Femtochemistry in enzyme catalysis: DNA photolyase

Cell Biochemistry and Biophysics

Volumn 48, Issue 1, 2007, Pages 32-44

  Kao, Ya Ting ^a   Saxena, Chaitanya ^a   Wang, Lijuan ^a   Sancar, Aziz ^b   Zhong, Dongping ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Cyclobutane pyrimidine dimer (CPD); DNA photolyase; DNA repair; Electron transfer (ET); Enzyme catalysis; Femtochemistry; Photoinitiation; Photoreduction; Photorepair; Resonance energy transfer (RET); Solvation dynamics

Indexed keywords

DEOXYRIBODIPYRIMIDINE PHOTOLYASE;

ASPERGILLUS NIDULANS; BIOLOGICAL MODEL; CATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; DNA REPAIR; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; ENZYMOLOGY; ESCHERICHIA COLI; KINETICS; METABOLISM; PHOTOCHEMISTRY; REVIEW; THERMODYNAMICS; TIME; X RAY CRYSTALLOGRAPHY;

ASPERGILLUS NIDULANS; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DNA REPAIR; ELECTRON TRANSPORT; ESCHERICHIA COLI; KINETICS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PHOTOCHEMISTRY; THERMODYNAMICS; TIME FACTORS;

EID: 34548331981     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12013-007-0034-5     Document Type: Review

References (73)

1. Zewail, A. H. (2000). Femtochemistry: Atomic-scale dynamics of the chemical bond using ultrafast lasers. In T. Frängsmyr (Ed.), Les Prix Nobel: The Nobel prizes 1999 (p. 110). Stockholm: Almqvist & Wiksell.
2. Zewail, A. H. (2006). 4D ultrafast electron diffraction, crystallography, and microscopy. Annual Review of Physical Chemistry, 57, 65-103.
3. Callender, R., & Dyer, R. B. (2006). Advances in time-resolved approaches to characterize the dynamical nature of enzymatic catalysis. Chemical Reviews, 106, 3031-3042.
4. Boehr, D. D., Dyson, H. J., & Wright, P. E. (2006). An NMR perspective on enzyme dynamics. Chemical Reviews, 106, 3055-3079.
5. Wolynes, P. G. (2005). Energy landscapes and solved protein-folding problems. Philosophical Transactions of the Royal Society of London, A, 363, 453-464.
6. Frauenfelder, H., Sligar, S. G., & Wolynes, P. G. (1991). The energy landscapes and motions of proteins. Science, 254, 1598-1603.
7. Krushelnitsky, A., & Reichert, D. (2005). Solid-state NMR and protein dynamics. Progress in NMR Spectroscopy, 47, 1-25.
8. Kay, L. E. (2005). NMR studies of protein structure and dynamics. Journal of Magnetic Resonance, 173, 193-207.
9. Nagy, A., Prokhorenko, V., & Miller, R. J. D. (2006). Do we live in a quantum world? Advances in multidimensional coherent spectroscopies refine our understanding of quantum coherences and structural dynamics of biological systems. Current Opinion in Structural Biology, 16, 654-663.
10. Slayton, R. M., & Anfinrud, P. A. (1997). Time-resolved mid-infrared spectroscopy: Methods and biological applications. Current Opinion in Structural Biology, 7, 717-721.
11. Sancar, A. (2003). Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chemical Reviews, 103, 2203-2237.
12. Park, H. W., Kim, S. T., Sancar, A., & Deisenhofer, J. (1995). Crystal structure of DNA photolyase from Escherichia coli. Science, 268, 1866-1872.
13. Sancar, G. B., Jorns, M. S., Payne, G., Fluke, D. J., Rupert, C. S., & Sancar, A. (1987). Action mechanism of Escherichia coli DNA photolyase. III. Photolysis of the enzyme-substrate complex and the absolute action spectrum. Journal of Biological Chemistry, 262, 492-498.
14. 2-MTHF forms of Escherichia coli DNA photolyase. Biochemistry, 29, 7715-7727.
15. Ramsey, A. J., Alderfer, J. L., & Jorns, M. S. (1992). Energy transduction during catalysis by Escherichia coli DNA photolyase. Biochemistry, 31, 7134-7142.
16. Kim, S. T., Heelis, P. F., Okamura, T., Hirata, Y., Mataga, N., & Sancar, A. (1991). Determination of rates and yields of interchromophore (Folate → Flavin) energy transfer and intermolecular (Flavin → DNA) electron transfer in Escherichia coli photolyase by time-resolved fluorescence and absorption spectroscopy. Biochemistry, 30, 11262-11270.
17. Langenbacher, T., Zhao, X. D., Bieser, G., Heelis, P. F., Sancar, A., & Michel-Beyerle, M. E. (1997). Substrate and temperature dependence of DNA photolyase repair activity examined with ultrafast spectroscopy. Journal of the American Chemical Society, 119, 10532-10536.
18. MacFarlane, A. W., & Stanley, R. J. (2003). Cis-syn thymidine dimer repair by DNA photolyase in real time. Biochemistry, 42, 8558-8568.
19. Sanders, D. B., & Wiest, O. (1999). A model for the enzyme-substrate complex of DNA photolyase and photodamaged DNA. Journal of the American Chemical Society, 121, 5127-5134.
20. - and DNA thymine dimer. Journal of the American Chemical Society, 122, 1057-1065.
21. Komori, H., Masui, R., Kuramitsu, S., Yokoyama, S., Shibata, T., Inoue, Y., & Miki, K. (2001). Crystal structure of thermostable DNA photolyase: Pyrimidine-dimer recognition mechanism. Proceedings of the National Academy of Sciences of the United States of America, 98, 13560-13565.
22. Mees, A., Klar, T., Gnau, P., Hennecke, U., Eker, A. P. M., Carell, T., & Essen, L. O. (2004). Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science, 306, 1789-1793.
23. Kao, Y.-T., Saxena, C., Wang, L., Sancar, A., & Zhong, D. (2005). Direct observation of thymine dimer repair in DNA by photolyase. Proceedings of the National Academy of Sciences of the United States of America, 102, 16128-16132.
24. Saxena, C., Sancar, A., & Zhong, D. (2004). Femtosecond dynamics of DNA photolyase: Energy transfer of antenna initiation and electron transfer of cofactor reduction. Journal of Physical Chemistry B, 108, 18026-18033.
25. -, the catalytically active form of the cofactor. Proceedings of the National Academy of Sciences of the United States of America, 90, 8023-8027.
26. Li, Y. F., Heelis, P. F., & 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.
27. Heelis, P. F., Payne, G., & Sancar, A. (1987). Photochemical properties of Escherichia coli DNA photolyase: Selective photodecomposition of the second chromophore. Biochemistry, 26, 4634-4640.
28. Heelis, P. F., Okamura, T., & Sancar, A. (1990). Excited-state properties of Escherichia coli DNA photolyase in the picosecond to millisecond time scale. Biochemistry, 29, 5694-5698.
29. Aubert, C., Vos, M. H., Mathis, P., Eker, A. P. M., & Brettel, K. (2000). Intraprotein radical transfer during photoactivation of DNA photolyase. Nature, 405, 586-590.
30. Byrdin, M., Eker, A. P. M., Vos, M. H., & Brettel, K. (2003). Dissection of the triple tryptophan electron transfer chain in Escherichia coli DNA photolyase: Trp382 is the primary donor in photoactivation. Proceedings of the National Academy of Sciences of the United States of America, 100, 8676-8681.
31. Wang, H. Y., Saxena, C., Quan, D. H., Sancar, A., & Zhong, D. (2005). Femtosecond dynamics of flavin cofactor in DNA photolyase: Radical reduction, local solvation, and charge recombination. Journal of Physical Chemistry B, 109, 1329-1333.
32. Defelippis, M. R., Murthy, C. P., Broitman, F., Weinraub, D., Faraggi, M., & Klapper, M. H. (1991). Electrochemical properties of tyrosine phenoxy and tryptophan indolyl radicals in peptides and amino acid analogs. Journal of Physical Chemistry, 95, 3416-3419.
33. Heelis, P. F., Deeble, D. J., Kim, S. T., & Sancar, A. (1992). Splitting of cis-syn cyclobutane thymine-thymine dimers by radiolysis and its relevance to enzymatic photoreactivation. International Journal of Radiation Biology, 62, 137-143.
34. Mulliken, R. S. (1952). Molecular compounds and their spectra II. Journal of the American Chemical Society, 74, 811-824.
35. Cheng, P. Y., Zhong, D., & Zewail, A. H. (1996). Femtosecond real-time probing of reactions. XXI. Direct observation of transition-state dynamics and structure in charge-transfer reactions. Journal of Chemical Physics, 105, 6216-6248.
36. 306 to FADH. Biophysical Journal, 76, 1241-1249.
37. 4 at 77 K. Journal of Chemical Physics, 44, 2375-2377.
38. Mataga, N., Chosrowjan, H., Taniguchi, S., Tanaka, F., Kido, N., & Kitamura, M. (2002). Femtosecond fluorescence dynamics of flavoproteins: Comparative studies on flavodoxin, its site-directed mutants, and riboflavin binding protein regarding ultrafast electron transfer in protein nanospaces. Journal of Physical Chemistry B, 106, 8917-8920.
39. 2)-binding protein and in glucose oxidase enzyme. Proceedings of the National Academy of Sciences of the United States of America, 98, 11867-11872.
40. Mataga, N., Chosrowjan, H., Shibata, Y., Tanaka, F., Nishina, Y., Shiga, K. (2000). Dynamics and mechanisms of ultrafast fluorescence quenching reactions of flavin chromophores in protein nanospace. Journal of Physical Chemistry B, 104, 10667-10677.
41. Mattos, C. (2002). Protein-water interactions in a dynamic world. Trends in Biochemical Sciences, 27, 203-208.
42. Kim, S. T., & Sancar, A. (1991). Effect of base, pentose, and phosphodiester backbone structures on binding and repair of pyrimidine dimers by Escherichia coli DNA photolyase. Biochemistry, 30, 8623-8630.
43. Tamada, T., Kitadokoro, K., Higuchi, Y., Inaka, K., Yasui, A., de Ruiter, P. E., Eker, A. P. M., & Miki, K. (1997). Crystal structure of DNA photolyase from Anacystis nidulans. Nature Structural & Molecular Biology, 4, 887-891.
44. Seidel, C. A. M., Schulz, A., & Sauer, M. H. M. (1996). Nucleobase-specific quenching of fluorescent dyes. 1. Nucleobase one-electron redox potentials and their correlation with static and dynamic quenching efficiencies. Journal of Physical Chemistry, 100, 5541-5553.
45. Song, Q. H., Tang, W. M., Hei, X. M., Wang, H. B., Guo, Q. X., & Yu, S. Q. (2005). Efficient photosensitized splitting of thymine dimer by a covalently linked tryptophan in solvents of high polarity. European Journal of Organic Chemistry, 1097-1106.
46. Schramm, V. L. (2005). Enzymatic transition states and transition state analogues. Current Opinion in Structural Biology, 15, 604-613.
47. Wolfenden, R. (2003). Thermodynamic and extrathermodynamic requirements of enzyme catalysis. Biophysical Chemistry, 105, 559-572.
48. Boehr, D. D., McElheny, D., Dyson, H. J., & Wright, P. E. (2006). The dynamic energy landscape of dihydrofolate reductase catalysis. Science, 313, 1638-1642.
49. Vendruscolo, M., & Dobson, C. M. (2006). Dynamic visions of enzymatic reactions. Science, 313, 1586-1587.
50. Hammes-Schiffer, S., & Benkovic, S. J. (2006). Relating protein motion to catalysis. Annual Review of Biochemistry, 75, 519-541.
51. Olsson, M. H. M., Parson, W. W., & Warshel, A. (2006). Dynamical contributions to enzyme catalysis: Critical tests of a popular hypothesis. Chemical Reviews, 106, 1737-1756.
52. Pineda, J., & Schwartz, S. D. (2006). Protein dynamics and catalysis: The problems of transition state theory and the subtlety of dynamic control. Philosophical Transactions of the Royal Society of London, B, 361, 1433-1438.
53. Warshel, A., Sharma, P. K., Kato, M., Xiang, Y., Liu, H. B., & Olsson, M. H. M. (2006). Electrostatic basis for enzyme catalysis. Chemical Reviews, 106, 3210-3235.
54. Pu, J. Z., Gao, J., & Truhlar, D. G. (2006). Multidimensional tunneling, recrossing, and the transmission coefficient for enzymatic reactions. Chemical Reviews, 106, 3140-3169.
55. Antoniou, D., Basner, J., Núñez, S., & Schwartz, S. D. (2006). Computational and theoretical methods to explore the relation between enzyme dynamics and catalysis. Chemical Reviews, 106, 3170-3187.
56. Agarwal, P. K. (2006). Enzymes: An integrated view of structure, dynamics and function. Microbial Cell Factories, 5, 2.
57. Zhang, X. Y., & Houk, K. N. (2005). Why enzymes are proficient catalysts: Beyond the Pauling paradigm. Accounts of Chemical Research, 38, 379-385.
58. Bruice, T. C. (2006). Computational approaches: Reaction trajectories, structures, and atomic motions. Enzyme reactions and proficiency. Chemical Reviews, 106, 3119-3139.
59. Gao, J., Ma, S. H., Major, D. T., Nam, K., Pu, J. Z., & Truhlar, D. G. (2006). Mechanisms and free energies of enzymatic reactions. Chemical Reviews, 106, 3188-3209.
60. Hammes-Schiffer, S. (2006). Hydrogen tunneling and protein motion in enzyme reactions. Accounts of Chemical Research, 39, 93-100.
61. Onuchic, J. N., Kobayashi, C., Miyashita, O., Jennings, P., & Baldridge, K. K. (2006). Exploring biomolecular machines: Energy landscape control of biological reactions. Philosophical Transactions of the Royal Society of London, B, 361, 1439-1443.
62. Eisenmesser, E. Z., Bosco, D. A., Akke, M., & Kern, D. (2002). Enzyme dynamics during catalysis. Science, 295, 1520-1523.
63. Eisenmesser, E. Z., Millet, O., Labeikovsky, W., Korzhnev, D. M., Wolf-Watz, M., Bosco, D. A., Skalicky, J. J., Kay, L. E., & Kern, D. (2005). Intrinsic dynamics of an enzyme underlies catalysis. Nature, 438, 117-121.
64. Garcia-Viloca, M., Gao, J., Karplus, M., & Truhlar, D. G. (2004). How enzymes work: Analysis by modern rate theory and computer simulations. Science, 303, 186-195.
65. Benkovic, S. J., & Hammes-Schiffer, S. (2003). A perspective on enzyme catalysis. Science, 301, 1196-1202.
66. Benkovic, S. J., & Hammes-Schiffer, S. (2006). Enzyme motions inside and out. Science, 312, 208-209.
67. Masgrau, L., Roujeinikova, A., Johannissen, L. O., Hothi, P., Basran, J., Ranaghan, K. E., Mulholland, A. J., Sutcliffe, M. J., Scrutton, N. S., Leys, D. (2006). Atomic description of an enzyme reaction dominated by proton tunneling. Science, 312, 237-241.
68. Knapp, M. J., Rickert K., Klinman, J. P. (2002). Temperature-dependent isotope effects in soybean lipoxygenase-1: Correlating hydrogen tunneling with protein dynamics. Journal of the American Chemical Society, 124, 3865-3874.
69. Knapp, M. J., Klinman, J. P. (2002). Environment coupled hydrogen tunneling-Linking catalysis to dynamics. European Journal of Biochemistry, 269, 3113-3121.
70. Klinman, J. P. (2006). Linking protein structure and dynamics to catalysis: The role of hydrogen tunnelling. Philosophical Transactions of the Royal Society of London, B, 361, 1323-1331.
71. Wang, L., Goodey, N. M., Benkovic, S. J., Kohen, A. (2006). Coordinated effects of distal mutations on environmentally coupled tunneling in dihydrofolate reductase. Proceedings of the National Academy of Sciences of the United States of America, 103, 15753-15758.
72. Wong, K. F., Selzer, T., Benkovic, S. J., & Hammes-Schiffer, S. (2005). Impact of distal mutations on the network of coupled motions correlated to hydride transfer in dihydrofolate reductase. Proceedings of the National Academy of Sciences of the United States of America, 102, 6807-6812.
73. Zhong, D. (2007). Ultrafast catalytic processes in enzymes. Current Opinion in Chemical Biology, 11, 174-181.