Response of the sensory animal-like cryptochrome aCRY to blue and red light as revealed by infrared difference spectroscopy

Biochemistry

Volumn 53, Issue 6, 2014, Pages 1041-1050

  Spexard, Meike ^a   Thöing, Christian ^a   Beel, Benedikt ^b   Mittag, Maria ^b   Kottke, Tilman ^a  

^a BIELEFELD UNIVERSITY   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHLAMYDOMONAS REINHARDTII; COLOR; CRYPTOCHROMES; DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DEUTERIUM OXIDE; FLAVOPROTEINS; HYDROGEN-ION CONCENTRATION; LIGHT; SPECTROPHOTOMETRY, ULTRAVIOLET; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 84894238342     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401599z     Document Type: Article

References (49)

1. Chaves, I., Pokorny, R., Byrdin, M., Hoang, N., Ritz, T., Brettel, K., Essen, L. O., van der Horst, G. T., Batschauer, A., and Ahmad, M. (2011) The cryptochromes: Blue light photoreceptors in plants and animals Annu. Rev. Plant Biol. 62, 335-364
2. Etchegaray, J. P., Lee, C., Wade, P. A., and Reppert, S. M. (2003) Rhythmic histone acetylation underlies transcription in the mammalian circadian clock Nature 421, 177-182
3. Gegear, R. J., Casselman, A., Waddell, S., and Reppert, S. M. (2008) Cryptochrome mediates light-dependent magnetosensitivity in Drosophila Nature 454, 1014-1018
4. Rupert, C. S. (1960) Photoreactivation of transforming DNA by an enzyme from bakers' yeast J. Gen. Physiol. 43, 573-595
5. Todo, T., Takemori, H., Ryo, H., Ihara, M., Matsunaga, T., Nikaido, O., Sato, K., and Nomura, T. (1993) A new photoreactivating enzyme that specifically repairs ultraviolet light-induced (6-4) photoproducts Nature 361, 371-374
6. Pokorny, R., Klar, T., Hennecke, U., Carell, T., Batschauer, A., and Essen, L. O. (2008) Recognition and repair of UV lesions in loop structures of duplex DNA by DASH-type cryptochrome Proc. Natl. Acad. Sci. U.S.A. 105, 21023-21027
7. Selby, C. P. and Sancar, A. (2006) A cryptochrome/photolyase class of enzymes with single-stranded DNA-specific photolyase activity Proc. Natl. Acad. Sci. U.S.A. 103, 17696-17700
8. Coesel, S., Mangogna, M., Ishikawa, T., Heijde, M., Rogato, A., Finazzi, G., Todo, T., Bowler, C., and Falciatore, A. (2009) Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity EMBO Rep. 10, 655-661
9. Heijde, M., Zabulon, G., Corellou, F., Ishikawa, T., Brazard, J., Usman, A., Sanchez, F., Plaza, P., Martin, M., Falciatore, A., Todo, T., Bouget, F. Y., and Bowler, C. (2010) Characterization of two members of the cryptochrome/photolyase family from Ostreococcus tauri provides insights into the origin and evolution of cryptochromes Plant Cell Environ. 33, 1614-1626
10. Malhotra, K., Kim, S. T., Batschauer, A., Dawut, L., and Sancar, A. (1995) Putative blue-light photoreceptors from Arabidopsis thaliana and Sinapis alba with a high degree of sequence homology to DNA photolyase contain the two photolyase cofactors but lack DNA repair activity Biochemistry 34, 6892-6899
11. Beel, B., Prager, K., Spexard, M., Sasso, S., Weiss, D., Müller, N., Heinnickel, M., Dewez, D., Ikoma, D., Grossman, A. R., Kottke, T., and Mittag, M. (2012) A Flavin Binding Cryptochrome Photoreceptor Responds to Both Blue and Red Light in Chlamydomonas reinhardtii Plant Cell 24, 2992-3008
12. Losi, A. and Gärtner, W. (2011) Old chromophores, new photoactivation paradigms, trendy applications: Flavins in blue light-sensing photoreceptors Photochem. Photobiol. 87, 491-510
13. Barth, A. (2007) Infrared spectroscopy of proteins Biochim. Biophys. Acta 1767, 1073-1101
14. Immeln, D., Pokorny, R., Herman, E., Moldt, J., Batschauer, A., and Kottke, T. (2010) Photoreaction of Plant and DASH Cryptochromes Probed by Infrared Spectroscopy: The Neutral Radical State of Flavoproteins J. Phys. Chem. B 114, 17155-17161
15. Kottke, T., Batschauer, A., Ahmad, M., and Heberle, J. (2006) Blue-light-induced changes in Arabidopsis cryptochrome 1 probed by FTIR difference spectroscopy Biochemistry 45, 2472-2479
16. Iwata, T., Zhang, Y., Hitomi, K., Getzoff, E. D., and Kandori, H. (2010) Key dynamics of conserved asparagine in a cryptochrome/photolyase family protein by Fourier transform infrared spectroscopy Biochemistry 49, 8882-8891
17. Schleicher, E., Hessling, B., Illarionova, V., Bacher, A., Weber, S., Richter, G., and Gerwert, K. (2005) Light-induced reactions of Escherichia coli DNA photolyase monitored by Fourier transform infrared spectroscopy FEBS J. 272, 1855-1866
18. Wijaya, I. M., Zhang, Y., Iwata, T., Yamamoto, J., Hitomi, K., Iwai, S., Getzoff, E. D., and Kandori, H. (2013) Detection of distinct α-helical rearrangements of cyclobutane pyrimidine dimer photolyase upon substrate binding by Fourier transform infrared spectroscopy Biochemistry 52, 1019-1027
19. Yamada, D., Zhang, Y., Iwata, T., Hitomi, K., Getzoff, E. D., and Kandori, H. (2012) Fourier-transform infrared study of the photoactivation process of Xenopus (6-4) photolyase Biochemistry 51, 5774-5783
20. Zhang, Y., Iwata, T., Yamamoto, J., Hitomi, K., Iwai, S., Todo, T., Getzoff, E. D., and Kandori, H. (2011) FTIR study of light-dependent activation and DNA repair processes of (6-4) photolyase Biochemistry 50, 3591-3598
21. Iwata, T., Yamamoto, A., Tokutomi, S., and Kandori, H. (2007) Hydration and temperature similarly affect light-induced protein structural changes in the chromophoric domain of phototropin Biochemistry 46, 7016-7021
22. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J. A., Jr., Vreven, T., Kudin, K. N., Burant, J. C., Millam, J. M., Iyengar, S. S., Tomasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, G. A., Nakatsuji, H., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Klene, M., Li, X., Knox, J. E., Hratchian, H. P., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Ayala, P. Y., Morokuma, K., Voth, G. A., Salvador, P., Dannenberg, J. J., Zakrzewski, V. G., Dapprich, S., Daniels, A. D., Strain, M. C., Farkas, O., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Ortiz, J. V., Cui, Q., Baboul, A. G., Clifford, S., Cioslowski, J., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Gonzalez, C., and Pople, J. A. (2004) Gaussian 03, Gaussian, Inc., Wallingford, CT.
23. Spexard, M., Immeln, D., Thöing, C., and Kottke, T. (2011) Infrared spectrum and absorption coefficient of the cofactor flavin in water Vib. Spectrosc. 57, 282-287
24. Thöing, C., Pfeifer, A., Kakorin, S., and Kottke, T. (2013) Protonated triplet-excited flavin resolved by step-scan FTIR spectroscopy: Implications for photosensory LOV domains Phys. Chem. Chem. Phys. 15, 5916-5926
25. Hitomi, K., DiTacchio, L., Arvai, A. S., Yamamoto, J., Kim, S. T., Todo, T., Tainer, J. A., Iwai, S., Panda, S., and Getzoff, E. D. (2009) Functional motifs in the (6-4) photolyase crystal structure make a comparative framework for DNA repair photolyases and clock cryptochromes Proc. Natl. Acad. Sci. U.S.A. 106, 6962-6967
26. Berndt, A., Kottke, T., Breitkreuz, H., Dvorsky, R., Hennig, S., Alexander, M., and Wolf, E. (2007) A novel photoreaction mechanism for the circadian blue light photoreceptor Drosophila cryptochrome J. Biol. Chem. 282, 13011-13021
27. Immeln, D., Schlesinger, R., Heberle, J., and Kottke, T. (2007) Blue light induces radical formation and autophosphorylation in the light-sensitive domain of Chlamydomonas cryptochrome J. Biol. Chem. 282, 21720-21728
28. Müller, P. and Ahmad, M. (2011) Light-activated Cryptochrome Reacts with Molecular Oxygen to Form a Flavin-Superoxide Radical Pair Consistent with Magnetoreception J. Biol. Chem. 286, 21033-21040
29. Schleicher, E., Hitomi, K., Kay, C. W., Getzoff, E. D., Todo, T., and Weber, S. (2007) Electron nuclear double resonance differentiates complementary roles for active site histidines in (6-4) photolyase J. Biol. Chem. 282, 4738-4747
30. Alexandre, M. T., Domratcheva, T., Bonetti, C., van Wilderen, L. J., van Grondelle, R., Groot, M. L., Hellingwerf, K. J., and Kennis, J. T. (2009) Primary reactions of the LOV2 domain of phototropin studied with ultrafast mid-infrared spectroscopy and quantum chemistry Biophys. J. 97, 227-237
31. Murgida, D. H., Schleicher, E., Bacher, A., Richter, G., and Hildebrandt, P. (2001) Resonance Raman spectroscopic study of the neutral flavin radical complex of DNA photolyase from Escherichia coli J. Raman Spectrosc. 32, 551-556
32. Wille, G., Ritter, M., Friedemann, R., Mäntele, W., and Hübner, G. (2003) Redox-triggered FTIR difference spectra of FAD in aqueous solution and bound to flavoproteins Biochemistry 42, 14814-14821
33. Li, J., Uchida, T., Ohta, T., Todo, T., and Kitagawa, T. (2006) Characteristic structure and environment in FAD cofactor of (6-4) photolyase along function revealed by resonance Raman spectroscopy J. Phys. Chem. B 110, 16724-16732
34. Krimm, S. and Bandekar, J. (1986) Vibrational spectroscopy and conformations of peptides, polypeptides, and proteins Adv. Protein Chem. 38, 181-364
35. Braun, F. J. and Hegemann, P. (1999) Direct measurement of cytosolic calcium and pH in living Chlamydomonas reinhardtii cells Eur. J. Cell Biol. 78, 199-208
36. Messerli, M. A., Maral-Zettler, L. A., Zettler, E., Jung, S. K., Smith, P. J., and Sogin, M. L. (2005) Life at acidic pH imposes an increased energetic cost for a eukaryotic acidophile J. Exp. Biol. 208, 2569-2579
37. Burney, S., Hoang, N., Caruso, M., Dudkin, E. A., Ahmad, M., and Bouly, J. P. (2009) Conformational change induced by ATP binding correlates with enhanced biological function of Arabidopsis cryptochrome FEBS Lett. 583, 1427-1433
38. Ozturk, N., Selby, C. P., Annayev, Y., Zhong, D., and Sancar, A. (2011) Reaction mechanism of Drosophila cryptochrome Proc. Natl. Acad. Sci. U.S.A. 108, 516-521
39. Vaidya, A. T., Top, D., Manahan, C. C., Tokuda, J. M., Zhang, S., Pollack, L., Young, M. W., and Crane, B. R. (2013) Flavin reduction activates Drosophila cryptochrome Proc. Natl. Acad. Sci. U.S.A. 110, 20455-20460
40. Hitomi, K., Nakamura, H., Kim, S. T., Mizukoshi, T., Ishikawa, T., Iwai, S., and Todo, T. (2001) Role of two histidines in the (6-4) photolyase reaction J. Biol. Chem. 276, 10103-10109
41. Kavakli, I. H. and Sancar, A. (2004) Analysis of the role of intraprotein electron transfer in photoreactivation by DNA photolyase in vivo Biochemistry 43, 15103-15110
42. Kondoh, M., Hitomi, K., Yamamoto, J., Todo, T., Iwai, S., Getzoff, E. D., and Terazima, M. (2011) Light-induced conformational change and product release in DNA repair by (6-4) photolyase J. Am. Chem. Soc. 133, 2183-2191
43. Partch, C. L., Clarkson, M. W., Özgür, S., Lee, A. L., and Sancar, A. (2005) Role of structural plasticity in signal transduction by the cryptochrome blue-light photoreceptor Biochemistry 44, 3795-3805
44. Kondoh, M., Shiraishi, C., Müller, P., Ahmad, M., Hitomi, K., Getzoff, E. D., and Terazima, M. (2011) Light-induced conformational changes in full-length Arabidopsis thaliana cryptochrome J. Mol. Biol. 413, 128-137
45. Yang, H. Q., Wu, Y. J., Tang, R. H., Liu, D., Liu, Y., and Cashmore, A. R. (2000) The C termini of Arabidopsis cryptochromes mediate a constitutive light response Cell 103, 815-827
46. Czarna, A., Berndt, A., Singh, H. R., Grudziecki, A., Ladurner, A. G., Timinszky, G., Kramer, A., and Wolf, E. (2013) Structures of Drosophila cryptochrome and mouse cryptochrome1 provide insight into circadian function Cell 153, 1394-1405
47. Zoltowski, B. D., Vaidya, A. T., Top, D., Widom, J., Young, M. W., and Crane, B. R. (2011) Structure of full-length Drosophila cryptochrome Nature 480, 396-399
48. Banerjee, R., Schleicher, E., Meier, S., Viana, R. M., Pokorny, R., Ahmad, M., Bittl, R., and Batschauer, A. (2007) The signaling state of Arabidopsis cryptochrome 2 contains flavin semiquinone J. Biol. Chem. 282, 14916-14922
49. Bouly, J. P., Schleicher, E., Dionisio-Sese, M., Vandenbussche, F., Van Der Straeten, D., Bakrim, N., Meier, S., Batschauer, A., Galland, P., Bittl, R., and Ahmad, M. (2007) Cryptochrome blue light photoreceptors are activated through interconversion of flavin redox states J. Biol. Chem. 282, 9383-9391