Electric field effects on electron transfer rates in dichromophoric peptides: The effect of helix unfolding

Journal of the American Chemical Society

Volumn 119, Issue 23, 1997, Pages 5277-5285

  Fox, Marye Anne ^a   Galoppini, Elena ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROLINE; PYRENE;

ARTICLE; CIRCULAR DICHROISM; DENATURATION; DNA HELIX; ELECTRON TRANSPORT; PEPTIDE ANALYSIS; PHOTOREACTIVITY; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 0030859221     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja963269k     Document Type: Article

References (54)

1. For a review on the role of an α-helix dipole on protein function and structure see: (a) Hol, W. G. J. Prog. Biophys. Mol. Biol. 1985, 45, 149. (b) Hol, W. G. J.; van Duijnen, P. T.; Berendsen, H. J. C. Nature 1978, 273, 443. (c) Wada, A. Adv. Biophys. 1976, 9, 1. (d) Abraham, R. J.; Hudson, B. D.; Thomas, W. A.; Krohn, A. J. Mol. Graph. 1986, 4, 28.
2. For a review on the role of an α-helix dipole on protein function and structure see: (a) Hol, W. G. J. Prog. Biophys. Mol. Biol. 1985, 45, 149. (b) Hol, W. G. J.; van Duijnen, P. T.; Berendsen, H. J. C. Nature 1978, 273, 443. (c) Wada, A. Adv. Biophys. 1976, 9, 1. (d) Abraham, R. J.; Hudson, B. D.; Thomas, W. A.; Krohn, A. J. Mol. Graph. 1986, 4, 28.
3. For a review on the role of an α-helix dipole on protein function and structure see: (a) Hol, W. G. J. Prog. Biophys. Mol. Biol. 1985, 45, 149. (b) Hol, W. G. J.; van Duijnen, P. T.; Berendsen, H. J. C. Nature 1978, 273, 443. (c) Wada, A. Adv. Biophys. 1976, 9, 1. (d) Abraham, R. J.; Hudson, B. D.; Thomas, W. A.; Krohn, A. J. Mol. Graph. 1986, 4, 28.
4. For a review on the role of an α-helix dipole on protein function and structure see: (a) Hol, W. G. J. Prog. Biophys. Mol. Biol. 1985, 45, 149. (b) Hol, W. G. J.; van Duijnen, P. T.; Berendsen, H. J. C. Nature 1978, 273, 443. (c) Wada, A. Adv. Biophys. 1976, 9, 1. (d) Abraham, R. J.; Hudson, B. D.; Thomas, W. A.; Krohn, A. J. Mol. Graph. 1986, 4, 28.
5. 9 V/m is calculated from vacuum electrostatics.
6. (a) Gosztola, D.; Yamada, H.; Wasielewski, M. R. J. Am. Chem. Soc. 1995, 117, 2041.
7. (b) Brothers, H. M., III; Zhou, J. S.; Kostic, N. M. J. Inorg. Organomet. Polym. 1993, 3, 59.
8. (c) Lockhart, D. J.; Kim, P. S. Science 1992, 257, 947.
9. (d) Franzen, S.; Lao, K.; Boxer, S. G.; Chem. Phys. Lett. 1992, 197, 380.
10. (e) Alegria, G.; Dutton, P. L. Biochim. Biophys. Acta 1991, 234, 1057 and 258.
11. (f) Warshel, A.; Åqvist, J. Annu. Rev. Biophys. Chem. 1991, 20, 267.
12. (g) Boxer, S. G.; Lockhart, D. J.; Franzen, S. In Photochemical Energy Conversion; Norris, J. R., Meisel, D., Eds.; Elsevier: Amsterdam, 1989; p 196.
13. (h) Boxer, S. G.; Goldstein, R. A.; Franzen, S. In Photoinduced Electron Transfer Part B. Experimental Techniques and Medium Effect; Fox, M. A., Chanon, M., Eds.; Elsevier: Amsterdam, 1988; p 163.
14. (i) Abraham, R. J.; Hudson, B. D.; Thomas, W. A.; Krohn, A. J. Mol. Graph. 1986, 4, 28.
15. (a) Galoppini, E.; Fox, M. A. J. Am. Chem. Soc. 1996, 118, 2299. This reference describes the synthesis of 1 and 2 in Supporting Information.
16. 1
17. 4b
18. Short (5-15 amino acids) peptides can adopt rapidly interconverting conformations in solution, and biexponential decays were often observed in studies of electron transfer in peptides: (a) Pispisa, B.; Venanzi, M.; Palleschi, A.; Zanotti, G. J. Phys. Chem. 1996, 100, 6835. (b) Pispisa, B.; Venanzi, M.; Palleschi, A.; Zanotti, G. Macromolecules 1994, 27, 7800. (c) Inai, Y.; Sisido, M.; Imanishi, Y. J. Phvs. Chem. 1991, 95, 3847. (d) Inai, Y.; Sisido, M.; Imanishi, Y. J. Phys. Chem. 1990, 94, 6237. (e) Basu, G.; Kubasik, M.; Anglos, D.; Secor, B.; Kuki, A. J. Am. Chem. Soc. 1990, 112, 9410.
19. Short (5-15 amino acids) peptides can adopt rapidly interconverting conformations in solution, and biexponential decays were often observed in studies of electron transfer in peptides: (a) Pispisa, B.; Venanzi, M.; Palleschi, A.; Zanotti, G. J. Phys. Chem. 1996, 100, 6835. (b) Pispisa, B.; Venanzi, M.; Palleschi, A.; Zanotti, G. Macromolecules 1994, 27, 7800. (c) Inai, Y.; Sisido, M.; Imanishi, Y. J. Phvs. Chem. 1991, 95, 3847. (d) Inai, Y.; Sisido, M.; Imanishi, Y. J. Phys. Chem. 1990, 94, 6237. (e) Basu, G.; Kubasik, M.; Anglos, D.; Secor, B.; Kuki, A. J. Am. Chem. Soc. 1990, 112, 9410.
20. Short (5-15 amino acids) peptides can adopt rapidly interconverting conformations in solution, and biexponential decays were often observed in studies of electron transfer in peptides: (a) Pispisa, B.; Venanzi, M.; Palleschi, A.; Zanotti, G. J. Phys. Chem. 1996, 100, 6835. (b) Pispisa, B.; Venanzi, M.; Palleschi, A.; Zanotti, G. Macromolecules 1994, 27, 7800. (c) Inai, Y.; Sisido, M.; Imanishi, Y. J. Phvs. Chem. 1991, 95, 3847. (d) Inai, Y.; Sisido, M.; Imanishi, Y. J. Phys. Chem. 1990, 94, 6237. (e) Basu, G.; Kubasik, M.; Anglos, D.; Secor, B.; Kuki, A. J. Am. Chem. Soc. 1990, 112, 9410.
21. Short (5-15 amino acids) peptides can adopt rapidly interconverting conformations in solution, and biexponential decays were often observed in studies of electron transfer in peptides: (a) Pispisa, B.; Venanzi, M.; Palleschi, A.; Zanotti, G. J. Phys. Chem. 1996, 100, 6835. (b) Pispisa, B.; Venanzi, M.; Palleschi, A.; Zanotti, G. Macromolecules 1994, 27, 7800. (c) Inai, Y.; Sisido, M.; Imanishi, Y. J. Phvs. Chem. 1991, 95, 3847. (d) Inai, Y.; Sisido, M.; Imanishi, Y. J. Phys. Chem. 1990, 94, 6237. (e) Basu, G.; Kubasik, M.; Anglos, D.; Secor, B.; Kuki, A. J. Am. Chem. Soc. 1990, 112, 9410.
22. Short (5-15 amino acids) peptides can adopt rapidly interconverting conformations in solution, and biexponential decays were often observed in studies of electron transfer in peptides: (a) Pispisa, B.; Venanzi, M.; Palleschi, A.; Zanotti, G. J. Phys. Chem. 1996, 100, 6835. (b) Pispisa, B.; Venanzi, M.; Palleschi, A.; Zanotti, G. Macromolecules 1994, 27, 7800. (c) Inai, Y.; Sisido, M.; Imanishi, Y. J. Phvs. Chem. 1991, 95, 3847. (d) Inai, Y.; Sisido, M.; Imanishi, Y. J. Phys. Chem. 1990, 94, 6237. (e) Basu, G.; Kubasik, M.; Anglos, D.; Secor, B.; Kuki, A. J. Am. Chem. Soc. 1990, 112, 9410.
23. 3c
24. We observed that 1 and 2 rather easily undergo chemical decomposition when heated or exposed to light and air for a few weeks.
25. THF, the solvent used in some of the time-resolved fluorescence measurements, could not be used as the solvent for CD spectra because the UV cutoff of THF is 210 nm.
26. 2 ratio did not change appreciably when the measurements were repeated on the same samples on sequential days (Table 1, entries 4 and 5), implying that the unfolding process had reached equilibrium by the time the measurements were made.
27. 3c For calculations of ∈ in proteins, see also: (a) King, G; Lee, F. S.; Warshel, A. J. Chem. Phys. 1991, 95, 4366. (b) Wipff, G.; Dearing, A.; Weiner, P. K.; Blaney, J. M.; Kollman, P. A. J. Am. Chem. Soc. 1983, 105, 997. (c) Blaney, J. M.; Weiner, P. K.; Dearing, A.; Kollman, P. A.; Jorgensen, E. C.; Oatley, S. J.; Burridge, J. M.; Blake, C. C. F. J. Am. Chem. Soc. 1982, 104, 6424.
28. 3c For calculations of ∈ in proteins, see also: (a) King, G; Lee, F. S.; Warshel, A. J. Chem. Phys. 1991, 95, 4366. (b) Wipff, G.; Dearing, A.; Weiner, P. K.; Blaney, J. M.; Kollman, P. A. J. Am. Chem. Soc. 1983, 105, 997. (c) Blaney, J. M.; Weiner, P. K.; Dearing, A.; Kollman, P. A.; Jorgensen, E. C.; Oatley, S. J.; Burridge, J. M.; Blake, C. C. F. J. Am. Chem. Soc. 1982, 104, 6424.
29. 3c For calculations of ∈ in proteins, see also: (a) King, G; Lee, F. S.; Warshel, A. J. Chem. Phys. 1991, 95, 4366. (b) Wipff, G.; Dearing, A.; Weiner, P. K.; Blaney, J. M.; Kollman, P. A. J. Am. Chem. Soc. 1983, 105, 997. (c) Blaney, J. M.; Weiner, P. K.; Dearing, A.; Kollman, P. A.; Jorgensen, E. C.; Oatley, S. J.; Burridge, J. M.; Blake, C. C. F. J. Am. Chem. Soc. 1982, 104, 6424.
30. n peptides are more rigid than an α-helical peptide, and are valuable rigid spacers. Photoinduced electron transfer across oligoproline peptides (0 < n < 4) has been extensively studied by Isied and co-workers. Their models are structurally very different from 3 and 4, as the donor and acceptor (inorganic complexes) are linked at the two ends of the peptide backbones, which contain only proline units (nonalternating), and the experimental conditions (low pH, water) were selected to favor the trans conformation. Therefore, a direct comparison of the conformation with 3 and 4 with elegant earlier work by the Isied group is not possible. (a) Vassilian, A.; Wishart, J. F.; van Hemelryck, B.; Schwarz, H.; Isied, S. S. J. Am. Chem. Soc. 1990, 112, 7278. (b) Isied, S. S.; Vassilian, A.; Magnuson, R. H.; Schwarz, H. J. Am. Chem. Soc. 1985, 107, 7432. (c) Isied, S. S.; Vassilian, A. J. Am. Chem. Soc. 1984, 106, 1732 and references therein for energy-transfer studies across oligoproline.
31. n peptides are more rigid than an α-helical peptide, and are valuable rigid spacers. Photoinduced electron transfer across oligoproline peptides (0 < n < 4) has been extensively studied by Isied and co-workers. Their models are structurally very different from 3 and 4, as the donor and acceptor (inorganic complexes) are linked at the two ends of the peptide backbones, which contain only proline units (nonalternating), and the experimental conditions (low pH, water) were selected to favor the trans conformation. Therefore, a direct comparison of the conformation with 3 and 4 with elegant earlier work by the Isied group is not possible. (a) Vassilian, A.; Wishart, J. F.; van Hemelryck, B.; Schwarz, H.; Isied, S. S. J. Am. Chem. Soc. 1990, 112, 7278. (b) Isied, S. S.; Vassilian, A.; Magnuson, R. H.; Schwarz, H. J. Am. Chem. Soc. 1985, 107, 7432. (c) Isied, S. S.; Vassilian, A. J. Am. Chem. Soc. 1984, 106, 1732 and references therein for energy-transfer studies across oligoproline.
32. n peptides are more rigid than an α-helical peptide, and are valuable rigid spacers. Photoinduced electron transfer across oligoproline peptides (0 < n < 4) has been extensively studied by Isied and co-workers. Their models are structurally very different from 3 and 4, as the donor and acceptor (inorganic complexes) are linked at the two ends of the peptide backbones, which contain only proline units (nonalternating), and the experimental conditions (low pH, water) were selected to favor the trans conformation. Therefore, a direct comparison of the conformation with 3 and 4 with elegant earlier work by the Isied group is not possible. (a) Vassilian, A.; Wishart, J. F.; van Hemelryck, B.; Schwarz, H.; Isied, S. S. J. Am. Chem. Soc. 1990, 112, 7278. (b) Isied, S. S.; Vassilian, A.; Magnuson, R. H.; Schwarz, H. J. Am. Chem. Soc. 1985, 107, 7432. (c) Isied, S. S.; Vassilian, A. J. Am. Chem. Soc. 1984, 106, 1732 and references therein for energy-transfer studies across oligoproline.
33. n peptides, see: (a) McDonald, D. Q.; Still, W. C. J. Org. Chem. 1996, 61, 1385. (b) Oka, M.; Nakajima, A. Polym. Bull. 1994, 33, 693.
34. n peptides, see: (a) McDonald, D. Q.; Still, W. C. J. Org. Chem. 1996, 61, 1385. (b) Oka, M.; Nakajima, A. Polym. Bull. 1994, 33, 693.
35. n peptides, see: (a) McDonald, D. Q.; Still, W. C. J. Org. Chem. 1996, 61, 1385. (b) Oka, M.; Nakajima, A. Polym. Bull. 1994, 33, 693.
36. n peptides, see: (a) McDonald, D. Q.; Still, W. C. J. Org. Chem. 1996, 61, 1385. (b) Oka, M.; Nakajima, A. Polym. Bull. 1994, 33, 693.
37. n peptides, see: (a) McDonald, D. Q.; Still, W. C. J. Org. Chem. 1996, 61, 1385. (b) Oka, M.; Nakajima, A. Polym. Bull. 1994, 33, 693.
38. n peptides, see: (a) McDonald, D. Q.; Still, W. C. J. Org. Chem. 1996, 61, 1385. (b) Oka, M.; Nakajima, A. Polym. Bull. 1994, 33, 693.
39. For general coupling procedures, see: Bodanszky, M. The Practice of Peptide Synthesis; Springer-Verlag: Berlin, 1994.
40. 13c
41. No difference in the chemical shift of the chromophore protons was observed between the spectra of 1 and 2.
42. The fluorescence quantum yields of 1 and 2 were calculated from the formula reported by Eaton, D. F. Pure Appl. Chem. 1988, 60, 1107. The pyrene fluorescence quantum yield is reported by Birks, J. B. Photophysics of Aromatic Molecules; Wiley & Sons: New York, 1970; p 252.
43. The fluorescence quantum yields of 1 and 2 were calculated from the formula reported by Eaton, D. F. Pure Appl. Chem. 1988, 60, 1107. The pyrene fluorescence quantum yield is reported by Birks, J. B. Photophysics of Aromatic Molecules; Wiley & Sons: New York, 1970; p 252.
44. From the data available, it is not possible to know whether both compounds have identical conformations in more polar solvents in which the peptide backbone is more extended and the exciplex emission is not observed.
45. The transient absorption spectra of 3 and 4 show the presence of pyrene radical anion at 500 nm, in direct analogy to that observed in the transient absorption spectra of 1 and 2.
46. n peptides are in an all-trans conformation. However, these conditions (acidic aqueous solution) could not be employed, because at low pH the N,N-dimethylanilino group would be protonated and could no longer act as an electron donor.
47. We attempted the synthesis of oligopeptides analogous to 1 and 2, but substituted with the conformationally restricted amino acids I and II. (We thank Dr. Mark Minton for assistance in the preparation of these compounds.) (Matrix Presented) Unfortunately, we were unsuccessful in incorporating I or II into an Ala-Aib backbone, because of solubility problems and/or the difficulty of coupling bulky α,α-disubstituted amino acids. The latter is a problem which is well documented in the literature: Kaminski, Z.; Leplawy, M. T.; Olma, A.; Redlinski, A. In Peptides 1980, Proceedings of the European Peptide Symposium; Brunfeldt, K., Ed.; Scriptor: Copenhagen, 1981; Vol. 16, p 201.
48. Von Arx, E.; Faupel, M.; Brugger, M. J. Chromatogr. 1976, 120, 224.
49. O'Connor, D. V.; Phillips, D. Time Correlated Single Photon Counting; Academic Press: New York, 1984; Chapter 4.
50. The synthesis of Boc-dmaPhe-OH is described by Bergel, F.; Stock, J. A. J. Chem. Soc. 1959, 90.
51. Lott, R. S.; Chauhan, V. S.; Stammer, C. H. J. Chem. Soc., Chem. Commun. 1979, 495.
52. The synthesis of H-pyrAla-OMe was adapted from (a) Schmidt, U.; Lieberknecht, A.; Wild, J. Synthesis 1988, 159. (b) Schmidt, U.; Lieberknecht, A.; Wild, J. Synthesis 1984, 53. (c) Burk, M. J; Feaster, J. E.; Nugent, W. A.; Harlow, R. L. J. Am. Chem. Soc. 1993, 115, 10125.
53. The synthesis of H-pyrAla-OMe was adapted from (a) Schmidt, U.; Lieberknecht, A.; Wild, J. Synthesis 1988, 159. (b) Schmidt, U.; Lieberknecht, A.; Wild, J. Synthesis 1984, 53. (c) Burk, M. J; Feaster, J. E.; Nugent, W. A.; Harlow, R. L. J. Am. Chem. Soc. 1993, 115, 10125.
54. The synthesis of H-pyrAla-OMe was adapted from (a) Schmidt, U.; Lieberknecht, A.; Wild, J. Synthesis 1988, 159. (b) Schmidt, U.; Lieberknecht, A.; Wild, J. Synthesis 1984, 53. (c) Burk, M. J; Feaster, J. E.; Nugent, W. A.; Harlow, R. L. J. Am. Chem. Soc. 1993, 115, 10125.