The class III cyclobutane pyrimidine dimer photolyase structure reveals a new antenna chromophore binding site and alternative photoreduction pathways

Journal of Biological Chemistry

Volumn 290, Issue 18, 2015, Pages 11504-11514

  Scheerer, Patrick ^a   Zhang, Fan ^b   Kalms, Jacqueline ^a   Von Stetten, David ^c   Krauß, Norbert ^d   Oberpichler, Inga ^b   Lamparter, Tilman ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTENNAS; AROMATIC COMPOUNDS; CHROMOPHORES; DIMERS; PROTEINS; REPAIR; VISION;

AGROBACTERIUM TUMEFACIENS; ANTENNA CHROMOPHORE; BLUE-LIGHT PHOTORECEPTORS; CYCLOBUTANE PYRIMIDINE DIMERS; ELECTRONS FLOW; EVOLUTIONARY TRANSITIONS; PHOTO-REDUCTION; STRUCTURAL STUDIES;

CRYSTAL STRUCTURE;

5 METHYLTETRAHYDROFOLIC ACID; 5,10 METHENYLTETRAHYDROFOLIC ACID; CRYPTOCHROME I; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; FLAVINE ADENINE NUCLEOTIDE; FLAVOPROTEIN; PHOTOLYASE RELATED PROTEIN A; UNCLASSIFIED DRUG; 5,10-METHENYLTETRAHYDROFOLATE; CYTOCHROME; PYRIMIDINE DIMER; TETRAHYDROFOLIC ACID DERIVATIVE;

AGROBACTERIUM TUMEFACIENS; AMINO TERMINAL SEQUENCE; ANTENNA CHROMOPHORE; ARTICLE; BINDING SITE; CHROMATOPHORE; CRYSTALLIZATION; ELECTRON TRANSPORT; ENZYME STABILITY; ENZYME STRUCTURE; MOLECULAR EVOLUTION; PHOTODYNAMICS; PHOTORECEPTOR; PHOTOREDUCTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN FUNCTION; RADIATION INJURY; ULTRAVIOLET RADIATION; ULTRAVIOLET SPECTROSCOPY; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DNA DAMAGE; ENZYMOLOGY; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN TERTIARY STRUCTURE; RADIATION RESPONSE; X RAY CRYSTALLOGRAPHY;

AGROBACTERIUM TUMEFACIENS;

AGROBACTERIUM TUMEFACIENS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CYTOCHROMES; DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DNA DAMAGE; ENZYME STABILITY; EVOLUTION, MOLECULAR; FLAVIN-ADENINE DINUCLEOTIDE; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; OXIDATION-REDUCTION; PROTEIN STRUCTURE, TERTIARY; PYRIMIDINE DIMERS; TETRAHYDROFOLATES; ULTRAVIOLET RAYS;

EID: 84929485473     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.637868     Document Type: Article

References (67)

1. Sancar, A. (2003) Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103, 2203-2237
2. Müller, M., and Carell, T. (2009) Structural biology of DNA photolyases and cryptochromes. Curr. Opin. Struct. Biol. 19, 277-285
3. 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
4. Oberpichler, I., Pierik, A. J., Wesslowski, J., Pokorny, R., Rosen, R., Vugman, M., Zhang, F., Neubauer, O., Ron, E. Z., Batschauer, A., and Lamparter, T. (2011) A photolyase-like protein from Agrobacterium tumefaciens with an iron-sulfur cluster. Plos One 6, e26775
5. 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
6. Liu, Z., Tan, C., Guo, X., Kao, Y. T., Li, J., Wang, L., Sancar, A., and Zhong, D. (2011) Dynamics and mechanism of cyclobutane pyrimidine dimer repair by DNA photolyase. Proc. Natl. Acad. Sci. U. S. A. 108, 14831-14836
7. Hoang, N., Schleicher, E., Kacprzak, S., Bouly, J. P., Picot, M., Wu, W., Berndt, A., Wolf, E., Bittl, R., and Ahmad, M. (2008) Human and Drosophila cryptochromes are light activated by flavin photoreduction in living cells. PLoS Biol. 6, e160
8. Kiontke, S., Geisselbrecht, Y., Pokorny, R., Carell, T., Batschauer, A., and Essen, L. O. (2011) Crystal structures of an archaeal class II DNA photolyase and its complex with UV-damaged duplex DNA. EMBO J. 30, 4437-4449
9. Hitomi, K., Arvai, A. S., Yamamoto, J., Hitomi, C., Teranishi, M., Hirouchi, T., Yamamoto, K., Iwai, S., Tainer, J. A., Hidema, J., and Getzoff, E. D. (2012) Eukaryotic class II cyclobutane pyrimidine dimer photolyase structure reveals basis for improved ultraviolet tolerance in plants. J. Biol. Chem. 287, 12060-12069
10. Geisselbrecht, Y., Frühwirth, S., Schroeder, C., Pierik, A. J., Klug, G., and Essen, L. O. (2012) CryB from Rhodobacter sphaeroides: a unique class of cryptochromes with new cofactors. EMBO Rep. 13, 223-229
11. Zhang, F., Scheerer, P., Oberpichler, I., Lamparter, T., and Krauß, N. (2013) Crystal structure of a prokaryotic (6-4) photolyase with an Fe-S cluster and a 6, 7-dimethyl-8-ribityllumazine antenna chromophore. Proc. Natl. Acad. Sci. U. S. A. 110, 7217-7222
12. Li, Y. F., Heelis, P. F., and 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
13. Li, X., Wang, Q., Yu, X., Liu, H., Yang, H., Zhao, C., Liu, X., Tan, C., Klejnot, J., Zhong, D., and Lin, C. (2011) Arabidopsis cryptochrome 2 (CRY2) functions by the photoactivation mechanism distinct from the tryptophan (trp) triad-dependent photoreduction. Proc. Natl. Acad. Sci. U. S. A. 108, 20844-20849
14. Biskup, T., Paulus, B., Okafuji, A., Hitomi, K., Getzoff, E. D., Weber, S., and Schleicher, E. (2013) Variable electron transfer pathways in an amphibian cryptochrome: tryptophan versus tyrosine-based radical pairs. J. Biol. Chem. 288, 9249-9260
15. Liu, Z., Tan, C., Guo, X., Li, J., Wang, L., Sancar, A., and Zhong, D. (2013) Determining complete electron flow in the cofactor photoreduction of oxidized photolyase. Proc. Natl. Acad. Sci. U. S. A. 110, 12966-12971
16. Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Cassarino, T. G., Bertoni, M., Bordoli, L., and Schwede, T. (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42, W252-W258
17. Klar, T., Kaiser, G., Hennecke, U., Carell, T., Batschauer, A., and Essen, L. O. (2006) Natural and non-natural antenna chromophores in the DNA photolyase from Thermus thermophilus. Chembiochem 7, 1798-1806
18. Tamada, T., Kitadokoro, K., Higuchi, Y., Inaka, K., Yasui, A., De Ruiter, P. E., Eker, A. P., and Miki, K. (1997) Crystal structure of DNA photolyase from Anacystis nidulans. Nat. Struct. Biol. 4, 887-891
19. Fujihashi, M., Numoto, N., Kobayashi, Y., Mizushima, A., Tsujimura, M., Nakamura, A., Kawarabayasi, Y., and Miki, K. (2007) Crystal structure of archaeal photolyase from Sulfolobus tokodaii with two FAD molecules: implication of a novel light-harvesting cofactor. J. Mol. Biol. 365, 903-910
20. Park, H. W., Kim, S. T., Sancar, A., and Deisenhofer, J. (1995) Crystal structure of DNA photolyase from Escherichia coli. Science 268, 1866-1872
21. Huang, Y., Baxter, R., Smith, B. S., Partch, C. L., Colbert, C. L., and Deisenhofer, J. (2006) Crystal structure of cryptochrome 3 from Arabidopsis thaliana and its implications for photolyase activity. Proc. Natl. Acad. Sci. U. S. A. 103, 17701-17706
22. Hoang, N., Bouly, J. P., and Ahmad, M. (2008) Evidence of a light-sensing role for folate in Arabidopsis cryptochrome blue-light receptors. Mol. Plant 1, 68-74
23. Malhotra, K., Kim, S. T., Batschauer, A., Dawut, L., and Sancar, A. (1995) Putative blue-light photoreceptors from Arabidopsis thaliana and Sinapis albawith ahigh degreeof sequence homology to DNA photolyase contain the two photolyase cofactors but lack DNA repair activity. Biochemistry 34, 6892-6899
24. Selby, C. P., and Sancar, A. (2012) The second chromophore in Drosophila photolyase/cryptochrome family photoreceptors. Biochemistry 51, 167-171
25. Brautigam, C. A., Smith, B. S., Ma, Z., Palnitkar, M., Tomchick, D. R., Machius, M., and Deisenhofer, J. (2004) Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 101, 12142-12147
26. Kottke, T., Batschauer, A., Ahmad, M., and Heberle, J. (2006) Blue-lightinduced changes in Arabidopsis cryptochrome 1 probed by FTIR difference spectroscopy. Biochemistry 45, 2472-2479
27. Komori, H., Masui, R., Kuramitsu, S., Yokoyama, S., Shibata, T., Inoue, Y., and Miki, K. (2001) Crystal structure of thermostable DNA photolyase: pyrimidine-dimer recognition mechanism. Proc. Natl. Acad. Sci. U. S. A. 98, 13560-13565
28. Maul, M. J., Barends, T. R., Glas, A. F., Cryle, M. J., Domratcheva, T., Schneider, S., Schlichting, I., and Carell, T. (2008) Crystal structure and mechanism of a DNA (6-4) photolyase. Angew. Chem. Int. Ed. Engl. 47, 10076-10080
29. Mees, A., Klar, T., Gnau, P., Hennecke, U., Eker, A. P., Carell, T., and Essen, L. O. (2004) Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science 306, 1789-1793
30. Glas, A. F., Schneider, S., Maul, M. J., Hennecke, U., and Carell, T. (2009) Crystal structure of the T (6-4) C lesion in complex with a (6-4) DNA photolyase and repair of UV-induced (6-4) and Dewar photolesions. Chemistry 15, 10387-10396
31. Oztürk, N., Kao, Y. T., Selby, C. P., Kavakli, I. H., Partch, C. L., Zhong, D., and Sancar, A. (2008) Purification and characterization of a type III photolyase from Caulobacter crescentus. Biochemistry 47, 10255-10261
32. De Sanctis, D., Beteva, A., Caserotto, H., Dobias, F., Gabadinho, J., Giraud, T., Gobbo, A., Guijarro, M., Lentini, M., Lavault, B., Mairs, T., McSweeney, S., Petitdemange, S., Rey-Bakaikoa, V., Surr, J., Theveneau, P., Leonard, G. A., and Mueller-Dieckmann, C. (2012) ID29: a high-intensity highly automated ESRF beamline for macromolecular crystallography experiments exploiting anomalous scattering. J. Synchrotron Radiat. 19, 455-461
33. Mueller, U., Darowski, N., Fuchs, M. R., Förster, R., Hellmig, M., Paithankar, K. S., Pühringer, S., Steffien, M., Zocher, G., and Weiss, M. S. (2012) Facilities for macromolecular crystallography at the Helmholtz-Zentrum Berlin. J. Synchrotron Radiat. 19, 442-449
34. Kabsch, W. (2010) Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
35. Collaborative Computational Project, Number 4. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
36. Evans, P. (2006) Scaling and assessmentof data quality. Acta Crystallogr. D Biol. Crystallogr. 62, 72-82
37. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
38. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
39. Winn, M. D., Isupov, M. N., and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. 57, 122-133
40. Vagin, A. A., Steiner, R. A., Lebedev, A. A., Potterton, L., McNicholas, S., Long, F., and Murshudov, G. N. (2004) REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr. D Biol. Crystallogr. 60, 2184-2195
41. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
42. Cowtan, K., Emsley, P., and Wilson, K. S. (2011) From crystal to structure with CCP4 introduction. Acta Crystallogr. D Biol. Crystallogr. 67, 233-234
43. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954
44. Vaguine, A. A., Richelle, J., and Wodak, S. J. (1999) SFCHECK: aunified set of procedures for evaluating the quality of macromolecular structurefactor data and their agreement with the atomic model. Acta Crystallogr. DBiol. Crystallogr. 55, 191-205
45. Laskowski, R. A., Moss, D. S., and Thornton, J. M. (1993) Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231, 1049-1067
46. Hooft, R. W., Vriend, G., Sander, C, and Abola, E. E. (1996) Errors in protein structures. Nature 381, 272
47. Vriend, G. (1990) WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 8, 52-6, 29
48. Lovell, S. C, Davis, I. W., Arendall, W. B., 3rd, De Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Cα geometry: lt;j), ij) and Cβ deviation. Proteins 50, 437-450
49. McDonald, I. K., and Thornton, J. M. (1994) Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238, 777-793
50. Laskowski, R. A., and Swindells, M. B. (2011) LigPlot+: multiple ligandprotein interaction diagrams for drug discovery. J. Chem. Inf. Model 51, 2778-2786
51. De Lano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA
52. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882
53. Edgar, R. C (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797
54. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739
55. Royant, A., Carpentier, P., Ohana, J., McGeehan, J., Paetzold, B., Noirclerc-Savoye, M., Vernede, X., Adam, V., and Bourgeois, D. (2007) Advances in spectroscopic methods for biological crystals: 1. fluorescence lifetime measurements. J. Appl. Crystallogr. 40, 1105-1112
56. Kort, R., Komori, H., Adachi, S., Miki, K., and Eker, A. (2004) DNA apophotolyase fromAnacystis nidulans: 1.8-Å structure, 8-HDF reconstitution and x-ray-induced FAD reduction. Acta Crystallogr. D Biol. Crystallogr. 60, 1205-1213
57. Holm, L., and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138
58. Klar, T., Pokorny, R., Moldt, J., Batschauer, A., and 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
59. 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
60. Balland, V., Byrdin, M., Eker, A. P., Ahmad, M., and Brettel, K. (2009) What makes the difference between a cryptochrome and DNA photolyase? a spectroelectrochemical comparison of the flavin redox transitions. J. Am. Chem. Soc. 131, 426-427
61. Burney, S., Wenzel, R., Kottke, T., Roussel, T., Hoang, N., Bouly, J. P., Bittl, R., Heberle, J., and Ahmad, M. (2012) Single amino acid substitution reveals latent photolyase activity in Arabidopsis cry1. Angew. Chem. Int. Ed. Engl. 51, 9356-9360
62. Juhas, M., Von Zadow, A., Spexard, M., Schmidt, M., Kottke, T., and Büchel, C. (2014) A novel cryptochrome in the diatom Phaeodactylum tricornutum influences the regulation of light-harvesting protein levels. FEBS J. 281, 2299-2311
63. Payne, G., and Sancar, A. (1990) Absolute action spectrum of E-FADH2 and E-FADH2-MTHF forms of Escherichia coli DNA photolyase. Biochemistry 29, 7715-7727
64. Liu, B., Liu, H., Zhong, D., and Lin, C. (2010) Searching for a photocycle of the cryptochrome photoreceptors. Curr. Opin. Plant Biol. 13, 578-586
65. Aubert, C., Mathis, P., Eker, A. P., and Brettel, K. (1999) Intraprotein electron transfer between tyrosine and tryptophan in DNA photolyase from Anacystis nidulans. Proc. Natl. Acad. Sci. U. S. A. 96, 5423-5427
66. Aubert, C., Vos, M. H., Mathis, P., Eker, A. P., and Brettel, K. (2000) Intraprotein radical transfer during photoactivation of DNA photolyase. Nature 405, 586-590
67. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U. S. A. 98, 10037-10041