; X RAY CRYSTALLOGRAPHY;

CIRCADIAN RHYTHM; DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DNA REPAIR; ELECTRON SPIN RESONANCE SPECTROSCOPY; FLAVOPROTEINS; LIGHT;

EID: 68749097389     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07141.x     Document Type: Short Survey

References (88)

1. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA Ellenberger T (2006) DNA Repair and Mutagenesis, 2nd edn. ASM Press, Washington, DC.
2. Weber S (2005) Light-driven enzymatic catalysis of DNA repair: a review of recent biophysical studies on photolyase. Biochim Biophys Acta 1707, 1 23.
3. Essen L-O (2006) Photolyases and cryptochromes: common mechanisms of DNA repair and light-driven signaling? Curr Opin Struct Biol 16, 51 59.
4. Sancar A (2008) Structure and function of photolyase and in vivo enzymology: 50th anniversary. J Biol Chem 283, 32153 32157.
5. Todo T (1999) Functional diversity of the DNA photolyase/blue light receptor family. Mutat Res 434, 89 97.
6. Todo T, Ryo H, Yamamoto K, Toh H, Inui T, Ayaki H, Nomura T Ikenaga M (1996) Similarity among the Drosophila (6-4) photolyase, a human photolyase homolog, and the DNA photolyase-blue-light photoreceptor family. Science 272, 109 112.
7. Nakajima S, Sugiyama M, Iwai S, Hitomi K, Otoshi E, Kim S-T, Jiang C-Z, Todo T, Britt AB Yamamoto K (1998) Cloning and characterization of a gene (UVR3) required for photorepair of 6-4 photoproducts in Arabidopsis thaliana. Nucleic Acids Res 26, 638 644.
8. Sancar A Sancar GB (1984) Escherichia coli DNA photolyase is a flavoprotein. J Mol Biol 172, 223 227.
9. Todo T, Kim S-T, Hitomi K, Otoshi E, Inui T, Morioka H, Kobayashi H, Ohtsuka E, Toh H Ikenaga M (1997) Flavin adenine dinucleotide as a chromophore of the Xenopus (6-4) photolyase. Nucleic Acids Res 25, 764 768.
10. Jorns MS, Sancar GB Sancar A (1984) Identification of a neutral flavin radical and characterization of a second chromophore in Escherichia coli DNA photolyase. Biochemistry 23, 2673 2679.
11. Eker APM, Kooiman P, Hessels JKC Yasui A (1990) DNA photoreactivating enzyme from the cyanobacterium Anacystis nidulans. J Biol Chem 265, 8009 8015.
12. Lin C Todo T (2005) The cryptochromes. Genome Biol 6, Art. No. 220.
13. Cashmore AR (2003) Cryptochromes: enabling plants and animals to determine circadian time. Cell (Cambridge, Mass) 114, 537 543.
14. Partch CL Sancar A (2005) Photochemistry and photobiology of cryptochrome blue-light photopigments: the search for a photocycle. Photochem Photobiol 81, 1291 1304.
15. Brudler R, Hitomi K, Daiyasu H, Toh H, Kucho K-i, Ishiura M, Kanehisa M, Roberts VA, Todo T, Tainer JA et al. (2003) Identification of a new cryptochrome class: structure, function, and evolution. Mol Cell 11, 59 67.
16. Selby CP Sancar A (2006) A cryptochrome/photolyase class of enzymes with single-stranded DNA-specific photolyase activity. Proc Natl Acad Sci USA 103, 17696 17700.
17. Pokorny R, Klar T, Hennecke U, Carell T, Batschauer A Essen L-O (2008) Recognition and repair of UV lesions in loop structures of duplex DNA by DASH-type cryptochrome. Proc Natl Acad Sci USA 105, 21023 21027.
18. Ceriani MF, Darlington TK, Staknis D, Más P, Petti AA, Weitz CJ Kay SA (1999) Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science 285, 553 556.
19. van der Horst GTJ, Muijtjens M, Kobayashi K, Takano R, Kanno S-i, Takao M, de Wit J, Verkerk A, Eker APM, van Leenen D et al. (1999) Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398, 627 630.
20. Li Q-H Yang H-Q (2007) Cryptochrome signaling in plants. Photochem Photobiol 83, 94 101.
21. Gegear RJ, Casselman A, Waddell S Reppert SM (2008) Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature 454, 1014 1018.
22. Mouritsen H Ritz T (2005) Magnetoreception and its use in bird navigation. Curr Opin Neurobiol 15, 406 414.
23. Rodgers CT Hore PJ (2009) Chemical magnetoreception in birds: the radical pair mechanism. Proc Natl Acad Sci USA 106, 353 360.
24. Yang H-Q, Wu Y-J, Tang R-H, Liu D, Liu Y Cashmore AR (2000) The C termini of Arabidopsis cryptochromes mediate a constitutive light response. Cell (Cambridge, Mass) 103, 815 827.
25. Klar T, Pokorny R, Moldt J, Batschauer A Essen L-O (2007) Cryptochrome 3 from Arabidopsis thaliana: structural and functional analysis of its complex with a folate light antenna. J Mol Biol 366, 954 964.
26. Edmondson DE (1985) Electron-spin-resonance studies on flavoenzymes. Biochem Soc Trans 13, 593 600.
27. Kay CWM Weber S (2002) EPR of radical intermediates in flavoenzymes. In Electron Paramagnetic Resonance (Gilbert BC, Davies MJ Murphy DM, eds pp. 222 253. Royal Society of Chemistry, Cambridge, UK.
28. Weber S, Kay CWM, Bacher A, Richter G Bittl R (2005) Probing the N(5)-H bond of the isoalloxazine moiety of flavin radicals by X- and W-band pulsed electron-nuclear double resonance. ChemPhysChem 6, 292 299.
29. García JI, Medina M, Sancho J, Alonso PJ, Gómez-Moreno C, Mayoral JA Martínez JI (2002) Theoretical analysis of the electron spin density distribution of the flavin semiquinone isoalloxazine ring within model protein environments. J Phys Chem A 106, 4729 4735.
30. Fuchs M, Schleicher E, Schnegg A, Kay CWM, Törring JT, Bittl R, Bacher A, Richter G, Möbius K Weber S (2002) The g-tensor of the neutral flavin radical cofactor of DNA photolyase revealed by 360-GHz electron paramagnetic resonance spectroscopy. J Phys Chem B 106, 8885 8890. (Pubitemid 35382897)
31. +-translocating NADH:quinone oxidoreductase from Vibrio cholerae. J Am Chem Soc 125, 265 275.
32. Kay CWM, Bittl R, Bacher A, Richter G Weber S (2005) Unambiguous determination of the g-matrix orientation in a neutral flavin radical by pulsed electron-nuclear double resonance at 94 GHz. J Am Chem Soc 127, 10780 10781. (Pubitemid 41129824)
33. Schnegg A, Kay CWM, Schleicher E, Hitomi K, Todo T, Möbius K Weber S (2006) The g-tensor of the flavin cofactor in (6-4) photolyase: a 360 GHz/12.8 T electron paramagnetic resonance study. Mol Phys 104, 1627 1633.
34. Schnegg A, Okafuji A, Bacher A, Bittl R, Fischer M, Fuchs MR, Hegemann P, Joshi M, Kay CWM, Richter G et al. (2006) Towards an identification of chemically different flavin radicals by means of their g-tensor. Appl Magn Reson 30, 345 358.
35. Okafuji A, Schnegg A, Schleicher E, Möbius K Weber S (2008) G-tensors of the flavin adenine dinucleotide radicals in glucose oxidase: a comparative multifrequency electron paramagnetic resonance and electron-nuclear double resonance study. J Phys Chem B 112, 3568 3574.
36. Kay CWM, El Mkami H, Molla G, Pollegioni L Ramsay RR (2007) Characterization of the covalently bound anionic flavin radical in monoamine oxidase A by electron paramagnetic resonance. J Am Chem Soc 129, 16091 16097.
37. Murphy DM Farley RD (2006) Principles and applications of ENDOR spectroscopy for structure determination in solution and disordered matrices. Chem Soc Rev 35, 249 268.
38. van Doorslaer S Vinck E (2007) The strength of EPR and ENDOR techniques in revealing structure-function relationships in metalloproteins. Phys Chem Chem Phys 9, 4620 4638.
39. Kay CWM, Feicht R, Schulz K, Sadewater P, Sancar A, Bacher A, Möbius K, Richter G Weber S (1999) EPR, ENDOR and TRIPLE resonance spectroscopy on the neutral flavin radical in Escherichia coli DNA photolyase. Biochemistry 38, 16740 16748.
40. Medina M Cammack R (2007) ENDOR and related EMR methods applied to flavoprotein radicals. Appl Magn Reson 31, 457 470.
41. Bittl R, Kay CWM, Weber S Hegemann P (2003) Characterization of a flavin radical product in a C57M mutant of a LOV1 domain by electron paramagnetic resonance. Biochemistry 42, 8506 8512.
42. +-pumping NADH:quinone oxidoreductase from Vibrio cholerae. An EPR/electron nuclear double resonance investigation of the role of the covalently bound flavins in subunits B and C. J Biol Chem 281, 36482 36491.
43. Nagai H, Fukushima Y, Okajima K, Ikeuchi M Mino H (2008) Formation of interacting spins on flavosemiquinone and tyrosine radical in photoreaction of a blue light sensor BLUF protein TePixD. Biochemistry 47, 12574 12582.
44. Banerjee R, Schleicher E, Meier S, Muñoz Viana R, Pokorny R, Ahmad M, Bittl R Batschauer A (2007) The signaling state of Arabidopsis cryptochrome 2 contains flavin semiquinone. J Biol Chem 282, 14916 14922.
45. Hoang N, Schleicher E, Kacprzak S, Bouly J-P, Picot M, Wu W, Berndt A, Wolf E, Bittl R Ahmad M (2008) Human and Drosophila cryptochromes are light activated by flavin photoreduction in living cells. PLoS Biol 6, 1559 1569.
46. Goldfarb D Arieli D (2004) Spin distribution and the location of protons in paramagnetic proteins. Annu Rev Biophys Biomol Struct 33, 441 468.
47. Goldfarb D (2006) High field ENDOR as a characterization tool for functional sites in microporous materials. Phys Chem Chem Phys 8, 2325 2343.
48. Schleicher E, Hitomi K, Kay CWM, Getzoff ED, Todo T Weber S (2007) Electron nuclear double resonance differentiates complementary roles for active site histidines in (6-4) photolyase. J Biol Chem 282, 4738 4747.
49. Kurreck H, Bock M, Bretz N, Elsner M, Kraus H, Lubitz W, Müller F, Geissler J Kroneck PMH (1984) Fluid solution and solid-state electron nuclear double resonance studies of flavin model compounds and flavoenzymes. J Am Chem Soc 106, 737 746.
50. Çinkaya I, Buckel W, Medina M, Gómez-Moreno C Cammack R (1997) Electron-nuclear double resonance spectroscopy investigation of 4-hydroxybutyryl-CoA dehydrase from Chlostridium aminobutyricum: comparison with other flavin radical enzymes. Biol Chem 378, 843 849.
51. Medina M, Lostao A, Sancho J, Gómez-Moreno C, Cammack R, Alonso PJ Martínez JI (1999) Electron-nuclear double resonance and hyperfine sublevel correlation spectroscopic studies of flavodoxin mutants from Anabaena sp. PCC 7119. Biophys J 77, 1712 1720.
52. Weber S, Richter G, Schleicher E, Bacher A, Möbius K Kay CWM (2001) Substrate binding to DNA photolyase studied by electron paramagnetic resonance spectroscopy. Biophys J 81, 1195 1204.
53. Kay CWM, Schleicher E, Hitomi K, Todo T, Bittl R Weber S (2005) Determination of the g-matrix orientation in flavin radicals by high-field/high-frequency electron-nuclear double resonance. Magn Reson Chem 43, S96 S102.
54. Martínez JI, Alonso PJ, Gómez-Moreno C Medina M (1997) One- and two-dimensional ESEEM spectroscopy of flavoproteins. Biochemistry 36, 15526 15537.
55. Medina M, Vrielink A Cammack R (1997) Electron spin echo envelope modulation studies of the semiquinone anion radical of cholesterol oxidase from Brevibacterium sterolicum. FEBS Lett 400, 247 251.
56. Stehlik D Möbius K (1997) New EPR methods for investigating photoprocesses with paramagnetic intermediates. Annu Rev Phys Chem 48, 745 784.
57. Bittl R Weber S (2005) Transient radical pairs studied by time-resolved EPR. Biochim Biophys Acta 1707, 117 126.
58. Kowalczyk RM, Schleicher E, Bittl R Weber S (2004) The photo-induced triplet of flavins and its protonation states. J Am Chem Soc 126, 11393 11399.
59. Schleicher E, Kowalczyk RM, Kay CWM, Hegemann P, Bacher A, Fischer M, Bittl R, Richter G Weber S (2004) On the reaction mechanism of adduct formation in LOV domains of the plant blue-light receptor phototropin. J Am Chem Soc 126, 11067 11076.
60. Turro NJ, Kleinman MH Karatekin E (2000) Electron spin polarization and time-resolved paramagnetic resonance: applications to the paradigms of molecular and supramolecular photochemistry. Angew Chem Int Ed 39, 4436 4461.
61. Woodward JR (2002) Radical pairs in solution. Prog React Kinet Mec 27, 165 207.
62. Hirota N Yamauchi S (2003) Short-lived excited triplet states studied by time-resolved EPR spectroscopy. J Photochem Photobiol C Photochem Rev 4, 109 124.
63. Jordan SP Jorns MS (1988) Evidence for a singlet intermediate in catalysis by Escherichia coli DNA photolyase and evaluation of substrate binding determinants. Biochemistry 27, 8915 8923.
64. Kim S-T, Malhotra K, Smith CA, Taylor J-S Sancar A (1994) Characterization of (6-4) photoproduct DNA photolyase. J Biol Chem 269, 8535 8540.
65. Zhao X, Liu J, Hsu DS, Zhao S, Taylor J-S Sancar A (1997) Reaction mechanism of (6-4) photolyase. J Biol Chem 272, 32580 32590.
66. Hitomi K, Kim S-T, Iwai S, Harima N, Otoshi E, Ikenaga M Todo T (1997) Binding and catalytic properties of Xenopus (6-4) photolyase. J Biol Chem 272, 32591 32598.
67. Hitomi K, Nakamura H, Kim S-T, Mizukoshi T, Ishikawa T, Iwai S Todo T (2001) Role of two histidines in the (6-4) photolyase reaction. J Biol Chem 276, 10103 10109.
68. Lv XY, Qiao DR, Xiong Y, Xu H, You FF, Cao Y, He X Cao Y (2008) Photoreactivation of (6-4) photolyase in Dunaliella salina. FEMS Microbiol Lett 283, 42 46.
69. Varghese AJ Wang SY (1968) Photoreversible photoproduct of thymine. Biochem Biophys Res Commun 33, 102 107.
70. Asgatay S, Petermann C, Harakat D, Guillaume D, Taylor J-S Clivio P (2008) Evidence that the (6-4) photolyase mechanism can proceed through an oxetane intermediate. J Am Chem Soc 130, 12618 12619.
71. Knauer BR Napier JJ (1976) The nitrogen hyperfine splitting constant of the nitroxide functional group as a solvent polarity parameter. The relative importance for a solvent polarity parameter of its being a cybotactic probe vs. its being a model process. J Am Chem Soc 98, 4395 4400.
72. Khramtsov VV, Weiner LM, Grigoriev IA Volodarsky LB (1982) Proton exchange in stable nitroxyl radicals EPR study of the pH of aqueous solutions. Chem Phys Lett 91, 69 72.
73. Saracino GAA, Tedeschi A, D'Errico G, Improta R, Franco L, Ruzzi M, Corvaia C Barone V (2002) Solvent polarity and pH effects on the magnetic properties of ionizable nitroxide radicals: a combined computational and experimental study of 2,2,5,5-tetramethyl-3-carboxypyrrolidine and 2,2,6,6-tetramethyl-4-carboxypiperidine nitroxides. J Phys Chem A 106, 10700 10706.
74. Weber S, Möbius K, Richter G Kay CWM (2001) The electronic structure of the flavin cofactor in DNA photolyase. J Am Chem Soc 123, 3790 3798.
75. Maul MJ, Barends TRM, Glas AF, Cryle MJ, Domratcheva T, Schneider S, Schlichting I Carell T (2008) Crystal structure and mechanism of a DNA (6-4) photolyase. Angew Chem Int Ed 47, 10076 10080.
76. Park H-W, Kim S-T, Sancar A Deisenhofer J (1995) Crystal structure of DNA photolyase from Escherichia coli. Science 268, 1866 1872.
77. Merrow M Roenneberg T (2001) Circadian clocks: running on redox. Cell (Cambridge, Mass) 106, 141 143.
78. Froy O, Chang DC Reppert SM (2002) Redox potential: differential roles in dCRY and mCRY1 functions. Curr Biol 12, 147 152.
79. Weber S, Kay CWM, Mögling H, Möbius K, Hitomi K Todo T (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.
80. 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.
81. Lukacs A, Eker APM, Byrdin M, Brettel K Vos MH (2008) Electron hopping through the 15 Å triple tryptophan molecular wire in DNA photolyase occurs within 30 ps. J Am Chem Soc 130, 14394 14395.
82. Byrdin M, Sartor V, Eker APM, Vos MH, Aubert C, Brettel K Mathis P (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.
83. Kavakli IH Sancar A (2004) Analysis of the role of intraprotein electron transfer in photoreactivation by DNA photolyase in vivo. Biochemistry 43, 15103 15110.
84. Zeugner A, Byrdin M, Bouly J-P, Bakrim N, Giovani B, Brettel K Ahmad M (2005) Light-induced electron transfer in Arabidopsis cryptochrome-1 correlates with in vivo function. J Biol Chem 280, 19437 19440.
85. Ritz T, Adem S Schulten K (2000) A model for photoreceptor-based magnetoreception in birds. Biophys J 78, 707 718.
86. Biskup T, Schleicher E, Okafuji A, Link G, Hitomi K, Getzoff ED Weber S (2009) Direct observation of a photoinduced radical pair in a cryptochrome blue-light photoreceptor. Angew Chem Int Ed 48, 404 407.
87. Henbest KB, Maeda K, Hore PJ, Joshi M, Bacher A, Bittl R, Weber S, Timmel CR Schleicher E (2008) Magnetic-field effect on the photoactivation reaction of Escherichia coli DNA photolyase. Proc Natl Acad Sci USA 105, 14395 14399.
88. 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.