A 2,3'-substituted biphenyl-based amino acid facilitates the formation of a monomeric β-hairpin-like structure in aqueous solution at elevated temperature

Journal of the American Chemical Society

Volumn 118, Issue 25, 1996, Pages 5836-5845

  Nesloney, Carey L ^a   Kelly, Jeffery W ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID DERIVATIVE; BIPHENYL DERIVATIVE; SYNTHETIC PEPTIDE;

ARTICLE; CIRCULAR DICHROISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN FOLDING; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION;

EID: 0030037714     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja952472x     Document Type: Article

References (121)

1. (a) Finkelstein, A. V. Proteins: Struct., Funct. Genet. 1991, 9, 23-27.
2. (b) Liu, Z.-P.; Rizo, J.; Gierasch, L. M. Biochemistry 1994, 33, 134-142.
3. (c) Dyson, H. J.; Sayre, J. R.; Merutka, G.; Shin, H. C.; Lerner, R. A.; Wright, P. E. J. Mol. Biol. 1992, 226, 819-835.
4. (d) Dyson, H. J.; Merutka, G.; Waltho, J. P.; Lerner, R. A.; Wright, P. E. J. Mol. Biol. 1992, 226, 795-817.
5. (e) Kemp, D. S. Trends Biotechnol. 1990, 8, 249-255.
6. (f) Minor, D. L., Jr.; Kim, P. S. Nature 1994, 367, 660-663.
7. (g) Minor, D. L., Jr.; Kim, P. S. Nature 1994, 371, 264-267.
8. (h) Smith, C. K.; Withka, J. M.; Regan, L. Biochemistry 1994, 33, 5510-5517.
9. (i) Smith, C. K.; Regan, L. Science 1995, 270, 980-982.
10. (j) Kim, C. A.; Berg, J. M. Nature 1993, 362, 267-270.
11. (k) Erickson, B. W., Daniels, S. B., Higgins, M. L., Reddy, P. A. Advances in Gene Technology: Protein Engineering and Production; Oxford IRL Press: New York, 1988; pp 240.
12. (l) Varley, P.; Gronenborn, A. M.; Christensen, H.; Wingfield, P. T.; Pain, R. H.; Clore, G. M. Science 1993, 260, 1110-1113.
13. (m) Tsang, K. Y.; Díaz, H.; Graciani, N.; Kelly, J. W. J. Am. Chem. Soc. 1994, 116, 3988-4005.
14. (n) Yan, Y.; Erickson, B. W. Protein Sci. 1994, 3, 1069-1073.
15. (o) Blanco, F. J.; Rivas, G.; Serrano, L. Struct. Biol. 1994, 1, 584-590.
16. (p) Fedorov, A. N.; Dolgikh, D. A.; Chemeris, V. V.; Chernov, B. K.; Finklestein, A. V.; Schulga, A. A.; Alakhov, Y. B.; Kirpichnikov, M. P.; Ptitsyn, O. B. J. Mol. Biol. 1992, 225, 927-931.
17. (q) Zhang, S.; Holmes, T.; Lockshin, C.; Rich, A. Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 3334-3338.
18. (r) Hecht, M. H. Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 8729-8730.
19. (s) Quinn, T. P.; Tweedy, N. B.; Williams, R. W.; Richardson, J. S.; Richardson, D. C. Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 8747-8751.
20. (a) Creighton, T. E. Proteins: Structure and Molecular Properties, 2nd ed.; W. H. Freeman and Co.: New York, 1993.
21. (b) Mattice, W. L. Annu. Rev. Biophys. Biophys. Chem. 1989, 18, 93-111.
22. (c) Dyson, H. J.; Wright, P. E. Annu. Rev. Biophys. Biophys. Chem. 1991, 20, 519-538.
23. (d) Yapa, K.; Weaver, D. L.; Karplus, M. Proteins: Struct., Funct. Genet. 1992, 12, 237-265.
24. (a) Maeda, H.; Ooi, K. Biopolymers 1981, 20, 1549-1563.
25. (b) Maeda, H.; Gatto, Y.; Ikeda, S. Macromolecules 1984, 17, 2031-2038.
26. (c) Maeda, H. Bull. Chem. Soc. Jpn. 1987, 60, 3438-3440.
27. (d) Brack, A.; Orgel, L. E. Nature 1975, 250, 383-387.
28. (e) Brack, A,; Caille, A. Int. J. Peptide Protein Res. 1978, 11, 128-139.
29. (f) Brack, A.; Spach, G. J. Am. Chem. Soc. 1981, 103, 6319-6323.
30. (g) Johnson, B. J. J. Pharm. Sci. 1974, 63, 313-327.
31. (h) Mattice, W. L.; Lee, E.; Scheraga, H. A. Can. J. Chem. 1985, 63, 140-146.
32. (i) Rippon, W. B.; Chen, H. H.; Walton, A. G. J. Mol Biol. 1973, 75, 369-375.
33. (j) Seipke, G.; Arfmann, H. A.; Wagner, K. G. Biopolymers 1974, 13, 1621-1633.
34. (k) Osterman, D. G.; Kaiser, E. T. J. Cell. Biochem. 1985, 29, 57-72.
35. (l) DeGrado, W. F.; Lear, J. D. J. Am. Chem. Soc. 1985, 107, 7684-7689.
36. (m) Rajasekharan Pillai, V. N.; Mütter, M. Acc. Chem. Res. 1981, 14, 122-130.
37. (n) Choo, D. W.; Schneider, J. P.; Graciani, N. R.; Kelly, J. W. Macromolecules 1996, 29, 355-366.
38. (o) Zhang, S.; Lockshin, C.; Cook, R.; Rich, A. Biopolymers 1994, 34, 663-672.
39. (p) Krantz, D. D.; Zidovetzki, R.; Kagan, B. L.; Zipursky, S. L. J. Biol. Chem. 1991, 266, 16801-16807.
40. (q) Ghadiri, M. R.; Granja, J. R.; Milligan, R. A.; McRee, D. E.; Khazanovich, N. Nature 1993, 366, 324-327.
41. (r) Ghadiri, M. R.; Granja, J. R.; Buehler, L. K. Nature 1994, 369, 301-304.
42. (s) Graciani, N. R.; Tsang, K. Y.; McCutchen, S. L.; Kelly, J. W. Bioorg. Med. Chem. 1994, 2, 999-1006.
43. (t) Sun, X.; Lorenzi, G. P. Helv. Chim. Acta 1994, 77, 1520-1526.
44. (a) Lifson, S.; Sander, C. J. Mol. Biol. 1980, 139, 627-639.
45. (b) Nesloney, C. L.; Kelly, J. W. Bioorg. Med. Chem., in press,
46. (c) Schneider, J. P.; Kelly, J. W. Chem. Rev. 1995, 95, 2169-2187.
47. Several small peptides are capable of populating a β-turn conformation; see: (a) Rose, G. D.; Gierasch, L. M.; Smith, J. A. Adv. Protein Chem. 1985, 17, 1-109. (b) Rizo, J.; Gierasch, L. M. Annu. Rev. Biochem. 1992, 61, 387-418. (c) Dyson, H. J.; Cross, K. J.; Houghten, R. A.; Wilson, I. A.; Wright, P. E.; Lerner, R. A. Nature 1985, 318, 480. (d) Hruby, V. J. In Chemistry and Biochemistry of Amino Acids; Weinstein, B., Ed.; M. Dekker: New York, 1974; Vol. 3, pp 1-188. (e) Hruby, V. J.; Al-Obeidi, F.; Kazmierski, W. Biochem. J. 1990, 268, 249-262. (f) Hruby, V. J. Life Sci. 1982, 31, 189-199. However, concensus β-turn sequences do not appear to be sufficient to nucleate folding within sequences which are known to fold when nucleated by unnatural amino acids such as the 4-(2-aminoethyl)-6-dibenzofuranpropionic acid, unpublished results.
48. Several small peptides are capable of populating a β-turn conformation; see: (a) Rose, G. D.; Gierasch, L. M.; Smith, J. A. Adv. Protein Chem. 1985, 17, 1-109. (b) Rizo, J.; Gierasch, L. M. Annu. Rev. Biochem. 1992, 61, 387-418. (c) Dyson, H. J.; Cross, K. J.; Houghten, R. A.; Wilson, I. A.; Wright, P. E.; Lerner, R. A. Nature 1985, 318, 480. (d) Hruby, V. J. In Chemistry and Biochemistry of Amino Acids; Weinstein, B., Ed.; M. Dekker: New York, 1974; Vol. 3, pp 1-188. (e) Hruby, V. J.; Al-Obeidi, F.; Kazmierski, W. Biochem. J. 1990, 268, 249-262. (f) Hruby, V. J. Life Sci. 1982, 31, 189-199. However, concensus β-turn sequences do not appear to be sufficient to nucleate folding within sequences which are known to fold when nucleated by unnatural amino acids such as the 4-(2-aminoethyl)-6-dibenzofuranpropionic acid, unpublished results.
49. Several small peptides are capable of populating a β-turn conformation; see: (a) Rose, G. D.; Gierasch, L. M.; Smith, J. A. Adv. Protein Chem. 1985, 17, 1-109. (b) Rizo, J.; Gierasch, L. M. Annu. Rev. Biochem. 1992, 61, 387-418. (c) Dyson, H. J.; Cross, K. J.; Houghten, R. A.; Wilson, I. A.; Wright, P. E.; Lerner, R. A. Nature 1985, 318, 480. (d) Hruby, V. J. In Chemistry and Biochemistry of Amino Acids; Weinstein, B., Ed.; M. Dekker: New York, 1974; Vol. 3, pp 1-188. (e) Hruby, V. J.; Al-Obeidi, F.; Kazmierski, W. Biochem. J. 1990, 268, 249-262. (f) Hruby, V. J. Life Sci. 1982, 31, 189-199. However, concensus β-turn sequences do not appear to be sufficient to nucleate folding within sequences which are known to fold when nucleated by unnatural amino acids such as the 4-(2-aminoethyl)-6-dibenzofuranpropionic acid, unpublished results.
50. Several small peptides are capable of populating a β-turn conformation; see: (a) Rose, G. D.; Gierasch, L. M.; Smith, J. A. Adv. Protein Chem. 1985, 17, 1-109. (b) Rizo, J.; Gierasch, L. M. Annu. Rev. Biochem. 1992, 61, 387-418. (c) Dyson, H. J.; Cross, K. J.; Houghten, R. A.; Wilson, I. A.; Wright, P. E.; Lerner, R. A. Nature 1985, 318, 480. (d) Hruby, V. J. In Chemistry and Biochemistry of Amino Acids; Weinstein, B., Ed.; M. Dekker: New York, 1974; Vol. 3, pp 1-188. (e) Hruby, V. J.; Al-Obeidi, F.; Kazmierski, W. Biochem. J. 1990, 268, 249-262. (f) Hruby, V. J. Life Sci. 1982, 31, 189-199. However, concensus β-turn sequences do not appear to be sufficient to nucleate folding within sequences which are known to fold when nucleated by unnatural amino acids such as the 4-(2-aminoethyl)-6-dibenzofuranpropionic acid, unpublished results.
51. Several small peptides are capable of populating a β-turn conformation; see: (a) Rose, G. D.; Gierasch, L. M.; Smith, J. A. Adv. Protein Chem. 1985, 17, 1-109. (b) Rizo, J.; Gierasch, L. M. Annu. Rev. Biochem. 1992, 61, 387-418. (c) Dyson, H. J.; Cross, K. J.; Houghten, R. A.; Wilson, I. A.; Wright, P. E.; Lerner, R. A. Nature 1985, 318, 480. (d) Hruby, V. J. In Chemistry and Biochemistry of Amino Acids; Weinstein, B., Ed.; M. Dekker: New York, 1974; Vol. 3, pp 1-188. (e) Hruby, V. J.; Al-Obeidi, F.; Kazmierski, W. Biochem. J. 1990, 268, 249-262. (f) Hruby, V. J. Life Sci. 1982, 31, 189-199. However, concensus β-turn sequences do not appear to be sufficient to nucleate folding within sequences which are known to fold when nucleated by unnatural amino acids such as the 4-(2-aminoethyl)-6-dibenzofuranpropionic acid, unpublished results.
52. Several small peptides are capable of populating a β-turn conformation; see: (a) Rose, G. D.; Gierasch, L. M.; Smith, J. A. Adv. Protein Chem. 1985, 17, 1-109. (b) Rizo, J.; Gierasch, L. M. Annu. Rev. Biochem. 1992, 61, 387-418. (c) Dyson, H. J.; Cross, K. J.; Houghten, R. A.; Wilson, I. A.; Wright, P. E.; Lerner, R. A. Nature 1985, 318, 480. (d) Hruby, V. J. In Chemistry and Biochemistry of Amino Acids; Weinstein, B., Ed.; M. Dekker: New York, 1974; Vol. 3, pp 1-188. (e) Hruby, V. J.; Al-Obeidi, F.; Kazmierski, W. Biochem. J. 1990, 268, 249-262. (f) Hruby, V. J. Life Sci. 1982, 31, 189-199. However, concensus β-turn sequences do not appear to be sufficient to nucleate folding within sequences which are known to fold when nucleated by unnatural amino acids such as the 4-(2-aminoethyl)-6-dibenzofuranpropionic acid, unpublished results.
53. (a) Díaz, H.; Kelly, J. W. Tetrahedron Lett. 1991, 32, 5725-5728.
54. (b) Díaz, H.; Espina, J. R.; Kelly, J. W. J. Am. Chem. Soc. 1992, 114, 8316-8318.
55. (c) Díaz, H.; Tsang, K. Y.; Choo, D.; Espina, J. R.; Kelly, J. W. J. Am. Chem. Soc. 1993, 115, 3790-3791.
56. (d) Díaz, H.; Tsang, K. Y.; Choo, D.; Kelly, J. W. Tetrahedron 1993, 49, 3533-3545.
57. (e) Schneider, J. P.; Kelly, J. W. J. Am. Chem. Soc. 1995, 117, 2533-2546.
58. (f) Kemp, D. S.; Bowen, B. R. Tetrahedron Lett. 1988, 29, 5081-5082.
59. (g) Kemp, D. S.; Bowen, B. R. Tetrahedron Lett. 1988, 29, 5077-5080.
60. (h) Kemp, D. S.; Bowen, B. R.; Muendel, C. C. J. Org. Chem. 1990, 55, 4650-4657.
61. (i) Mütter, M. Trends Biochem. Sci. 1988, 13, 260.
62. (j) Mütter, M.; Vuilleumicr, S. Angew. Chem., Int. Ed. Engl. 1989, 28, 535.
63. (k) Brandmeier, V.; Feigel, M. Tetrahedron 1989, 45, 1365-1376.
64. (l) Brandmeier, V.; Feigel, M.; Bremer, M. Angew. Chem., Int. Ed. Engl. 1989, 28, 486-488.
65. (m) Brandmeier, V.; Sauer, W. H. B.; Fiegel, M. Helv. Chim. Acta 1994, 77, 70-85.
66. (n) Wagner, G.; Feigel, M. Tetrahedron 1993, 49, 10831-10842.
67. (o) Feigel, M. J. Am. Chem. Soc. 1986, 108, 181-182.
68. (p) Sato, K.; Nagai, U. J. Chem. Soc., Perkin Trans. 1 1986, 1231-1234.
69. (q) Gardner, R. R.; Liang, G.-B.; Gellman, S. H. J. Am. Chem. Soc. 1995, 117, 3280-3281.
70. (r) Nowick, J. S.; Powell, N. A.; Martinez, E. J.; Smith, E. M.; Noronha, G. J. Org. Chem. 1992, 57, 3763-3765.
71. (s) Nowick, J. S.; Smith, E. M.; Noronha, G. J. Org. Chem. 1995, 60, 7386-7387.
72. (t) Veber, D. F.; Strachan, R. G.; Bergstrand, S. J.; Holly, F. W.; Homnick, C. F.; Hirschmann, R. J. J. Am. Chem. Soc. 1976, 98, 2367-2369.
73. (u) Veber, D. F.; Holly, F. W.; Paleveda, W. J.; Nutt, R. F.; Bergstrand, S. J.; Torchiana, M.; Glitzer, M. S.; Saperstein, R.; Hirschmann, R. Proc. Natl. Acad. Sci. U.S.A. 1978, 75, 2636-2640.
74. (v) Veber, D. F.; Saperstein, R.; Nutt, R. F.; Freidinger, R. M.; Brady, S. F.; Curley, P.; Perlow, D. S.; Palveda, W. J.; Colton, C. D.; Zacchei, A. G.; Toco, D. J.; Hoff, D. R.; Vandlen, R. L.; Gerich, J. E.; Hall, L.; Mandarino, L.; Cordes, E. H.; Anderson, P. S.; Hirschmann, R. Life Sci. 1984, 34, 1371-1378.
75. (w) Freidinger, R. M.; Veber, D. F.; Schwenk Perlow, D. Science 1980, 210, 656-658.
76. Nesloney, C. L.; Kelly, J. W. J. Org. Chem. 1996, 61, 3227-3237.
77. (a) Scharfenberg, P.; Rozsondai, B.; Hargittai, I. Z. Naturforsch., A 1980, 35a, 431-436.
78. (b) Kriz, J.; Jakes, J. J. Mol. Struct. 1972, 12, 367-372.
79. (a) Dill, K. A. Biochemistry 1990, 29, 7133-7155.
80. (b) Kauzmann, W. Adv. Protein Chem. 1959, 14, 1-63.
81. (c) Rose, G. D.; Roy, S. Proc. Natl. Acad. Sci. U.S.A. 1980, 77, 4643.
82. (d) Neri, D.; Billeter, M.; Wider, G.; Wüthrich, K. Science 1992, 257, 1559-1563.
83. (e) Topping, K. D.; Evans, P. A.; Dobson, C. M. Proteins: Struct., Funct., Genet. 1991, 9, 246.
84. (f) Garvey, E. P.; Swank. J.; Matthews, C. R. Proteins: Struct., Funct. Genet. 1989, 6, 259-266.
85. Kaiser, E. T.; Kézdy, F. J. Science 1984, 223, 249-255.
86. (a) Kelly, J. W.; Lansbury, P. T., Jr. Amyloid: Int. J. Exp. Clin. Invest. 1994, 1, 186-205.
87. (b) Lansbury, P. T., Jr. Biochemistry 1992, 31, 6865.
88. Hartman, R.; Schwaner, R. C.; Hermans, J. J. Mol. Biol. 1974, 90, 415-429.
89. (a) Tonelli, A. E. J. Am. Chem. Soc. 1970, 92, 6187-6190.
90. (b) Tonelli, A. E. J. Am. Chem. Soc. 1971, 93, 7153-7155.
91. (c) Tonelli, A. E. J. Mol. Biol. 1974, 86, 627-635.
92. (d) Tonelli, A. E. Biopolymers 1976, 15, 1615-1622.
93. (e) Tonelli, A. E.; Patel, D. J. Biopolymers 1976, 15, 1623.
94. (f) Vitoux, B.; Aubry, A.; Cung, M. T.; Marraud, M. Int. J. Peptide Protein Res. 1986, 27, 617-632.
95. (a) Rajarathnam, K.; Sykes, B. D.; Kay, C. M.; Dewald, B.; Geiser, T.; Baggiolini, M.; Clark-Lewis, I. Science 1994, 264, 90-92.
96. (b) Ghadiri, M. R.; Kobayashi, K.; Granja, J. R.; Chadha, R. K.; McRee, D. E. Angew. Chem., Int. Ed. Engl. 1995, 34, 93-95.
97. (a) Kumar, N. G.; Izumiya, N.; Miyoshi, M.; Sugano, H.; Urry, D. W. Biochemistry 1975, 14, 2197-2207.
98. (b) Patel, D. J.; Tonelli, A. E. Biopolymers 1976, 15, 1623-1635.
99. Tam, J. P.; Merrifield, R. B. In The Peptides; Analysis, Synthesis, and Biology; Udenfriend, S., Meienhofer, J., Eds.; Academic Press: New York, 1987; pp 185-244.
100. (a) Chait, B. T.; Kent, S. B. H. Science 1992, 257, 1885.
101. (b) Kinsel, G. R.; Preston, L. M.; Russell, D. H. Biol. Mass Spectrom. 1994, 23, 205-211.
102. Paliwal, S.; Geib, S.; Wilcox, C. S. J. Am. Chem. Soc. 1994, 116, 4497-4498.
103. The higher concentration of peptide E (0.20 mM) versus peptide D (0.15 mM) in these studies increases the likelihood of stabilizing an intramolecular sheet by self-assembly. However, no structure is observed over the pH range of 4-9.8, providing strong evidence that peptide E does not form intramolecular β-sheet structure under these conditions.
104. 3 group of Leu-3 in peptide A and Leu-6 in peptide E was also observed. The significant increase in upfield shifting (0.3 ppm relative to that of the remaining valine methyl groups) suggests the presence of a closer interaction between the leucine δ′-methyl group and one of the aromatic rings of the biphenyl system.
105. Kobayasi, T.; Asboe-Hansen, G. J. Microsc. 1971, 93, 55-60.
106. Urry, D. W.; Luan, C-H.; Parker, T. M.; Gowda, D. C.; Prasad, K. U.; Reid, M. C.; Safavy, A. J. Am. Chem. Soc. 1991, 113, 4346-4348.
107. (a) Haris, P. I.; Chapman, D. Biopolymers 1995, 37, 251-263.
108. (b) Byler, D. M.; Susi, H. Biopolymers 1986, 25, 469-487.
109. (c) Byler, D. M.; van Gusteren, W. F. FEBS Lett. 1993, 323, 215-217.
110. (d) Surewicz, W. K.; Mantsch, H. H. Biochim. Biophys. Acta 1988, 952, 115-130.
111. (e) Surewicz, W. K.; Mantsch, H. H.; Chapman, D. Biochemistry 1993, 32, 389-394.
112. (f) Dong, A.; Caughey, W. S. Biochemistry 1990, 29, 3303-3308.
113. (g) Krimm, S.; Bandekar, J. Adv. Protein Chem. 1986, 38, 181-364.
114. (h) Takeda, N.; Kato, M.; Taniguchi, Y. Biochemistry 1995, 34, 5980-5987.
115. (i) Arrondo, J. L. J.; Young, N. M.; Mantsch, H. H. Biochim. Biophys. Acta 1988, 952, 261-268.
116. (j) Oberg, K.; Chrunyk, B. A.; Wetzel, R.; Fink, A. L. Biochemistry 1994, 33, 2628-2634.
117. Pardi, A.; Billeter, M.; Wüthrich, K. J. Mol. Biol. 1984, 180, 741-751.
118. Choo, D. W.; Fiori, W. R.; Kelly, J. W. Unpublished results.
119. Still, W. C.; Kahn, M.; Maitra, A. J. Org. Chem. 1978, 43, 2923-2925.
120. Protein Structure: A Practical Approach; Creighton, T. E., Ed.; IRL Press: Oxford, 1989; pp 251-285.
121. This figure was prepared with MolScript; see: Kraulis, P. T. J. Appl. Crystallogr. 1991, 24, 946-950.