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J. Biol. Chem., Vol. 281, Issue 35, 25551-25559, September 1, 2006

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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^*

Jiang Li¹, Takeshi Uchida², Takeshi Todo^¶, and Teizo Kitagawa³

From the Okazaki Institute for Integrative Bioscience, National Institutes of Natural Sciences, Myodaiji, Okazaki, Aichi 444-8787, the Department of Photoscience, School of Advanced Sciences, Graduate University for Advanced Studies, Shonan Village, Hayama, Kanagawa 240-0193, and the ^¶Radiation Biology Center, Kyoto University, Yoshidakonoe-cho, Sakyo-ku, Kyoto 606-8501, Japan

The cyclobutane pyrimidine dimer (CPD) and (6-4) photoproduct, two major types of DNA damage caused by UV light, are repaired under illumination with near UV-visible light by CPD and (6-4) photolyases, respectively. To understand the mechanism of DNA repair, we examined the resonance Raman spectra of complexes between damaged DNA and the neutral semiquinoid and oxidized forms of (6-4) and CPD photolyases. The marker band for a neutral semiquinoid flavin and band I of the oxidized flavin, which are derived from the vibrations of the benzene ring of FAD, were shifted to lower frequencies upon binding of damaged DNA by CPD photolyase but not by (6-4) photolyase, indicating that CPD interacts with the benzene ring of FAD directly but that the (6-4) photoproduct does not. Bands II and VII of the oxidized flavin and the 1398/1391 cm^-1 bands of the neutral semiquinoid flavin, which may reflect the bending of U-shaped FAD, were altered upon substrate binding, suggesting that CPD and the (6-4) photoproduct interact with the adenine ring of FAD. When substrate was bound, there was an upshifted 1528 cm^-1 band of the neutral semiquinoid flavin in CPD photolyase, indicating a weakened hydrogen bond at N(5)-H of FAD, and band X seemed to be downshifted in (6-4) photolyase, indicating a weakened hydrogen bond at N(3)-H of FAD. These Raman spectra led us to conclude that the two photolyases have different electron transfer mechanisms as well as different hydrogen bonding environments, which account for the higher redox potential of CPD photolyase.

Received for publication, May 10, 2006 , and in revised form, June 27, 2006.

^* This work was supported in part by the Ministry of Education, Culture, Sports, Science, and Technology of Japan Grant-in-aid 14001004 (to T. K.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ Supported by a scholarship from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.

² Present address: Div. of Chemistry, Graduate School of Science, Hokkaido University, Sapporo 060-0810, Japan.

³ To whom correspondence should be addressed: Toyota Physical & Chemical Research Inst., Nagakute, Aichi 480-1192, Japan. Tel.: 81-564-59-5225; Fax: 81-564-59-5229; E-mail: teizo{at}ims.ac.jp.

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