Conformational analysis of furanoid ε-sugar amino acid containing cyclic peptides by NMR spectroscopy, molecular dynamics simulation, and X-ray crystallography: Evidence for a novel turn structure

Journal of the American Chemical Society

Volumn 125, Issue 36, 2003, Pages 10822-10829

  Van Well, Renate M ^a   Marinelli, Luciana ^b   Altona, Cornelis ^a   Erkelens, Kees ^a   Siegal, Gregg ^a   Van Raaij, Mark ^a,c   Llamas Saiz, Antonio L ^c   Kessler, Horst ^b   Novellino, Ettore ^d   Lavecchia, Antonio ^d   Van Boom, Jacques H ^a   Overhand, Mark ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; HYDROGEN BONDS; MOLECULAR DYNAMICS; SUGAR (SUCROSE); X RAY ANALYSIS;

PEPTIDE SCAFFOLDS;

AMINO ACIDS;

CYCLO(ARGINYLGLYCYLASPARTYLSERYLALANYLALANINE); CYCLO(ARGINYLGLYCYLASPARTYLVALYLSERYLALANYLALANINE); CYCLO(PHENYLALANYLSERYLALANYLALANYLSERYLALANYLALANYLALANINE); CYCLOPEPTIDE; FURAN DERIVATIVE; FURANOID EPSILON SUGAR AMINO ACID; UNCLASSIFIED DRUG; VALINE;

ARTICLE; CALCULATION; CRYSTAL STRUCTURE; DRUG ACTIVITY; DRUG CONFORMATION; DRUG STRUCTURE; HYBRID; HYDROGEN BOND; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOLECULE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; STRUCTURE ANALYSIS; THROMBOCYTE AGGREGATION; X RAY CRYSTALLOGRAPHY;

AMINO ACIDS; AMINO SUGARS; CARBOHYDRATE CONFORMATION; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; FURANS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES, CYCLIC; PROTEIN STRUCTURE, SECONDARY; SUGAR ACIDS;

EID: 10744230715     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja035461+     Document Type: Article

References (84)

1. (a) Lohof, E.; Burkhart, F.; Born, M. A.; Planker, E.; Kessler, H. Advances in Amino Acid Mimetics and Peptidomimetics; Abell, A., Ed.; JAI Press, Inc.: Stanford, Conneticut, 1999; Vol. 2, p 263.
2. (b) Gruner, S. A. W.; Locardi, E.; Lohof, E.; Kessler, H. Chem. Rev. 2002, 102, 491.
3. (c) Schweizer, F. Angew. Chem. Int. Ed. 2002, 41, 230.
4. (d) Chakraborty, T. K.; Ghosh, S.; Jayaprakash, S. Curr. Med. Chem. 2002, 9, 421.
5. (e) Graf von Roedern, E.; Born, M. A.; Stöckle, M.; Kessler, H. Synthesis of Peptides with Sugar Amino Acids; Goodman, M., Ed.; In Houben-Weyl; Thieme: Stuttgart, 2003; Vol. E22c, p 807.
6. Biochemistry; Zubay, G., Ed.; Macmillan Publishing: New York, 1988; p 149.
7. (a) Schauer, R. Glycoconjugate J. 2000, 17, 485.
8. (b) Kiefel, M. J.; von Itzstein, M. Chem. Rev. 2002, 102, 471.
9. Umezawa, H.; Aoyagi, T.; Komiyama, H.; Hamada, M.; Takeuchi, T. J. Antibiot. 1974, 27, 963.
10. (a) Sakata, K.; Sakurai, A.; Tamura, S. Tetrahedron Lett. 1974, 16, 1533.
11. (b) Sakata, K.; Sakurai, A.; Tamura, S. Tetrahedron Lett. 1974, 49, 4327.
12. Fuchs, E.; Lehman, J. Carbohydr. Res. 1976, 49, 267.
13. (a) Timmers, C. M.; Turner, J. J.; Ward, C. M.; van der Marel, G. A.; Kouwijzer, M. L. C. E.; Grootenhuis, P. D. J.; van Boom, J. H. Chem.-Eur. J. 1997, 3, 920.
14. (b) Szabo, L.; Smith, B. L.; McReynolds, K. D.; Parrill, A. L.; Morris, E. R.; Gervay, J. J. Org. Chem. 1998, 63, 1074.
15. (c) Smith, M. D.; Long, D. D.; Martin, A.; Marquess, D. G.; Claridge, T. D. W.; Fleet, G. W. J. Chem. Commun. 1998, 2041.
16. (d) Smith, M. D.; Claridge, T. D. W.; Tranter, G. E.; Sansom, M. S. P.; Fleet, G. W. J. Chem. Commun. 1998, 2039.
17. (e) Long, D. D.; Smith, M. D.; Martin, A.; Marquess, D. G.; Claridge, T. D. W.; Fleet, G. W. J. Tetrahedron Lett. 1998, 39, 9293.
18. (f) Smith, M. D.; Long, D. D.; Martin, A.; Marquess, D. G.; Claridge, T. D. W.; Fleet, G. W. J. Tetrahedron Lett. 1999, 40, 2191.
19. (g) Long, D. D.; Hungerford, N. L.; Smith, M. D.; Brittain, D. E. A.; Marquess, D. G.; Claridge, T. D. W.; Fleet, G. W. J. Tetrahedron Lett. 1999, 40, 2195.
20. (h) Hungerford, N. L.; Claridge, T. D. W.; Aplin, R. T.; Moreno, A.; Fleet, G. W. J. J. Chem. Soc., Perkin Trans. 1 2000, 3666.
21. (i) Brittain, D. E. A.; Watterson, M. P.; Claridge, T. D. W.; Smith, M. D.; Fleet, G. W. J. J. Chem. Soc., Perkin Trans. 1 2000, 3655.
22. (j) Chakraborty, T. K.; Jayaprakash, S.; Srinivasu, P.; Govardhana Chary, M.; Diwan, P. V.; Nagaraj, R.; Ravi Sankar, A.; Kunwar, A. C. Tetrahedron Lett. 2000, 41, 8167.
23. (k) Suhara, Y.; Yamaguchi, Y.; Collins, B.; Schnaar, R.; Yanagishita, M. ; Hildreth, J. E. K.; Shimada, I.; Ichikawa, Y. Bioorg. Med. Chem. 2002, 10, 1999.
24. Gruner, S. A. W.; Truffault, V.; Voll, G.; Locardi, E.; Stöckle, M. ; Kessler, H. Chem.-Eur. J. 2002, 8, 4365.
25. (a) Graf von Roedern, E.; Lohof, E.; Hessler, G.; Hoffman, M.; Kessler, H. J. Am. Chem. Soc. 1996, 118, 10156.
26. (b) Lohof, E.; Planker, E.; Mang, C.; Burkhart, F.; Dechantsreiter, M. A.; Haubner, R.; Wester, H. J.; Schwaiger, M.; Hölzemann, G.; Goodman, S. L.; Kessler, H. Angew. Chem., Int. Ed. 2000, 39, 2761.
27. (c) Gruner, S. A. W.; Kéri, G.; Schwab, R.; Venetianer, A.; Kessler, H. Org. Lett. 2001, 3, 3723.
28. (d) Chakraborty, T. K.; Jayaprakash, S.; Diwan, P. V.; Nagaraj, R.; Jampani, S. R. B.; Kunwar, A. C. J. Am. Chem. Soc. 1998, 120, 12962.
29. (e) Chakraborty, T. K.; Ghosh, S.; Jayaprakash, S.; Sharma, J. A. R. P.; Ravikanth, V.; Diwan, P. V.; Nagaraj, R.; Kunwar, A. C. J. Org. Chem. 2000, 65, 6441.
30. (f) Smith, A. B., III; Sasho, S.; Barwis, B. A.; Sprengeler, P.; Barbosa, J.; Hirschmann, R.; Cooperman, B. S. Bioorg. Med. Chem. Lett. 1998, 8, 3133.
31. (g) Overkleeft, H. S.; Verhelst, S. H. L.; Pieterman, E.; Meeuwenoord, N. J.; Overhand, M.; Cohen, L. H.; van der Marel, G. A.; van Boom, J. H. Tetrahedron Lett. 1999, 40, 4130.
32. (h) Aguilera, B.; Siegal, G.; Overkleeft, H. S.; Meeuwenoord, N. J.; Rutjes, F. P. J. T.; van Hest, J. C. M.; Schoemaker, H. E.; van der Marel, G. A.; van Boom, J. H.; Overhand, M. Eur. J. Org. Chem. 2001, 1541.
33. (i) El Oualid, F.; Bruining, L.; Leroy, I. M.; Cohen, L. H.; van Boom, J. H.; van der Marel, G. A.; Overkleeft, H. S.; Overhand, M. Helv. Chim. Acta 2002, 85, 3455.
34. (j) Chakraborty, T. K.; Jayaprakash, S.; Srinivasu, Madhavendra, S. S.; Ravi Sankar, A.; Kunwar, A. C. Tetrahedron 2002, 58, 2853.
35. McDevitt, J. P.; Lansbury, P. T., Jr. J. Am. Chem. Soc. 1996, 118, 3818.
36. (a) van Well, R. M.; Overkleeft, H. S.; Overhand, M.; Vang Carstenen, E. ; van der Marel, G. A.; van Boom, J. H. Tetrahedron Lett. 2000, 41, 9331.
37. (b) van Well, R. M.; Overkleeft, H. S.; Overhand, M.; van der Marel, G. A.; Bruss, D.; de Groot, P. G.; van Boom, J. H. Bioorg. Med. Chem. Lett. 2003, 13, 331.
38. (a) Haubner, R.; Finsinger, D.; Kessler, H. Angew. Chem., Int. Ed. Engl. 1997, 36, 1375.
39. (b) Ojima, I.; Chakravarty, S.; Dong, Q. Bioorg. Med. Chem. 1995, 3, 337.
40. NMR of proteins and nucleic acids; Wüthrich, K., Ed.; Wiley: New York, 1986; Chapter 7, p 123.
41. NMR of proteins and nucleic acids; Wüthrich, K., Ed.; Wiley: New York, 1986; Chapter 2, p 17.
42. 2O, and the observed -Δδ/ΔT values of the NH of the SAA residues are comparable with those values found in other structured and unstructured linear SAA containing oligomers.8j
43. (a) Mierke, D. F.; Kessler, H. Biopolymers 1993, 33, 1003.
44. (b) Havel, T. F. Prog. Biophys. Mol. Biol. 1991, 56, 43.
45. (c) Havel, T. F. Quantum Chemistry Program, Exchange No. 507; Indiana University, 1988.
46. Tordam, A. E.; Scheek, R. M.; van Gunsteren, W. F. J. Mol. Biol. 1990, 214, 223.
47. (a) Maple, J. R.; Dinur, U.; Hagler, A. T. Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 5350.
48. (b) Dauber Osguthorpe, P.; Roberts, V. A.; Osguthorpe, D. J.; Wolff, J.; Genest, M.; Hagler, A. T. Proteins: Strut., Funct., Genet. 1988, 4, 31.
49. The H bond population has been calculated accepting a distance between the donor and the acceptor of <3.2 Å and an angle between the vectors CO and NH of 180 × 70°.
50. Structure and conformation of nucleic acids and protein-nucleic acid interactions; Sundaralingam, M.; Rao, S. T., Eds.; University Park Press: Baltimore, 1974; Part 5, p 487.
51. (a) Altona, C.; Sundaralingam, M. J. Am. Chem. Soc. 1972, 94, 8205.
52. (b) Altona, C.; Sundaralingam, M. J. Am. Chem. Soc. 1973, 95, 2333.
53. 1 side chain was impossible, information about its orientation was lost. Therefore, the conformation of the Phe side chain could not be calculated and the depicted structures are not representative concerning its orientation.
54. (a) van Wijk, J.; Haasnoot, C. A. G.; de Leeuw, F. A. A. M.; Huckriede, B. D.; Westra Hoekzema, A.; Altona, C. PSEUROT 6.3; Leiden Institute of Chemistry, Leiden University: The Netherlands, 1999.
55. (b) de Leeuw, F. A. A. M.; Altona, C. J. Comput. Chem. 1983, 4, 428.
56. (c) Altona, C. Recl. Trav. Chim. Pays-Bas 1982, 101, 413.
57. (a) Laatikainen, R.; Niemitz, M.; Weber, U.; Sundelin, J.; Hassinen, T.; Vepsäläinen, J. J. Magn. Reson. 1996, A120, 1.
58. (b) Laatikainen, R.; Niemitz, M.; Malaisse, W. J.; Biesemans, M.; Willem, R. Magn. Reson. Med. 1996, 36, 359.
59. (a) Altona, C. Vicinal Coupling Constants & Conformation of Biomolecules in Encyclopedia of NMR; Grant, D. M., Harris, R. K., Eds.; Wiley: New York, 1996; p 4909.
60. (b) van Wijk, J.; Huckriede, B. D.; Ippel, J. H.; Altona, C. Furanose sugar conformations in DNA from NMR coupling constants. In Methods in Enzymology; Lilley, D. J. M., Dahlberg, J. E., Eds.; Academic Press: San Diego, 1992; Vol. 211, p 286.
61. (c) Altona, C.; Ippel, J. H.; Westra Hoekzema, A. J. A.; Erkelens, C.; Groesbeek, M.; Donders, L. A. Magn. Reson. Chem. 1989, 27, 564.
62. (d) Altona, C.; Francke, R.; de Haan, R.; Ippel, J. H.; Daalmans, G. J.; van Wijk, J. Magn. Reson. Chem. 1994, 32, 670.
63. Klyne, W.; Prelog, V. Experientia 1960, 16, 521.
64. Kessler, H.; Zimmerman, G.; Förster, H.; Engel, J.; Oepem, G.; Sheldrick, W. S. Angew. Chem., Int. Ed. Engl. 1981, 20, 1053.
65. (a) Hanson, K. R. J. Am. Chem. Soc. 1966, 88, 2731.
66. (b) Hirschmann, H.; Hanson, K. R. J. Org. Chem. 1971, 36, 3293.
67. As diastereotopic assignment of the β protons in the side chains of Asp and Arg was impossible, information about the side chain orientation was lost. Therefore, the conformation of the Arg and Asp side chains could not be calculated and the depicted structures are not representative concerning their orientation.
68. Dechantsreiter, M. A.; Planker, E.; Mathä, B.; Lohof, E.; Hölzeman, G.; Jonczyk, A.; Goodman, S. L.; Kessler, H. J. Med. Chem. 1999, 42, 3033.
69. The possibility to fix the rotamer populations around the exocyclic methylene functions to predetermine the conformation of the ε-SAA residue is currently under investigation.
70. (a) Kessler, H. Angew. Chem., Int. Ed. Engl. 1982, 21, 512.
71. (b) Gurrath, M.; Müller, G.; Kessler, H.; Aumailley, M.; Timpl, R. Eur. J. Biochem. 1992, 210, 911.
72. A cyclic-modified peptide, containing a structurally related ε-amino acid having a thiophene ring rather than a furanoid ring and three amino acids, adopts a totally different conformation: Feigel, M.; Lugert, G.; Heichert, C. Liebigs Ann. Chem. 1987, 367.
73. (a) Pfaff, M.; Tangemann, K.; Müller, B.; Gurrath, M.; Müller, G.; Kessler, H.; Timpl, R.; Engel, J. J. Biol. Chem. 1994, 269, 20233.
74. (b) Müller, G.; Gurrath, M.; Kessler, H. J. Comput.-Aided Mol. Des. 1994, 8, 709.
75. A pyranoid ε-SAA incorporated as a scaffold in a mammalian ribonucleotide reductase inhibitor was shown to be able to adopt a conformation similar to the β-turn conformation of the parent heptapeptide with the SAA replacing the i + 1 and i + 2 residues of the turn.8f It is not excluded that a nine-member intraresidue H bond interaction can also be observed in this ε-SAA-containing peptide.
76. (a) Gellman, S. H. Acc. Chem. Res. 1998, 31, 173.
77. (b) Seebach, D.; Matthews, J. L. Chem. Commun. 1997, 2015.
78. (c) Gademann, K.; Hintermann, T.; Schreiber, J. V. Curr. Med. Chem. 1999, 6, 905.
79. (d) DeGrado, W. F.; Schneider, J. P.; Hamuro, Y. J. Pept. Res. 1999, 54, 206.
80. (e) Hill, D. J.; Mio, M. J.; Prince, R. B.; Hughes, T. S.; Moore, J. S. Chem. Rev. 2001, 101, 3893.
81. Piotto, M.; Saudek, V.; Sklenar, V. J. Biom. NMR 1992, 2, 661.
82. Bax, A. J. Magn. Reson. 1988, 77, 134.
83. Weeks, C. M.; Miller, R. J. Appl. Crystallogr. 1999, 32, 120.
84. Herbst-Irmer, R.; Sheldrick, G. M. Acta Crystallogr., Sect. B 1998, 54, 443.