Electron transfer between bases in double helical DNA

Science

Volumn 283, Issue 5400, 1999, Pages 375-381

  Kelley, Shana O ^a   Barton, Jacqueline K ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE A2; ADENINE DERIVATIVE; DNA; UNCLASSIFIED DRUG;

ARTICLE; BASE PAIRING; BINDING KINETICS; CHEMICAL ANALYSIS; DNA BINDING; DNA HELIX; ELECTRON TRANSPORT; LIGHT; MOLECULAR INTERACTION; PRIORITY JOURNAL; SPECTROSCOPY; STRUCTURE ANALYSIS;

2-AMINOPURINE; ADENINE; BASE PAIRING; DNA; ELECTRONS; GUANINE; HYDROGEN BONDING; KINETICS; LIGHT; NUCLEIC ACID CONFORMATION; OXIDATION-REDUCTION; SPECTROMETRY, FLUORESCENCE; THERMODYNAMICS;

EID: 0033555454     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.283.5400.375     Document Type: Article

References (60)

1. R. E. Holmlin, P. J. Dandliker, J. K. Barton, Angew. Chem. Int. Ed. 36, 2714 (1997); S. O. Kelley and J. K. Barton, Met. Ions Biol. Sys., in press.
2. R. E. Holmlin, P. J. Dandliker, J. K. Barton, Angew. Chem. Int. Ed. 36, 2714 (1997); S. O. Kelley and J. K. Barton, Met. Ions Biol. Sys., in press.
3. D. B. Hall, R. E. Holmlin, J. K. Barton, Nature 382, 731 (1996); D. B. Hall and J. K. Barton, J. Am. Chem. Soc. 119, 5045 (1997); M. R. Arkin, E. D. A. Stemp, J. K. Barton, Chem. Biol. 4, 389 (1997); P. J. Dandliker, R. E. Holmlin, J. K. Barton, Science 275, 1465 (1997); S. M. Gasper and G. B. Schuster, J. Am. Chem. Soc. 119, 12762 (1997); P. J. Dandliker, M. E. Nunez, J. K. Barton, Biochemistry 37, 6491 (1998).
4. D. B. Hall, R. E. Holmlin, J. K. Barton, Nature 382, 731 (1996); D. B. Hall and J. K. Barton, J. Am. Chem. Soc. 119, 5045 (1997); M. R. Arkin, E. D. A. Stemp, J. K. Barton, Chem. Biol. 4, 389 (1997); P. J. Dandliker, R. E. Holmlin, J. K. Barton, Science 275, 1465 (1997); S. M. Gasper and G. B. Schuster, J. Am. Chem. Soc. 119, 12762 (1997); P. J. Dandliker, M. E. Nunez, J. K. Barton, Biochemistry 37, 6491 (1998).
5. D. B. Hall, R. E. Holmlin, J. K. Barton, Nature 382, 731 (1996); D. B. Hall and J. K. Barton, J. Am. Chem. Soc. 119, 5045 (1997); M. R. Arkin, E. D. A. Stemp, J. K. Barton, Chem. Biol. 4, 389 (1997); P. J. Dandliker, R. E. Holmlin, J. K. Barton, Science 275, 1465 (1997); S. M. Gasper and G. B. Schuster, J. Am. Chem. Soc. 119, 12762 (1997); P. J. Dandliker, M. E. Nunez, J. K. Barton, Biochemistry 37, 6491 (1998).
6. D. B. Hall, R. E. Holmlin, J. K. Barton, Nature 382, 731 (1996); D. B. Hall and J. K. Barton, J. Am. Chem. Soc. 119, 5045 (1997); M. R. Arkin, E. D. A. Stemp, J. K. Barton, Chem. Biol. 4, 389 (1997); P. J. Dandliker, R. E. Holmlin, J. K. Barton, Science 275, 1465 (1997); S. M. Gasper and G. B. Schuster, J. Am. Chem. Soc. 119, 12762 (1997); P. J. Dandliker, M. E. Nunez, J. K. Barton, Biochemistry 37, 6491 (1998).
7. D. B. Hall, R. E. Holmlin, J. K. Barton, Nature 382, 731 (1996); D. B. Hall and J. K. Barton, J. Am. Chem. Soc. 119, 5045 (1997); M. R. Arkin, E. D. A. Stemp, J. K. Barton, Chem. Biol. 4, 389 (1997); P. J. Dandliker, R. E. Holmlin, J. K. Barton, Science 275, 1465 (1997); S. M. Gasper and G. B. Schuster, J. Am. Chem. Soc. 119, 12762 (1997); P. J. Dandliker, M. E. Nunez, J. K. Barton, Biochemistry 37, 6491 (1998).
8. D. B. Hall, R. E. Holmlin, J. K. Barton, Nature 382, 731 (1996); D. B. Hall and J. K. Barton, J. Am. Chem. Soc. 119, 5045 (1997); M. R. Arkin, E. D. A. Stemp, J. K. Barton, Chem. Biol. 4, 389 (1997); P. J. Dandliker, R. E. Holmlin, J. K. Barton, Science 275, 1465 (1997); S. M. Gasper and G. B. Schuster, J. Am. Chem. Soc. 119, 12762 (1997); P. J. Dandliker, M. E. Nunez, J. K. Barton, Biochemistry 37, 6491 (1998).
9. C. J. Murphy et al., Science 262, 1025 (1993); C. J. Murphy et al., Proc. Natl. Acad. Sci. U.S.A. 91, 5315 (1994); M. R. Arkin et al., Science 273, 475 (1996).
10. C. J. Murphy et al., Science 262, 1025 (1993); C. J. Murphy et al., Proc. Natl. Acad. Sci. U.S.A. 91, 5315 (1994); M. R. Arkin et al., Science 273, 475 (1996).
11. C. J. Murphy et al., Science 262, 1025 (1993); C. J. Murphy et al., Proc. Natl. Acad. Sci. U.S.A. 91, 5315 (1994); M. R. Arkin et al., Science 273, 475 (1996).
12. S. O. Kelley, R. E. Holmlin, E. D. A. Stemp, J. K. Barton, J. Am. Chem. Soc. 119, 9861 (1997).
13. S. O. Kelley and J. K. Barton, Chem. Biol. 8, 413 (1997).
14. S. O. Kelley, N. M. Jackson, M. G. Hill, J. K. Barton, Angew. Chem. Int. Ed., in press.
15. T. J. Meade and J. F. Kayyem, Angew. Chem. Int. Ed. 34, 352 (1995).
16. F. D. Lewis et al., Science 277, 673 (1997); F. D. Lewis and R. L. Letsinger, J. Bioinorg. Chem. 3, 215 (1998).
17. F. D. Lewis et al., Science 277, 673 (1997); F. D. Lewis and R. L. Letsinger, J. Bioinorg. Chem. 3, 215 (1998).
18. E. Meggers, D. Kusch, M. Spichty, U. Wille, B. Giese, Angew. Chem. Int. Ed. 37, 460 (1998).
19. K. Fukui and K. Tanaka, ibid., p. 158.
20. R. A. Marcus and N. Sutin, Biochim. Biophys. Acta 811, 265 (1985).
21. D. C. Ward, E. Reich, L. Stryer, J. Biol. Chem. 244, 1228 (1959).
22. J. R. Barrio, J. A. Secrist, N. J. Leonard, Biochem. Biophys. Res. Commun. 46, 597 (1972); J. A. Secrist, J. R. Barrio, N. J. Leonard, G. Weber, Biochemistry 11, 3499 (1972); R. D. Spencer, G. Weber, G. L. Tolman, J. R. Barrio, N. J. Leonard, Eur. J. Biochem. 45, 425 (1974).
23. J. R. Barrio, J. A. Secrist, N. J. Leonard, Biochem. Biophys. Res. Commun. 46, 597 (1972); J. A. Secrist, J. R. Barrio, N. J. Leonard, G. Weber, Biochemistry 11, 3499 (1972); R. D. Spencer, G. Weber, G. L. Tolman, J. R. Barrio, N. J. Leonard, Eur. J. Biochem. 45, 425 (1974).
24. J. R. Barrio, J. A. Secrist, N. J. Leonard, Biochem. Biophys. Res. Commun. 46, 597 (1972); J. A. Secrist, J. R. Barrio, N. J. Leonard, G. Weber, Biochemistry 11, 3499 (1972); R. D. Spencer, G. Weber, G. L. Tolman, J. R. Barrio, N. J. Leonard, Eur. J. Biochem. 45, 425 (1974).
25. A. Holmen, B. Norden, B. Albinsson, J. Am. Chem. Soc. 119, 3114 (1997); A. Broo, J. Phys. Chem. A 102, 526 (1998).
26. A. Holmen, B. Norden, B. Albinsson, J. Am. Chem. Soc. 119, 3114 (1997); A. Broo, J. Phys. Chem. A 102, 526 (1998).
27. A. Holmen, B. Norden, B. Albinsson, J. Phys. Chem. 98, 13460 (1994).
28. The potentials of G, Z, and 1 are ∼ +1.3 V, +1.0 V, and +1.5 V versus NHE, respectively (5).
29. C. A. M. Seidel, A. Schultz, M. H. M. Sauer, J. Phys. Chem. 100, 5541 (1996); S. Steenken and S. V. Jovanovic, J. Am. Chem. Soc. 119, 617 (1997).
30. C. A. M. Seidel, A. Schultz, M. H. M. Sauer, J. Phys. Chem. 100, 5541 (1996); S. Steenken and S. V. Jovanovic, J. Am. Chem. Soc. 119, 617 (1997).
31. The equally low levels of quenching observed with deoxyinosine triphosphate, deoxyadenosine triphosphate, deoxycytidine triphosphate, and deoxythymidine triphosphate were not sensitive to the redox potentials of these bases (17), and therefore do not appear to be the result of ET.
32. q values would be expected as a result of higher electrostatic repulsions with the nucleotide triphosphate quenchers and an increase in the reduction potential of the alkylated base.
33. ε.
34. ε.
35. -) as +1.5 and +1.4 V versus NHE, respectively.
36. 2 is essentially identical, and (ii) I-dependent reactions were not occurring.
37. ε and G. However, the integration of the decay curves for the G-containing and I-containing duplexes provides a measure of dynamic quenching that is independent of any data-fitting routine. These quenching yields are identical to those observed in steady-state measurements, allowing the calculation of β. An analysis of the fluorescence decay data is available www. sciencemag.org/feature/data/984892.shl as supplementary material.
38. M. Kouchakdijan et al., Biochemistry 30, 1820 (1991).
39. T.M. Norlund et al., ibid. 28, 9095 (1989).
40. 2-T pairs were essentially indistinguishable from A-T pairs.
41. 2-G reaction because of the significant amount of static quenching, and therefore, the dependence of these quenching yields on distance does not solely reflect β. An analysis of the fluorescence decay data is available www.sciencemag.org/ feature/data/984892.shl as supplementary material.
42. W. Saenger, Principles of Nucleic Acid Structure (Springer-Verlag, New York, 1984).
43. S. Woitellier, J. P. Launay, C. W. Spangler, Inorg. Chem. 28, 758 (1989).
44. C. R. Guest, R. A Hochstrasser, L. C. Sowers, D. P. Millar, Biochemistry 30, 3271 (1991).
45. 2 do not participate in efficient ET when incorporated within a mispair and therefore do not interact strongly.
46. ε (which is not H bonded when incorporated across from T) shows only very small amounts of interstrand quenching with G (< 10%) 5.0 Å away.
47. 2/G reaction, as expected for the higher driving force reaction.
48. J. W. Evenson and M. Karplus, Science 262, 1247 (1993); S. Priyadarshy, S. M. Risser, D. N. Beratan, J. Bioinorg. Chem. 3, 196 (1998); J. J. Rejan et al., Chem. Biol. 2, 489 (1995).
49. J. W. Evenson and M. Karplus, Science 262, 1247 (1993); S. Priyadarshy, S. M. Risser, D. N. Beratan, J. Bioinorg. Chem. 3, 196 (1998); J. J. Rejan et al., Chem. Biol. 2, 489 (1995).
50. J. W. Evenson and M. Karplus, Science 262, 1247 (1993); S. Priyadarshy, S. M. Risser, D. N. Beratan, J. Bioinorg. Chem. 3, 196 (1998); J. J. Rejan et al., Chem. Biol. 2, 489 (1995).
51. W. B. Davis, W. A. Svec, M. A. Ratner, M. R. Wasielewski, Nature 396, 60 (1998).
52. 2-Z reaction results from energetic effects.
53. S. Georghiou, T. D Bradrick, A. Philippetis, J. M. Beechem, Biophys. J. 70, 1909 (1996).
54. J. Jortner, M. Bixon, T. Langenbacher, M. E. Michel-Beyerle, Proc. Natl. Acad. Sci. U.S.A. 95, 12759 (1998); A. K. Felts, W. T. Pollard, R. A. Freisner, J. Phys. Chem. 99, 2929 (1995); A. Okada, V. Chernyak, S. Mukamel, idib. 102, 1241 (1998).
55. J. Jortner, M. Bixon, T. Langenbacher, M. E. Michel- Beyerle, Proc. Natl. Acad. Sci. U.S.A. 95, 12759 (1998); A. K. Felts, W. T. Pollard, R. A. Freisner, J. Phys. Chem. 99, 2929 (1995); A. Okada, V. Chernyak, S. Mukamel, idib. 102, 1241 (1998).
56. J. Jortner, M. Bixon, T. Langenbacher, M. E. Michel- Beyerle, Proc. Natl. Acad. Sci. U.S.A. 95, 12759 (1998); A. K. Felts, W. T. Pollard, R. A. Freisner, J. Phys. Chem. 99, 2929 (1995); A. Okada, V. Chernyak, S. Mukamel, idib. 102, 1241 (1998).
57. 3], appropriate amounts of complementary materials were combined at 1:1 stoichiometry and dissolved in 100 mM sodium phosphate (pH 7) to give a final duplex concentration of 100 M. The resulting solutions were heated to 90°C and slowly cooled to ambient temperature over 2 to 3 hours to anneal the duplex. The ultraviolet-visible spectra of the duplex samples were carefully measured to ensure that the absorbance at the excitation wavelength was identical for every sample. Thermal denaturation experiments were performed on a HP8452A diode array spectrophotometer with samples at a duplex concentration of 25 μM in 100 mM phosphate (pH 7). Absorbance was monitored every 2°C with 3-min equilibration times. All duplexes used in these experiments exhibited cooperative thermal denaturation profiles with melting temperatures >25°C with 25 μM duplex and therefore were fully hybridized under the conditions of all fluorescence experiments (100 μM, 20°C).
58. ε. Two data sets were obtained for each sample, one containing >10,000 counts for the determination of decay lifetimes, and another taken over a 120-s time interval to quantitate static quenching. Experiments were otherwise performed under the same conditions as steady-state experiments (100 μM duplex, 100 mM sodium phosphate, pH 7).
59. C. Santhosh and P. C. Mishra, Spectrochim. Acta 47A, 1685 (1991).
60. We thank E. Stemp for assistance with transient absorption experiments, R. Villahermosa for assistance with single-photon counting measurements, and T. Fiebig for discussions and assistance with molecular modeling. In addition, we acknowledge the NIH (grant GM49216 to J.K.B., predoctoral traineeship to S.O.K.) for financial support.