Fast initiation of peptide and protein folding processes

European Journal of Organic Chemistry

Volumn , Issue 14, 2001, Pages 2605-2621

  Volk, Martin ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Amino acids; Helical structures; Kinetics; Photochemistry; Protein folding

Indexed keywords

PEPTIDE; PROTEIN;

CHEMICAL PROCEDURES; PEPTIDE SYNTHESIS; PHOTOCHEMISTRY; PROTEIN FOLDING; PROTEIN STRUCTURE; SHORT SURVEY; STRUCTURE ANALYSIS; TECHNIQUE;

EID: 0034940711     PISSN: 1434193X     EISSN: None     Source Type: Journal    
DOI: 10.1002/1099-0690(200107)2001:14<2605::aid-ejoc2605>3.0.co;2-u     Document Type: Short Survey

References (171)

1. C. B. Anfinsen, Science 1973, 181, 223-230.
2. [2a] A. Liwo, J. Lee, D. R. Ripoll, J. Pillardy, H. A. Scheraga, Proc. Natl. Acad. Sci. USA 1999, 96, 5482-5485.
3. [2b] M. Vasquez, G. Nemethy, H. A. Scheraga, Chem. Rev. 1994, 94, 2183-2239.
4. [3a] W. F. DeGrado, Science 1997, 278, 80-81.
5. [3b] B. I. Dahiyat, S. L. Mayo, Science 1997, 278, 82-87.
6. [3c] S. E. Radford, C. M. Dobson, Cell 1999, 97, 291-298.
7. [3d] T. Kortemme, M. Ramírez-Alvarado, L. Serrano, Science 1998, 281, 253-256.
8. [3e] P. B. Harbury, J. J. Plecs, B. Tidor, T. Alber, P. S. Kim, Science 1998, 282, 1462-1467.
9. C. Levinthal, J. Chim. Phys. Phys.-Chim. Biol. 1968, 65, 44-45.
10. [5a] O. B. Ptitsyn, J. Protein Chem. 1987, 6, 273-293.
11. [5b] O. B. Ptitsyn, Protein Eng. 1994, 7, 593-596.
12. [5c] M. Karplus, D. L. Weaver, Nature 1976, 260, 404-406.
13. [5d] M. Karplus, D. L. Weaver, Prot. Sci. 1994, 3, 650-668.
14. P. S. Kim, R. L. Baldwin, Annu. Rev. Biochem. 1982, 51, 459-489.
15. P. S. Kim, R. L. Baldwin, Annu. Rev. Biochem. 1990, 59, 631-660.
16. K. A. Dill, Biochemistry 1985, 24, 1501-1509.
17. K. A. Dill, S. Bromberg, K. Yue, K. M. Fiebig, D. P. Yee, P. D. Thomas, H. S. Chan, Protein Sci. 1995, 4, 561-602.
18. [10a] T. R. Sosnick, L. Mayne, S. W. Englander, Proteins 1996, 24, 413-426.
19. [10b] T. R. Sosnick, S. Jackson, R. R. Wilk, S. W. Englander, W. F. DeGrado, Proteins 1996, 24, 427-432.
20. [11a] D. E. Otzen, L. S. Itzhaki, N. F. ElMasry, S. E. Jackson, A. R. Fersht, Proc. Natl. Acad. Sci. USA 1994, 91, 10422-10425.
21. [11b] V. I. Abkevich, A. M. Gutin, E. I. Shakhnovich, Biochemistry 1994, 33, 10026-10036.
22. [11c] Z. Guo, D. Thirumalai, Biopolymers 1995, 36, 83-102.
23. A. R. Fersht, Curr. Opin. Struct. Biol. 1997, 7, 3-9.
24. [13a] T. E. Creighton, D. P., J. Mol. Biol. 1984, 179, 497-526.
25. [13b] J. S. Weissman, P. S. Kim, Science 1991, 253, 1386-1393.
26. J. S. Weissman, P. S. Kim, Cell 1992, 71, 841-851.
27. X. Zhu, Y. Ohta, F. Jordan, M. Inouye, Nature 1989, 339, 483-484.
28. [16a] K.-M. Pan, M. Baldwin, J. Nguyen, M. Gasset, A. Serban, D. Groth, I. Mehlhorn, Z. Huang, R. J. Fletterick, F. E. Cohen, S. B. Prusiner, Proc. Natl. Acad. Sci. USA 1993, 90, 10962-10966.
29. [16b] P. M. Harrison, P. Bamborough, V. Daggett, S. B. Prusiner, F. E. Cohen, Curr. Opin. Struct. Biol. 1997, 7, 53-59.
30. [16c] S. B. Prusiner, Proc. Natl. Acad. Sci. USA 1998, 95, 13363-13383.
31. [16d] H. Mihara, Y. Takahashi, Curr. Opin. Struct. Biol. 1997, 7, 501-508.
32. [17a] R. L. Baldwin, G. D. Rose, Trends Biochem. Sci. 1999, 24, 26-33.
33. [17b] R. L. Baldwin, G. D. Rose, Trends Biochem. Sci. 1999, 24, 77-83.
34. [17c] S.-R. Yeh, D. L. Rousseau, Nat. Struct. Biol. 2000, 7, 443-445.
35. [18a] O. B. Ptitsyn, Adv. Protein Chem. 1995, 47, 83-229.
36. [18b] M. Bycroft, A. Matouschek, J. T. Kellis Jr., L. Serrano, A. R. Fersht, Nature 1990, 346, 488-490.
37. [18c] W. A. Houry, D. M. Rothwarf, H. A. Scheraga, Nat. Struct. Biol. 1995, 2, 495-503.
38. [18d] G. A. Elöve, A. F. Chaffotte, H. Roder, M. E. Goldberg, Biochemistry 1992, 31, 6876-6883.
39. [18e] P. A. Jennines, P. E. Wright, Science 1993, 262, 892-895.
40. [18f] S. E. Radford, C. M. Dobson, P. A. Evans, Nature 1992, 358, 302-307.
41. B. H. Zimm, J. K. Bragg, J. Chem. Phys. 1959, 31, 526-535.
42. C. L. Brooks, J. Phys. Chem. 1996, 100, 2546-2549.
43. [21a] J. Tirado-Rives, W. L. Jorgensen, Biochemistry 1991, 30, 3864-3871.
44. [21b] K. V. Soman, A. Karimi, D. A. Case, Biopolymers 1993, 33, 1567-1580.
45. [21c] T. Lazaridis, M. Karplus, Science 1997, 278, 1928-1931.
46. [21d] Y. Duan, L. Wang, P. A. Kollman, Proc. Natl. Acad. Sci. USA 1998, 95, 9897-9902.
47. [21e] Y. Duan, A. Kollman, Science 1998, 282, 740-744.
48. M. C. R. Shastry, S. D. Luck, H. Roder, Biophys. J. 1998, 74, 2714-2721.
49. S. Takahashi, S.-R. Yeh, T. K. Das, C.-K. Chan, D. S. Gottfried, D. L. Rousseau, Nat. Struct. Biol. 1997, 4, 44-50.
50. C.-K. Chan, Y. Hu, S. Takahashi, D. L. Rousseau, W. A. Eaton, J. Hofrichter, Proc. Natl. Acad. Sci. USA 1997, 94, 1779-1784.
51. C. M. Jones, E. R. Henry, Y. Hu, C. K. Chan, S. D. Luck, A. Bhuyan, H. Roder, J. Hofrichter, W. A. Eaton, Proc. Natl. Acad. Sci. USA 1993, 90, 11860-11864.
52. T. Pascher, J. P. Chesick, J. R. Winkler, H. B. Gray, Science 1996, 271, 1558-1560.
53. P. Wittung-Stafshede, H. B. Gray, J. R. Winkler, J. Am. Chem. Soc. 1997, 119, 9562-9563.
54. W. A. Eaton, V. Muñoz, P. A. Thompson, E. R. Henry, J. Hofrichter, Acc. Chem. Res. 1998, 31, 745-753.
55. J. R. Telford, P. Wittung-Stafshede, H. B. Gray, J. R. Winkler, Acc. Chem. Res. 1998, 31, 755-763.
56. E. Chen, M. J. Wood, A. L. Fink, D. S. Kliger, Biochemistry 1998, 37, 5589-5598.
57. P. Wittung-Stafshede, J. C. Lee, J. R. Winkler, H. B. Gray, Proc. Natl. Acad. Sci. USA 1999, 96, 6587-6590.
58. J. R. Telford, F. A. Tezcan, H. B. Gray, J. R. Winkler, Biochemistry 1999, 38, 1944-1949.
59. S. J. Hagen, J. Hofrichter, A. Szabo, W. A. Eation, Proc. Natl. Acad. Sci. USA 1996, 93, 11615-11617.
60. M. R. Eftink, Biophys. J. 1994, 66, 482-501.
61. [35a] B. Nölting, R. Golbik, A. R. Fersht, Proc. Natl. Acad. Sci. USA 1995, 92, 10668-10672.
62. [35b] B. Nölting, R. Golbik, J. L. Neira, A. S. Soler-Gonzalez, G. Schreiber, A. R. Fersht, Proc. Natl. Acad. Sci. USA 1997, 94, 826-830.
63. M. Jamin, S.-R. Yeh, D. L. Rousseau, R. L. Baldwin, J. Mol. Biol. 1999, 292, 731-740.
64. R. M. Ballew, J. Sabelko, M. Gruebele, Nat. Struct. Biol. 1996, 3, 923-926.
65. J. Sabelko, J. Ervin, M. Gruebele, Proc. Natl. Acad. Sci. USA 1999, 95, 6031-6036.
66. M. P. Lillo, J. M. Beechem, Biochemistry 1997, 36, 11261-11272.
67. C.-K. Chan, J. Hofrichter, W. A. Eaton, Science 1996, 274, 628-629.
68. R. M. Ballew, J. Sabelko, M. Gruebele, Proc. Natl. Acad. Sci. USA 1996, 93, 5759-5764.
69. M. C. R. Shastry, H. Roder, Nat. Struct. Biol. 1998, 5, 385-392.
70. M. C. R. Shastry, J. M. Sauder, H. Roder, Acc. Chem. Res. 1998, 31, 717-725.
71. M. Gruebele, J. Sabelko, R. Ballew, J. Ervin, Acc. Chem. Res. 1998, 31, 699-707.
72. S.-R. Yeh, D. L. Rousseau, J. Biol. Chem. 1999, 274, 17853-17859.
73. J. G. Lyubovitsky, J. R. Telford, J. R. Winkler, H. B. Gray, J. Inorg. Biochem. 1999, 74, 216-216.
74. V. Muñoz, P. A. Thompson, J. Hofrichter, W. A. Eaton, Nature 1997, 390, 196-199.
75. [48a] P. A. Thompson, W. A. Eaton, J. Hofrichter, Biochemistry 1997, 36, 9200-9210.
76. [48b] P. A. Thompson, V. Muñoz, G. S. Jas, E. R. Henry, W. A. Eaton, J. Hofrichter, J. Phys. Chem. B 2000, 104, 378-389.
77. [49a] T. Mjyazawa, E. R. Blout, J. Am. Chem. Soc. 1961, 83, 712-719.
78. [49b] T. Miyazawa in Poly-α-amino acids - Protein models for conformational studies (Ed.: G. D. Fasman), Arnold, London, 1967, pp. 69-103.
79. [49c] S. Krimm, J. Bandekar, Adv. Protein Chem. 1986, 38, 181-364.
80. [49d] H. Susi, D. M. Byler, Methods Enzymol. 1986, 130, 290-311.
81. [49e] W. K. Surewicz, H. H. Mantsch, Biochim. Biophys. Acta 1988, 952, 115-130.
82. [49f] W. K. Surewicz, H. H. Mantsch, D. Chapman, Biochemistry 1993, 32, 389-394.
83. [49g] J. L. R. Arrondo, A. Muga, J. Castresana, F. M. Goñi, Prog. Biophys. Molec. Biol. 1993, 59, 23-56.
84. T. Miyazawa, J. Chem. Phys. 1960, 32, 1647-1652.
85. 2O absorption in the amide I region.
86. S. Williams, T. P. Causgrove, R. Gilmanshin, K. S. Fang, R. H. Callender, W. H. Woodruff, R. B. Dyer, Biochemistry 1996, 35, 691-697.
87. S. M. Decatur, J. Antonic, J. Am. Chem. Soc. 1999, 121, 11914-11915.
88. C. M. Phillips, Y. Mizutani, R. M. Hochstrasser, Proc. Natl. Acad. Sci. USA 1995, 92, 7292-7296.
89. [55a] R. Gilmanshin, S. Williams, R. H. Callender, W. H. Woodruff, R. B. Dyer, Proc. Natl. Acad. Sci. USA 1997, 94, 3709-3713.
90. [55b] R. Gilmanshin, S. Williams, R. H. Callender, W. H. Woodruff, R. B. Dyer, Biochemistry 1997, 36, 15006-15012.
91. R. B. Dyer, F. Gai, W. H. Woodruff, R. Gilmanshin, R. H. Callender, Acc. Chem. Res. 1998, 31, 709-716.
92. J. Wang, M. A. El-Sayed, Biophys. J. 1999, 76, 2777-2783.
93. D. T. Leeson, F. Gai, H. M. Rodriguez, L. M. Gregoret, R. B. Dyer, Proc. Natl. Acad. Sci. USA 2000, 97, 2527-2532.
94. M. Volk, Y. Kholodenko, H. S. M. Lu, E. A. Gooding, W. F. DeGrado, R. M. Hochstrasser, J. Phys. Chem. B 1997, 101, 8607-8616.
95. T. Elsaesser, J. G. Fujimoto, D. A. Wiersma, W. Zinth (Eds.), Ultrafast Phenomena XI, Springer-Verlag, Berlin, 1998.
96. Circular Dichroism, the Conformational Analysis of Biomolecules (Ed.: G. Fasman), Plenum Publishers, New York, 1996.
97. E. Chen, P. Wittung-Stafshede, D. S. Kliger, J. Am. Chem. Soc. 1999, 121, 3811-3817.
98. Z. Chi, X. G. Chen, J. S. W. Holtz, S. A. Asher, Biochemistry 1998, 37, 2854-2864.
99. [64a] S.-R. Yeh, S. Takahashi, B. Fan, D. L. Rousseau, Nat. Struct. Biol. 1997, 4, 51-56.
100. [64b] S.-R. Yeh, S. Han, D. L. Rousseau, Acc. Chem. Res. 1998, 31, 727-736.
101. S.-R. Yeh, D. L. Rousseau, Nat. Struct. Biol. 1998, 5, 222-228.
102. I. K. Lednev, A. S. Karnoup, M. C. Sparrow, S. A. Asher, J. Am. Chem. Soc. 1999, 121, 4076-4077.
103. E. Chen, R. A. Goldbeck, D. S. Kliger, Annu. Rev. Biophys. Biomol. Struct. 1997, 26, 327-355.
104. R. A. Goldbeck, Y. G. Thomas, E. Chen, R. M. Esquerra, D. S. Kliger, Proc. Natl. Acad. Sci. USA 1999, 96, 2782-2787.
105. V. M. Grigoryants, A. V. Veselov, C. P. Scholes, Biophys. J. 2000, 78, 2702-2708.
106. L. Pollack, M. W. Tate, N. C. Darnton, J. B. Knight, S. M. Gruner, W. A. Eaton, R. H. Austin, Proc. Natl. Acad. Sci. USA 1999, 96, 10115-10117.
107. S. Abbruzzetti, E. Crema, L. Masino, A. Vecli, C. Viappiani, J. R. Small, L. J. Libertini, E. W. Small, Biophys. J. 2000, 78, 405-415.
108. W. A. Eaton, P. A. Thompson, C. K. Chan, S. J. Hagen, J. Hofrichter, Structure 1996, 4, 1133-1139.
109. R. H. Callender, R. B. Dyer, R. Gilmanshin, W. H. Woodruff, Annu. Rev. Phys. Chem. 1998, 49, 173-202.
110. M. Gruebele, Annu. Rev. Phys. Chem. 1999, 50, 485-516.
111. D. J. Brockwell, D. A. Smith, S. E. Radford, Curr. Opin. Struct. Biol. 2000, 10, 16-25.
112. [76a] G. Schwarz, J. Seelig, Biopolymers 1968, 6, 1263-1277.
113. [76b] G. G. Hammes, P. B. Roberts, J. Am. Chem. Soc. 1969, 91, 1812-1816.
114. [76c] B. Gruenewald, C. U. Nicola, A. Lustig, G. Schwarz, H. Klump, Biophys. Chem. 1979, 9, 137-147.
115. B. Nölting, M. Jiang, S. G. Sligar, J. Am. Chem. Soc. 1993, 115, 9879-9882.
116. [78a] O. Bieri, J. Wirz, B. Hellrung, M. Schutkowski, M. Drewello, T. Kiefhaber, Proc. Natl. Acad. Sci. USA 1999, 96, 9597-9601.
117. [78b] L. J. Lapidus, W. A. Eaton, J. Hofrichter, Proc. Natl. Acad. Sci. USA 2000, 97, 7220-7225.
118. S. Akiyama, S. Takahashi, K. Ishimori, I. Morishima, Nat. Struct. Biol. 2000, 7, 514-520.
119. S. J. Hagen, J. Hofrichter, W. A. Eaton, J. Phys. Chem. B 1997, 101, 2352-2365.
120. P. Wittung-Stafshede, B. G. Malmström, J. R. Winkler, H. B. Gray, J. Phys. Chem. A 1998, 102, 5599-5601.
121. J. H. Clark, S. L. Shapiro, A. J. Campillo, K. R. Winn, J. Am. Chem. Soc. 1979, 101, 746-748.
122. E. Pines, D. Huppert, M. Gutman, N. Nachliel, M. Fishman, J. Phys. Chem. 1986, 90, 6366-6370.
123. M. Gutman, Methods Enzymol. 1986, 127, 522-538.
124. [85a] P. L. Privalov, Annu. Rev. Biophys. Biophys. Chem. 1989, 18, 47-69.
125. [85b] P. L. Privalov, CRC Crit. Rev. Biochem. 1990, 25, 281-305.
126. B. H. Zimm, P. Doty, K. Iso, Proc. Natl. Acad. Sci. USA 1959, 45, 1601-1607.
127. S. Marqusee, R. L. Baldwin, Proc. Natl. Acad. Sci. USA 1987, 84, 8898-8902.
128. H. S. M. Lu, M. Volk, Y. Kholodenko, E. Gooding, R. M. H. Hochstrasser, W. F. DeGrado, J. Am. Chem. Soc. 1997, 119, 7173-7180.
129. G. Czerlinski, M. Eigen, Z. Elektrochem. 1959, 63, 652-661.
130. M. Eigen, L. DeMaeyer, in Technique of Organic Chemistry, vol. VIII, 2 (Eds.: S. L. Friess, E. S. Lewis, A. Weissberger), Interscience, New York, 1963, pp. 895-1054.
131. H. Staerk, G. Czerlinski, Nature 1965, 205, 63-64.
132. D. H. Turner, G. W. Flynn, N. Sutin, J. V. Beitz, J. Am. Chem. Soc. 1972, 94, 1554-1559.
133. T. Lian, B. Locke, Y. Kholodenko, R. M. Hochstrasser, J. Phys. Chem. 1994, 98, 11648-11656.
134. In Φ-value analysis, the effect of single-site mutations on the free energy of the transition state of a folding reaction is quantified by comparing the effect of the mutation on the folding kinetics with its effect on the equilibrium free energy difference between folded and unfolded state. The Φ-value thus determined allows conclusions on structural changes occurring in the transition state: A. R. Fersht, A. Matouschek, L. Serrano, J. Mol. Biol. 1992, 224, 771-782.
135. Apomyoglobin denotes myoglobin without the heme cofactor.
136. S. V. Evans, G. D. Brayer, J. Biol. Chem. 1988, 263, 4263-4268.
137. J. Sabelko, J. Ervin, M. Gruebele, J. Phys. Chem. B 1998, 102, 1806-1819.
138. R. Gilmanshin, R. H. Callender, R. B. Dyer, Nat. Struct. Biol. 1998, 5, 363-365.
139. S. Lifson, A. Roig, J. Chem. Phys. 1961, 34, 1963-1974.
140. Results for α-helix folding after fast dilution of denaturants indicating helix nucleation on the millisecond timescale have recently been reported, thus raising doubts about the conclusion of sub-microsecond nucleation from temperature-jump experiments: D. T. Clarke, A. J. Doig, B. J. Stapley, G. R. Jones, Proc. Natl. Acad. Sci. USA 1999, 96, 7232-7237.
141. V. Muñoz, E. R. Henry, J. Hofrichter, W. A. Eaton, Proc. Natl. Acad. Sci. USA 1998, 95, 5872-5879.
142. T. W. Scott, S. N. Liu, J. Phys. Chem. 1989, 93, 1393-1396.
143. N. P. Ernsting, Chem. Phys. Lett. 1990, 166, 221-226.
144. N. A. Borisevich, N. A. Lysak, S. V. Melnichuk, S. A. Tikhomirov, G. B. Tolstorozhev, in Ultrafast Phenomena in Spectroscopy, vol. 49 (Eds.: E. Klose, B. Wilhelmi), Springer-Verlag, Berlin, Heidelberg, 1990, pp. 276-281.
145. Y. Hirata, Y. Niga, T. Okada, Chem. Phys. Lett. 1994, 221, 283-288.
146. S. Marqusee, V. H. Robbins, R. L. Baldwin, Proc. Natl. Acad. Sci. USA 1989, 86, 5286-5290.
147. [107a] F. C. Thyrion, J. Phys. Chem. 1973, 77, 1478-1482.
148. [107b] G. H. Morine, R. R. Kuntz, Chem. Phys. Lett. 1979, 67, 552-554.
149. [107c] R. R. Lembke, L. V. Natarajan, R. R. Kuntz, J. Photochem. 1983, 21, 814-823.
150. The anisotropy r(t) at time t is defined as r(t) = A∥(t)-A⊥(t)/ A∥(t)+2A⊥(t) where A∥(t) and A⊥(t) denote the transient absorbance at time t measured with parallel and perpendicular polarisation of pump and probe light, respectively.
151. [109a] T. J. Chuang, K. B. Eisenthal, J. Chem. Phys. 1972, 57, 5094-5097.
152. [109b] G. G. Belford, R. L. Belford, G. Weber, Proc. Natl. Acad. Sci. USA 1972, 69, 1392-1393.
153. F. Perrin, J. Phys. Radium 1934, 5, 497.
154. [111a] I. Munro, I. Pecht, L. Stryer, Proc. Natl. Acad. Sci. USA 1979, 76, 56-60.
155. [111b] J. B. A. Ross, K. W. Rousslang, L. Brand, Biochemistry 1981, 20, 4361-4369.
156. [111c] C. D. Tran, G. S. Beddard, A. D. Osborne, Biochim. Biophys. Acta 1982, 709, 256-264.
157. 2O signal are not known with sufficient accuracy.
158. A. Plonka in Time Dependent Reactivity of Species in Condensed Media (Eds.: G. Berthier, M. J. S. Dewar, H. Fischer, K. Fukui, G. G. Hall, H. Hartmann, H. H. Jaffe, J. Jortner, W. Kutzelnigg, K. Ruedenberg, J. Tomasi), Springer-Verlag, Berlin, 1988, p. 151.
159. -1.
160. R. Metzler, J. Klafter, J. Jortner, M. Volk, Chem. Phys. Lett. 1998, 293, 477-484.
161. [78]). In these experiments, the triplet state of a chromophore at one peptide end is quenched upon contact formation with a chromophore attached to the opposite end of a flexible peptide. This probe of contact formation dynamics is strongly analogous to the radical recombination upon contact formation investigated here. In contrast to the observed extremely nonexponential radical recombination, however, exponential triplet decays (on the nanosecond timescale) were found in all cases. These different results can be explained by the different initial peptide conformations encountered in the two sets of experiments. In the triplet transfer experiments, the variety of peptide conformations at the moment of excitation corresponds to the equilibrium distribution, and contact formation is achieved by equilibrium fluctuations with a time-independent probability. In the radical recombination experiments, on the other hand, immediately after disulfide bond photolysis, all peptides are in conformations with small end-to-end distances: i.e., the distribution is far from equilibrium. Relaxation towards equilibrium results in a fast increase of the mean end-to-end distance and so the probability of contact formation decreases with time, as discussed in the text. For the triplet transfer experiments, moreover, peptides without internal structure were used, avoiding any internal peptide process apart from polypeptide chain diffusion. For the peptides used in the disulfide photolysis study, in contrast, additional processes such as α-helix nucleation and growth are expected to contribute to the internal peptide dynamics on longer timescales.
162. Other methods will need to be developed for incorporation of the cross-linker into larger proteins.
163. The stability of peptide 5 during repeated photolysis was checked by absorbance spectroscopy and HPLC and no indications for sample degradation were observed even after extensive measurements. In particular, no cross-linking between different peptides (nongeminate recombination) occurred under the conditions employed.
164. Recombination of thiyl radical pairs could be prevented by the addition of external radical quenchers in sufficient concentration. However, such an approach results in irreversible bond dissociation, precluding multiple excitation and thus ruling out the extensive data averaging needed for most of the currently available detection techniques.
165. G. Jeschke, M. Wakasa, Y. Sakaguchi, H. Hayashi, J. Phys. Chem. 1994, 98, 4069-4075.
166. T. Autrey, C. Devadoss, B. Sauerwein, J. A. Franz, G. B. Schuster, J. Phys. Chem. 1995, 99, 869-871.
167. J. R. Kumita, O. S. Smart, G. A. Woolley, Proc. Natl. Acad. Sci. USA 2000, 97, 3803-3808.
168. R. Behrendt, C. Renner, M. Schenk, F. Wang, J. Wachtveitl, D. Oesterhelt, L. Moroder, Angew. Chem. Int. Ed. 1999, 38, 2771-2774.
169. L. Ulysse, J. Cubillos, J. Chmielewski, J. Am. Chem. Soc. 1995, 117, 8466-8467.
170. J. Wachtveitl, T. Nagele, B. Puell, W. Zinth, M. Krüger, S. Rudolph-Böhner, D. Oesterhelt, L. Moroder, J. Photochem. Photobiol. A 1997, 105, 283-288.
171. R. Cerpa, F. E. Cohen, I. D. Kuntz, Folding Design 1996, 1, 91-101.