Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 30 June 1995:
Vol. 268. no. 5219, pp. 1866 - 1872
DOI: 10.1126/science.7604260
Prev | Table of Contents | Next

Articles

Science, Vol 268, Issue 5219, 1866-1872
Copyright © 1995 by American Association for the Advancement of Science

articles

Crystal structure of DNA photolyase from Escherichia coli

HW Park, ST Kim, A Sancar, and J Deisenhofer

Department of Biochemistry, University of Texas Southwestern Medical Center, Dallas 75235, USA.

Photolyase repairs ultraviolet (UV) damage to DNA by splitting the cyclobutane ring of the major UV photoproduct, the cis, syn-cyclobutane pyrimidine dimer (Pyr <> Pyr). The reaction is initiated by blue light and proceeds through long-range energy transfer, single electron transfer, and enzyme catalysis by a radical mechanism. The three-dimensional crystallographic structure of DNA photolyase from Escherichia coli is presented and the atomic model was refined to an R value of 0.172 at 2.3 A resolution. The polypeptide chain of 471 amino acids is folded into an amino-terminal alpha/beta domain resembling dinucleotide binding domains and a carboxyl-terminal helical domain; a loop of 72 residues connects the domains. The light-harvesting cofactor 5,10-methenyltetrahydrofolylpolyglutamate (MTHF) binds in a cleft between the two domains. Energy transfer from MTHF to the catalytic cofactor flavin adenine dinucleotide (FAD) occurs over a distance of 16.8 A. The FAD adopts a U-shaped conformation between two helix clusters in the center of the helical domain and is accessible through a hole in the surface of this domain. Dimensions and polarity of the hole match those of a Pyr <> Pyr dinucleotide, suggesting that the Pyr <> Pyr "flips out" of the helix to fit into this hole, and that electron transfer between the flavin and the Pyr <> Pyr occurs over van der Waals contact distance.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Evolution of Mutation Rates: Phylogenomic Analysis of the Photolyase/Cryptochrome Family.
J. I. Lucas-Lledo and M. Lynch (2009)
Mol. Biol. Evol. 26, 1143-1153
   Abstract »    Full Text »    PDF »
Functional motifs in the (6-4) photolyase crystal structure make a comparative framework for DNA repair photolyases and clock cryptochromes.
K. Hitomi, L. DiTacchio, A. S. Arvai, J. Yamamoto, S.-T. Kim, T. Todo, J. A. Tainer, S. Iwai, S. Panda, and E. D. Getzoff (2009)
PNAS 106, 6962-6967
   Abstract »    Full Text »    PDF »
Recognition and repair of UV lesions in loop structures of duplex DNA by DASH-type cryptochrome.
R. Pokorny, T. Klar, U. Hennecke, T. Carell, A. Batschauer, and L.-O. Essen (2008)
PNAS 105, 21023-21027
   Abstract »    Full Text »    PDF »
Structure and Function of Photolyase and in Vivo Enzymology: 50th Anniversary.
A. Sancar (2008)
J. Biol. Chem. 283, 32153-32157
   Full Text »    PDF »
Magnetic-field effect on the photoactivation reaction of Escherichia coli DNA photolyase.
K. B. Henbest, K. Maeda, P. J. Hore, M. Joshi, A. Bacher, R. Bittl, S. Weber, C. R. Timmel, and E. Schleicher (2008)
PNAS 105, 14395-14399
   Abstract »    Full Text »    PDF »
The Native Cyclobutane Pyrimidine Dimer Photolyase of Rice Is Phosphorylated.
M. Teranishi, K. Nakamura, H. Morioka, K. Yamamoto, and J. Hidema (2008)
Plant Physiology 146, 1941-1951
   Abstract »    Full Text »    PDF »
Animal Type 1 Cryptochromes: ANALYSIS OF THE REDOX STATE OF THE FLAVIN COFACTOR BY SITE-DIRECTED MUTAGENESIS.
N. Ozturk, S.-H. Song, C. P. Selby, and A. Sancar (2008)
J. Biol. Chem. 283, 3256-3263
   Abstract »    Full Text »    PDF »
Dipole-Dipole Interaction Stabilizes the Transition State of Apurinic/Apyrimidinic Endonuclease Abasic Site Interaction.
S. Adhikari, A. Uren, and R. Roy (2008)
J. Biol. Chem. 283, 1334-1339
   Abstract »    Full Text »    PDF »
Formation and Function of Flavin Anion Radical in Cryptochrome 1 Blue-Light Photoreceptor of Monarch Butterfly.
S.-H. Song, N. Ozturk, T. R. Denaro, N. O. Arat, Y.-T. Kao, H. Zhu, D. Zhong, S. M. Reppert, and A. Sancar (2007)
J. Biol. Chem. 282, 17608-17612
   Abstract »    Full Text »    PDF »
The Signaling State of Arabidopsis Cryptochrome 2 Contains Flavin Semiquinone.
R. Banerjee, E. Schleicher, S. Meier, R. M. Viana, R. Pokorny, M. Ahmad, R. Bittl, and A. Batschauer (2007)
J. Biol. Chem. 282, 14916-14922
   Abstract »    Full Text »    PDF »
A Novel Photoreaction Mechanism for the Circadian Blue Light Photoreceptor Drosophila Cryptochrome.
A. Berndt, T. Kottke, H. Breitkreuz, R. Dvorsky, S. Hennig, M. Alexander, and E. Wolf (2007)
J. Biol. Chem. 282, 13011-13021
   Abstract »    Full Text »    PDF »
Derepression of the NC80 motif is critical for the photoactivation of Arabidopsis CRY2.
X. Yu, D. Shalitin, X. Liu, M. Maymon, J. Klejnot, H. Yang, J. Lopez, X. Zhao, K. T. Bendehakkalu, and C. Lin (2007)
PNAS 104, 7289-7294
   Abstract »    Full Text »    PDF »
Electron Nuclear Double Resonance Differentiates Complementary Roles for Active Site Histidines in (6-4) Photolyase.
E. Schleicher, K. Hitomi, C. W. M. Kay, E. D. Getzoff, T. Todo, and S. Weber (2007)
J. Biol. Chem. 282, 4738-4747
   Abstract »    Full Text »    PDF »
Photoselected electron transfer pathways in DNA photolyase.
T. R. Prytkova, D. N. Beratan, and S. S. Skourtis (2007)
PNAS 104, 802-807
   Abstract »    Full Text »    PDF »
Structure and Function of Animal Cryptochromes.
N. Ozturk, S.-H. Song, S. Ozgur, C. P. Selby, L. Morrison, C. Partch, D. Zhong, and A. Sancar (2007)
Cold Spring Harb Symp Quant Biol 72, 119-131
   Abstract »    PDF »
A cryptochrome/photolyase class of enzymes with single-stranded DNA-specific photolyase activity.
C. P. Selby and A. Sancar (2006)
PNAS 103, 17696-17700
   Abstract »    Full Text »    PDF »
Crystal structure of cryptochrome 3 from Arabidopsis thaliana and its implications for photolyase activity.
Y. Huang, R. Baxter, B. S. Smith, C. L. Partch, C. L. Colbert, and J. Deisenhofer (2006)
PNAS 103, 17701-17706
   Abstract »    Full Text »    PDF »
Similarities and Differences between Cyclobutane Pyrimidine Dimer Photolyase and (6-4) Photolyase as Revealed by Resonance Raman Spectroscopy: ELECTRON TRANSFER FROM THE FAD COFACTOR TO ULTRAVIOLET-DAMAGED DNA.
J. Li, T. Uchida, T. Todo, and T. Kitagawa (2006)
J. Biol. Chem. 281, 25551-25559
   Abstract »    Full Text »    PDF »
Inaugural Article: Direct observation of thymine dimer repair in DNA by photolyase.
Y.-T. Kao, C. Saxena, L. Wang, A. Sancar, and D. Zhong (2005)
PNAS 102, 16128-16132
   Abstract »    Full Text »    PDF »
Identification and Characterization of a Second Chromophore of DNA Photolyase from Thermus thermophilus HB27.
T. Ueda, A. Kato, S. Kuramitsu, H. Terasawa, and I. Shimada (2005)
J. Biol. Chem. 280, 36237-36243
   Abstract »    Full Text »    PDF »
Supramolecular Structure and Dynamics Special Feature: Electrically monitoring DNA repair by photolyase.
M. C. DeRosa, A. Sancar, and J. K. Barton (2005)
PNAS 102, 10788-10792
   Abstract »    Full Text »    PDF »
Light-induced Electron Transfer in Arabidopsis Cryptochrome-1 Correlates with in Vivo Function.
A. Zeugner, M. Byrdin, J.-P. Bouly, N. Bakrim, B. Giovani, K. Brettel, and M. Ahmad (2005)
J. Biol. Chem. 280, 19437-19440
   Abstract »    Full Text »    PDF »
NMR Study of Repair Mechanism of DNA Photolyase by FAD-induced Paramagnetic Relaxation Enhancement.
T. Ueda, A. Kato, Y. Ogawa, T. Torizawa, S. Kuramitsu, S. Iwai, H. Terasawa, and I. Shimada (2004)
J. Biol. Chem. 279, 52574-52579
   Abstract »    Full Text »    PDF »
Crystal Structure of a Photolyase Bound to a CPD-Like DNA Lesion After in Situ Repair.
A. Mees, T. Klar, P. Gnau, U. Hennecke, A. P. M. Eker, T. Carell, and L.-O. Essen (2004)
Science 306, 1789-1793
   Abstract »    Full Text »    PDF »
Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana.
C. A. Brautigam, B. S. Smith, Z. Ma, M. Palnitkar, D. R. Tomchick, M. Machius, and J. Deisenhofer (2004)
PNAS 101, 12142-12147
   Abstract »    Full Text »    PDF »
Regulation of the Mammalian Circadian Clock by Cryptochrome.
A. Sancar (2004)
J. Biol. Chem. 279, 34079-34082
   Full Text »    PDF »
Serine phosphorylation of mCRY1 and mCRY2 by mitogen-activated protein kinase.
K. Sanada, Y. Harada, M. Sakai, T. Todo, and Y. Fukada (2004)
Genes Cells 9, 697-708
   Abstract »    Full Text »    PDF »
Investigation of the Cyclobutane Pyrimidine Dimer (CPD) Photolyase DNA Recognition Mechanism by NMR Analyses.
T. Torizawa, T. Ueda, S. Kuramitsu, K. Hitomi, T. Todo, S. Iwai, K. Morikawa, and I. Shimada (2004)
J. Biol. Chem. 279, 32950-32956
   Abstract »    Full Text »    PDF »
Identification of cryptochrome DASH from vertebrates.
H. Daiyasu, T. Ishikawa, K.-i. Kuma, S. Iwai, T. Todo, and H. Toh (2004)
Genes Cells 9, 479-495
   Abstract »    Full Text »    PDF »
NMR structure of the DNA decamer duplex containing double T{middle dot}G mismatches of cis-syn cyclobutane pyrimidine dimer: implications for DNA damage recognition by the XPC-hHR23B complex.
J.-H. Lee, C.-J. Park, J.-S. Shin, T. Ikegami, H. Akutsu, and B.-S. Choi (2004)
Nucleic Acids Res. 32, 2474-2481
   Abstract »    Full Text »    PDF »
Structural Studies on Flavin Reductase PheA2 Reveal Binding of NAD in an Unusual Folded Conformation and Support Novel Mechanism of Action.
R. H. H. van den Heuvel, A. H. Westphal, A. J. R. Heck, M. A. Walsh, S. Rovida, W. J. H. van Berkel, and A. Mattevi (2004)
J. Biol. Chem. 279, 12860-12867
   Abstract »    Full Text »    PDF »
Functional and Structural Analyses of Cryptochrome: VERTEBRATE CRY REGIONS RESPONSIBLE FOR INTERACTION WITH THE CLOCK:BMAL1 HETERODIMER AND ITS NUCLEAR LOCALIZATION.
J. Hirayama, H. Nakamura, T. Ishikawa, Y. Kobayashi, and T. Todo (2003)
J. Biol. Chem. 278, 35620-35628
   Abstract »    Full Text »    PDF »
Dissection of the triple tryptophan electron transfer chain in Escherichia coli DNA photolyase: Trp382 is the primary donor in photoactivation.
M. Byrdin, A. P. M. Eker, M. H. Vos, and K. Brettel (2003)
PNAS 100, 8676-8681
   Abstract »    Full Text »    PDF »
Chromatin Remodeling Activities Act on UV-damaged Nucleosomes and Modulate DNA Damage Accessibility to Photolyase.
H. Gaillard, D. J. Fitzgerald, C. L. Smith, C. L. Peterson, T. J. Richmond, and F. Thoma (2003)
J. Biol. Chem. 278, 17655-17663
   Abstract »    Full Text »    PDF »
Blue Light Perception in Plants. DETECTION AND CHARACTERIZATION OF A LIGHT-INDUCED NEUTRAL FLAVIN RADICAL IN A C450A MUTANT OF PHOTOTROPIN.
C. W. M. Kay, E. Schleicher, A. Kuppig, H. Hofner, W. Rudiger, M. Schleicher, M. Fischer, A. Bacher, S. Weber, and G. Richter (2003)
J. Biol. Chem. 278, 10973-10982
   Abstract »    Full Text »    PDF »
Crystal structure of a DNA decamer containing a cis-syn thymine dimer.
H. Park, K. Zhang, Y. Ren, S. Nadji, N. Sinha, J.-S. Taylor, and C. Kang (2002)
PNAS 99, 15965-15970
   Abstract »    Full Text »    PDF »
Cyclobutylpyrimidine Dimer Base Flipping by DNA Photolyase.
K. S. Christine, A. W. MacFarlane IV, K. Yang, and R. J. Stanley (2002)
J. Biol. Chem. 277, 38339-38344
   Abstract »    Full Text »    PDF »
Blue Light Receptors and Signal Transduction.
C. Lin (2002)
PLANT CELL 14, S207-225
   Full Text »    PDF »
Bacterial cryptochrome and photolyase: characterization of two photolyase-like genes of Synechocystis sp. PCC6803.
K. Hitomi, K. Okamoto, H. Daiyasu, H. Miyashita, S. Iwai, H. Toh, M. Ishiura, and T. Todo (2000)
Nucleic Acids Res. 28, 2353-2362
   Abstract »    Full Text »    PDF »
Photolyase/Cryptochrome Family Blue-light Photoreceptors Use Light Energy to Repair DNA or Set the Circadian Clock.
A. SANCAR, C. THOMPSON, R.J. THRESHER, F. ARAUJO, J. MO, S. OZGUR, E. VAGAS, L. DAWUT, and C.P. SELBY (2000)
Cold Spring Harb Symp Quant Biol 65, 157-172
   Abstract »    PDF »
Photoreceptors in Signal Transduction: Pathways of Enlightenment.
H. B. Smith (2000)
PLANT CELL 12, 1-4
   Full Text »    PDF »
Cryptochrome Nucleocytoplasmic Distribution and Gene Expression Are Regulated by Light Quality in the Fern Adiantum capillus-veneris.
T. Imaizumi, T. Kanegae, and M. Wada (2000)
PLANT CELL 12, 81-96
   Abstract »    Full Text »    PDF »
Tryptophan H33 plays an important role in pyrimidine (6-4) pyrimidone photoproduct binding by a high-affinity antibody.
H. Kobayashi, J. Kato, H. Morioka, J. D. Stewart, and E. Ohtsuka (1999)
Protein Eng. Des. Sel. 12, 879-884
   Abstract »    Full Text »    PDF »
Rapid Blue Light Regulation of a Trichoderma harzianum Photolyase Gene.
G. Berrocal-Tito, L. Sametz-Baron, K. Eichenberg, B. A. Horwitz, and A. Herrera-Estrella (1999)
J. Biol. Chem. 274, 14288-14294
   Abstract »    Full Text »    PDF »
Intraprotein electron transfer between tyrosine and tryptophan in DNA photolyase from Anacystis nidulans.
C. Aubert, P. Mathis, A. P. M. Eker, and K. Brettel (1999)
PNAS 96, 5423-5427
   Abstract »    Full Text »    PDF »
Cryptochromes: Blue Light Receptors for Plants and Animals.
A. R. Cashmore, J. A. Jarillo, Y. Wu, and D. Liu (1999)
Science 284, 760-765
   Abstract »    Full Text »
Role of Mouse Cryptochrome Blue-Light Photoreceptor in Circadian Photoresponses.
R. J. Thresher, M. H. Vitaterna, Y. Miyamoto, A. Kazantsev, D. S. Hsu, C. Petit, C. P. Selby, L. Dawut, O. Smithies, J. S. Takahashi, et al. (1998)
Science 282, 1490-1494
   Abstract »    Full Text »
Charge transfer and transport in DNA.
J. Jortner, M. Bixon, T. Langenbacher, and M. E. Michel-Beyerle (1998)
PNAS 95, 12759-12765
   Abstract »    Full Text »    PDF »
Enzymatic reaction with unnatural substrates: DNA photolyase (Escherichia coli) recognizes and reverses thymine [2+2] dimers in the DNA strand of a DNA/PNA hybrid duplex.
D. Ramaiah, Y. Kan, T. Koch, H. Orum, and G. B. Schuster (1998)
PNAS 95, 12902-12905
   Abstract »    Full Text »    PDF »
Evidence for Dinucleotide Flipping by DNA Photolyase.
B. J. Vande Berg and G. B. Sancar (1998)
J. Biol. Chem. 273, 20276-20284
   Abstract »    Full Text »    PDF »
Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2.
C. Lin, H. Yang, H. Guo, T. Mockler, J. Chen, and A. R. Cashmore (1998)
PNAS 95, 2686-2690
   Abstract »    Full Text »    PDF »
Regulation of Flowering Time by Arabidopsis Photoreceptors.
H. Guo, H. Yang, T. C. Mockler, and C. Lin (1998)
Science 279, 1360-1363
   Abstract »    Full Text »
Direct Measurement of the Substrate Preference of Uracil-DNA Glycosylase.
G. Panayotou, T. Brown, T. Barlow, L. H. Pearl, and R. Savva (1998)
J. Biol. Chem. 273, 45-50
   Abstract »    Full Text »    PDF »
Reaction Mechanism of (6-4) Photolyase.
X. Zhao, J. Liu, D. S. Hsu, S. Zhao, J.-S. Taylor, and A. Sancar (1997)
J. Biol. Chem. 272, 32580-32590
   Abstract »    Full Text »    PDF »
The Role of Base Flipping in Damage Recognition and Catalysis by T4 Endonuclease V.
A. K. McCullough, M. L. Dodson, O. D. Scharer, and R. S. Lloyd (1997)
J. Biol. Chem. 272, 27210-27217
   Abstract »    Full Text »    PDF »
Repair of O6-Benzylguanine by the Escherichia coli Ada and Ogt and the Human O6-Alkylguanine-DNA Alkyltransferases.
K. Goodtzova, S. Kanugula, S. Edara, G. T. Pauly, R. C. Moschel, and A. E. Pegg (1997)
J. Biol. Chem. 272, 8332-8339
   Abstract »    Full Text »    PDF »
DNA Distortion and Base Flipping by the EcoRV DNA Methyltransferase. A STUDY USING INTERFERENCE AT dA AND T BASES AND MODIFIED DEOXYNUCLEOSIDES.
S. Cal and B. A. Connolly (1997)
J. Biol. Chem. 272, 490-496
   Abstract »    Full Text »    PDF »
Photolyase of Myxococcus xanthus, a Gram-negative Eubacterium, Is More Similar to Photolyases Found in Archaea and ``Higher'' Eukaryotes than to Photolyases of Other Eubacteria.
K. A. O'Connor, M. J. McBride, M. West, H. Yu, L. Trinh, K. Yuan, T. Lee, and D. R. Zusman (1996)
J. Biol. Chem. 271, 6252-6259
   Abstract »    Full Text »    PDF »
Solution Structure of a Cisplatin-Induced DNA Interstrand Cross-Link.
H. Huang, L. Zhu, B. R. Reid, G. P. Drobny, and P. B. Hopkins (1995)
Science 270, 1842-1845
   Abstract »    PDF »
The structure of photolyase: using photon energy for DNA repair.
J. Hearst (1995)
Science 268, 1858-1859
   PDF »
Role of Two Histidines in the (6-4) Photolyase Reaction.
K. Hitomi, H. Nakamura, S.-T. Kim, T. Mizukoshi, T. Ishikawa, S. Iwai, and T. Todo (2001)
J. Biol. Chem. 276, 10103-10109
   Abstract »    Full Text »    PDF »
Photoactivation of the flavin cofactor in Xenopus laevis (6 - 4) photolyase: Observation of a transient tyrosyl radical by time-resolved electron paramagnetic resonance.
S. Weber, C. W. M. Kay, H. Mogling, K. Mobius, K. Hitomi, and T. Todo (2002)
PNAS 99, 1319-1322
   Abstract »    Full Text »    PDF »
Crystal structure of thermostable DNA photolyase: Pyrimidine-dimer recognition mechanism.
H. Komori, R. Masui, S. Kuramitsu, S. Yokoyama, T. Shibata, Y. Inoue, and K. Miki (2001)
PNAS 98, 13560-13565
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)