Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter (O) August 30, 2016

Intramolecular Electron Transfer from Tryptophan to Guanosyl Radicals in a Linked System as a Model of DNA Repair

Olga B. Morozova, Natalya N. Fishman and Alexandra V. Yurkovskaya

Abstract

As a model of chemical DNA repair, intramolecular electron transfer from tryptophan to the radical of the purine base guanosine combined into a conjugate by a flexible linker was studied by time-resolved chemically induced dynamic nuclear polarization (CIDNP). The guanosyl radicals were photochemically generated in the quenching reaction of the triplet excited dye 2,2′-dipyridyl. The CIDNP kinetics was obtained by detection of NMR spectra containing anomalously enhanced signals of diamagnetic products that are formed during a variable period after excitation by a laser pulse. The kinetic data obtained for the protons located on the guanosyl and tryptophanyl moieties of the conjugate were compared to those obtained in photoreactions of the molecules containing the same linker, but with only one of the two reactive moieties of the conjugate – tryptophanyl or guanosyl. Strong differences between the CIDNP kinetics of different conjugates were revealed and explained by a rapid intramolecular electron transfer from tryptophan to the guanosyl radical in the conjugate. Model simulations of the CIDNP kinetics allowed for determination of the rate constant of intramolecular electron transfer at (1.0±0.5)×106 s–1 indicating a high potential of chemical repair of the guanosyl radical by means of electron transfer from the tryptophanyl moiety in a surrounding protein pool that can provide rather efficient protection of oxidized DNA bases from pathological damage on a submicrosecond time scale.


Dedicated to: Kev Salikhov on the occasion of his 80th birthday.


Funding source: Russian Science Foundation

Award Identifier / Grant number: 15-13-20035

Funding statement: This work was supported by the Russian Science Foundation (Grant No. 15-13-20035), and by FASO Russia (project 0333-2014-0001) at the transient absorption measurements. We are thankful to Dr. T. V. Abramova (ICBFM, Novosibirsk) for providing us with G-L-Trp, G-L and L-Trp compounds.

Acknowledgments

This work was supported by the Russian Science Foundation (Grant No. 15-13-20035), and by FASO Russia (project 0333-2014-0001) at the transient absorption measurements. We are thankful to Dr. T. V. Abramova (ICBFM, Novosibirsk) for providing us with G-L-Trp, G-L and L-Trp compounds.

References

1. S. Kimura, K. Sakaguchi, Chem. Rev. 106 (2006) 753.10.1021/cr040482nSearch in Google Scholar PubMed

2. C. M. Cuquerella, V. Lhiaubet-Vallet, F. Bosca, M. A. Miranda, Chem. Sci. 2 (2011) 1219.10.1039/c1sc00088hSearch in Google Scholar

3. D. L. Narayanan, R. N. Saladi, J. L. Fox, Int. J. Dermatol. 49 (2010) 978.10.1111/j.1365-4632.2010.04474.xSearch in Google Scholar PubMed

4. C. von Sonntag, Free-Radical-Induced DNA Damage and Its Repair, Springer Verlag, Berlin (2006).10.1007/3-540-30592-0Search in Google Scholar

5. Z. Cai, Z. Gu, M. D. Sevilla, J. Phys. Chem. B 105 (2001) 6031.10.1021/jp010358xSearch in Google Scholar

6. T. Melvin, S. W. Botchway, A. W. Parker, P. O’Neill, J. Am. Chem. Soc. 118 (1996) 10031.10.1021/ja961722mSearch in Google Scholar

7. T. Melvin, S. M. T. Cunniffe, P. O’Neill, A. W. Parker, T. Roldan-Arjona, Nucleic Acids Res. 26 (1998) 4935.10.1093/nar/26.21.4935Search in Google Scholar PubMed PubMed Central

8. T. Douki, D. Angelov, J. Cadet, J. Am. Chem. Soc. 123 (2001) 11360.10.1021/ja016426aSearch in Google Scholar PubMed

9. C. J. Burrows, J. G. Muller, Chem. Rev. 98 (1998) 1109.10.1021/cr960421sSearch in Google Scholar PubMed

10. R. L. Willson, P. Wardman, K. D. Asmus, Nature 252 (1974) 323.10.1038/252323a0Search in Google Scholar PubMed

11. R. Zheng, Y. Shi, Z. Jia, C. Zhao, Q. Zhang, X. Tan, Chem. Soc. Rev. 39 (2010) 2827.10.1039/b924875gSearch in Google Scholar PubMed

12. J. R. Milligan, J. A. Aguilera, A. Ly, N. Q. Tran, O. Hoang, J. F. Ward, Nucleic Acids Res. 31 (2003) 6258.10.1093/nar/gkg816Search in Google Scholar PubMed PubMed Central

13. J. R. Milligan, N. Q. Tran, A. Ly, J. F. Ward, Biochemistry 43 (2004) 5102.10.1021/bi030232lSearch in Google Scholar PubMed

14. J. R. Milligan, J. A. Aguilera, O. Hoang, A. Ly, N. Q. Tran, J. F. Ward, J. Am. Chem. Soc. 126 (2004) 1682.10.1021/ja030319uSearch in Google Scholar PubMed

15. A. Ly, N. Q. Tran, K. Sullivan, S. L. Bandong, J. R. Milligan, Org. Biomol. Chem. 3 (2005) 917.10.1039/b418681hSearch in Google Scholar PubMed

16. S. Steenken, S. V. Jovanovic, J. Am. Chem. Soc. 119 (1997) 617.10.1021/ja962255bSearch in Google Scholar

17. K. Kobayashi, S. Tagawa, J. Am. Chem. Soc. 125 (2003) 10213.10.1021/ja036211wSearch in Google Scholar PubMed

18. J. R. Milligan, J. A. Aguilera, O. Hoang, A. Ly, N. Q. Tran, J. F. Ward, J. Am. Chem. Soc. 126 (2004) 1682.10.1021/ja030319uSearch in Google Scholar

19. A. Ly, N. Q. Tran, J. F. Ward, J. R. Milligan, Biochemistry 43 (2004) 9098.10.1021/bi0494830Search in Google Scholar PubMed

20. A. Ly, S. L. Bandong, N. Q. Tran, K. J. Sullivan, J. R. Milligan, J. Phys. Chem. B 109 (2005) 13368.10.1021/jp050495kSearch in Google Scholar PubMed

21. A. Ly, N. Q. Tran, K. Silliavan, S. L. Bandong, J. F. Ward, J. R. Milligan, Org. Biomol. Chem. 3 (2005) 917.10.1039/b418681hSearch in Google Scholar PubMed

22. J. R. Milligan, J. A. Aguilera, A. Ly, O. Hoang, N. Q. Tran, J. F. Ward, Nucleic Acid Res. 31 (2003) 6258.10.1093/nar/gkg816Search in Google Scholar PubMed PubMed Central

23. G. L. Closs, R. J. Miller, J. Am. Chem. Soc. 101 (1979) 1639.10.1021/ja00500a068Search in Google Scholar

24. K. M. Salikhov, Y. N. Molin, R. Z. Sagdeev, A. L. Buchachenko, Spin Polarization and Magnetic Effects in Chemical Reactions, Elsevier, Amsterdam (1984).Search in Google Scholar

25. O. B. Morozova, A. S. Kiryutin, A. V. Yurkovskaya, J. Phys. Chem. B 112 (2008) 2747.10.1021/jp0752318Search in Google Scholar PubMed

26. O. B. Morozova, A. S. Kiryutin, R. Z. Sagdeev, A. V. Yurkovskaya, J. Phys. Chem. B 111 (2007) 7439.10.1021/jp067722iSearch in Google Scholar PubMed

27. O. B. Morozova, A. V. Yurkovskaya, J. Phys. Chem. B 119 (2015) 140.10.1021/jp511068nSearch in Google Scholar PubMed

28. T. V. Abramova, O. B. Morozova, V. N. Silnikov, A. V. Yurkovskaya, Beilstein J. Org. Chem. 9 (2013) 2898.10.3762/bjoc.9.326Search in Google Scholar PubMed PubMed Central

29. Y. P. Tsentalovich, O. B. Morozova, A. V. Yurkovskaya, P. J. Hore, J. Phys. Chem. A 103 (1999) 5362.10.1021/jp9909917Search in Google Scholar

30. A. V. Yurkovskaya, O. A. Snytnikova, O. B. Morozova, Y. P. Tsentalovich, R. Z. Sagdeev, Phys. Chem. Chem. Phys. 5 (2003) 3653.10.1039/B305783FSearch in Google Scholar

31. O. B. Morozova, N. N. Saprygina, O. S. Fedorova, A. V. Yurkovskaya, Appl. Magn. Reson. 41 (2011) 239.10.1007/s00723-011-0252-2Search in Google Scholar

32. G. Buntinx, O. Poizat, P. Valat, V. Wintgens, R. Righini, P. Foggi, J. Chim. Phys. Phys.-Chim. Biol. 90 (1993) 1733.10.1051/jcp/1993901733Search in Google Scholar

33. M. L. Posener, G. E. Adams, P. Wardman, R. B. Cundall, J. Chem. Soc. Faraday Trans. I 2 (1976) 2231.10.1039/f19767202231Search in Google Scholar

34. R. Kaptein, J. Chem. Soc. Chem. Comm. 14 (1971) 732.10.1039/c29710000732Search in Google Scholar

35. G. Bleifuss, M. Kolberg, S. Poetsch, W. Hofbauer, R. Bittl, W. Lubitz, A. Graeslund, G. Lassmann, F. Lendzian, Biochemistry 40 (2001) 15362.10.1021/bi010707dSearch in Google Scholar

36. S. Grosse, A. V. Yurkovskaya, J. Lopez, H.-M. Vieth, J. Phys. Chem. A 105 (2001) 6311.10.1021/jp004582iSearch in Google Scholar

37. A. Adhikary, A. Kumar, D. Becker, M. D. Sevilla, J. Phys. Chem. B 110 (2006) 24171.10.1021/jp064361ySearch in Google Scholar

38. S. Stob, R. Kaptein, Photochem. Photobiol. 49 (1989) 565.10.1111/j.1751-1097.1989.tb08425.xSearch in Google Scholar

39. G. L. Closs, E. V. Sitzmann, J. Am. Chem. Soc. 103 (1981) 3217.10.1021/ja00401a052Search in Google Scholar

40. J. Burri, H. Fischer, Chem. Phys. 161 (1992) 429.10.1016/0301-0104(92)80158-RSearch in Google Scholar

41. J. K. Vollenweider, H. Fischer, J. Hennig, R. Leuschner, Chem. Phys. 97 (1985) 217.10.1016/0301-0104(85)87033-6Search in Google Scholar

42. J. K. Vollenweider, H. Fischer, Chem. Phys. 124 (1988) 333.10.1016/0301-0104(88)87058-7Search in Google Scholar

43. O. B. Morozova, A. V. Yurkovskaya, Y. P. Tsentalovich, M. D. E. Forbes, R. Z. Sagdeev, J. Phys. Chem. B 106 (2002) 1455.10.1021/jp011858tSearch in Google Scholar

Received: 2016-4-8
Accepted: 2016-6-17
Published Online: 2016-8-30
Published in Print: 2017-3-1

©2017 Walter de Gruyter GmbH, Berlin/Boston

Scroll Up Arrow