Contribution of peptide backbone atoms to binding of an antigenic peptide to class I major histocompatibility complex molecule

Molecular Immunology

Volumn 34, Issue 16-17, 1997, Pages 1133-1145

  Saito, Naoyuki G ^a   Paterson, Yvonne ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Antigenic peptide; Class I major histocompatibility complex; Cytotoxic T lymphocyte; Hydrogen bond; Molecular modeling; Peptide backbone; Peptidomimetic methods; Retro inverso peptide

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE;

ANTIGEN BINDING; ARTICLE; CELL MEDIATED LYMPHOLYSIS; COMPUTER MODEL; CYTOTOXIC T LYMPHOCYTE; HYDROGEN BOND; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MOLECULAR INTERACTION; MOLECULAR MODEL; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN STRUCTURE;

EID: 0344352477     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0161-5890(97)00140-5     Document Type: Article

References (56)

1. Benedetti, E., Pedone, E. M., Kawahata, N. H. and Goodman, M. (1995) Conformational studies of retro-inverso peptides: the crystal and molecular structure of the hydantoin from H-Ala-g-Ala-mGly-OBzl Biopolymers 36, 659-667.
2. Benkirane, N., Guichard, G., Van Regenmortel, M. H., Briand, J. P. and Muller, S. (1995) Cross-reactivity of antibodies to retro-inverso peptidomimetics with the parent protein histone H3 and chromatin core particle. Specificity and kin-etic rate-constant measurements. J. Biol. Chem. 270, 11921-11926.
3. Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennett, W. S., Strominger, J. L. and Wiley, D. C. (1987a) The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329, 512-518.
4. Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennett, W. S., Strominger, J. L. and Wiley, D. C. (1987b) Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329, 506-512.
5. Bouvier, M. and Wiley, D. C. (1994) Importance of peptide amino and carboxyl termini to the stability of MHC class I molecules. Science 265, 398-402.
6. Briand, J. P., Guichard, G., Dumortier, H. and Muller, S. (1995) Retro-inverso peptidomimetics as new immunological probes. Validation and application to the detection of antibodies in rheumatic diseases. J. Biol. Chem. 270, 20686-20691.
7. Brugidou, J., Legrand, C., Mery, J. and Rabie, A. (1995) The retro-inverso form of a homeobox-derived short peptide is rapidly internalised by cultured neurones: a new basis for an efficient intracellular delivery system. Biochem. Biophys. Res. Commun. 214, 685-693.
8. Chorev, M. and Goodman, M. (1995) Recent developments in retro peptides and proteins - an ongoing topochemical exploration. Trends Biotechnol. 13, 438-445.
9. Dauber-Osguthorpe, P., Roberts, V. A., Osguthorpe, D. J., Wolff, J., Genest, M. and Hagler, A. T. (1988) Structure and energetics of ligand binding to proteins: Escherichia coli dihydrofolate reductase-trimethoprim, a drug-receptor system. Proteins 4, 31-47.
10. Dürr. H., Goodman, M. and Jung, G. (1992) Retro-inverso amide bonds between trifunctional amino acids. Angew. Chem. Int. Ed. Engl. 31, 785-787.
11. Falk, K., Rotzschke, O., Stevanovic, S., Jung, G. and Rammensee, H. G. (1991) Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351, 290-296.
12. Feltkamp, M. C., Vierboom, M. P., Toes, R. E., Ossendorp, F., ter Schegget, J., Melief, C. J. and Kast, W. M. (1995) Competition inhibition of cytotoxic T-lymphocyte (CTL) lysis, a more sensitive method to identify candidate CTL epitopes than induction of antibody-detected MHC class I stabilization. Immunol. Lett. 47, 1-8.
13. b. Science 257, 919-927.
14. bovalbumin peptide complex reveals the interplay of primary and secondary anchor positions in the major histocompatibility complex binding groove. Proc. Natl. Acad. Sci. U.S.A. 92, 2479-2483.
15. Goodman, M. and Chorev, M. (1979) On the concept of linear modified retro-peptide structures. Acc. Chem. Res. 12, 1-7.
16. Goodman, M., Ro, S., Yamazaki, T., Spencer, J. R., Toy, A., Huang, Z., He, Y. and Reisine, T. (1992) Topochemical design of bioactive peptides and peptidomimetics. Bioorg. Khimi. 18, 1375-1393.
17. Guichard, G., Benkirane, N., Zeder-Lutz, G., van Regenmortel, M. H., Briand, J. P. and Muller, S. (1994) Antigenic mimicry of natural L-peptides with retro-inverso-peptidomimetics. Proc. Natl. Acad. Sci. U.S.A. 91, 9765-9769.
18. Guichard, G., Calbo, S., Muller, S., Kourilsky, P., Briand, J. P. and Abastado, J. P. (1995) Efficient binding of reduced peptide bond pseudopeptides to major histocompatibility complex class I molecule. J. Biol. Chem. 270, 26057-26059.
19. Guichard, G., Connan, F., Graff, R., Ostankovitch, M., Muller, S., Guillet, J. G., Choppin, J. and Briand, J. P. (1996) Partially modified retro-inverso pseudopeptides as non-natural ligands for the human class I histocompatibility molecule HLA-A2. J. Med. Chem. 39, 2030-2039.
20. Guo, H. C., Jardetzky, T. S., Garrett, T. P., Lane, W. S., Strominger, J. L. and Wiley, D. C. (1992) Different length peptides bind to HLA-Aw68 similarly at their ends but bulge out in the middle. Nature 360, 364-366.
21. Hillenkamp, F., Karas, M., Beavis, R. C. and Chait, B. T. (1991) Matrix-assisted laser desorption ionization mass spectroscopy. Anal. Chem. 63, 1193A-1203A.
22. b-restricted ovalbumin peptide and an assessment of the predictive power of MHC-binding motifs. Eur. J. Immunol. 22, 2663-2667.
23. b using a monoclonal antibody. Biochem. Biophys. Res. Commun. 186, 1449-1454.
24. Latron, F., Moots, R., Rothbard, J. B., Garrett, T. P., Strominger, J. L. and McMichael, A. (1991) Positioning of a peptide in the cleft of HLA-A2 by complementing amino acid changes. Proc. Natl. Acad. Sci. U.S.A. 88, 11325-11329.
25. Latron, F., Pazmany, L., Morrison, J., Moots, R., Saper, M. A., McMichael, A. and Strominger, J. L. (1992) A critical role for conserved residues in the cleft of HLA-A2 in presentation of a nonapeptide to T cells. Science 257, 964-967.
26. Lipford, G. B., Bauer, S., Wagner, H. and Heeg, K. (1995) In vivo CTL induction with point-substituted ovalbumin peptides: immunogenicity correlates with peptide-induced MHC class I stability. Vaccine 13, 313-320.
27. b binding motif. J. Immunol. 150, 1212-1222.
28. Ljunggren, H. G., Stam, N. J., Ohlen, C., Neefjes, J. J., Hoglund, P., Heemels, M. T., Bastin, J., Schumacher, T. N., Townsend, A., Karre, K., et al. (1990) Empty MHC class I molecules come out in the cold. Nature 346, 476-480.
29. Madden, D. R., Garboczi, D. N. and Wiley, D. C. (1993) The antigenic identity of peptide-MHC complexes: a comparison of the conformations of five viral peptides presented by HLA-A2. Cell 75, 693-708.
30. Madden, D. R., Gorga, J. C., Strominger, J. L. and Wiley, D. C. (1991) The structure of HLA-B27 reveals nonamer self-peptides bound in an extended conformation. Nature 353, 321-325.
31. Madden, D. R., Gorga, J. C., Strominger, J. L. and Wiley, D. C. (1992) The three-dimensional structure of HLA-B27 at 2.1 Å resolution suggests a general mechanism for tight peptide binding to MHC. Cell 70, 1035-1048.
32. Matsumura, M., Fremont, D. H., Peterson, P. A. and Wilson, I. A. (1992a) Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science 257, 927-934.
33. Matsumura, M., Saito, Y., Jackson, M. R., Song, E. S. and Peterson, P. A. (1992b) In vitro peptide binding to soluble empty class I major histocompatibility complex molecules isolated from transfected Drosophlla melanoyaster cells. J. Biol. Chem. 267, 23589-23595.
34. Merrifield, T. B. (1963) Solid phase peptide synthesis. I. The synthesis of a tetrapeptide. J. Am. Chem. Soc. 85, 2149-2154.
35. Miller, S. M., Simon, R. J., Ng. S., Zuckermann, R. N., Kerr, J. M. and Moos, W. H. (1995) Comparison of the proteolytic susceptibilities of homologous L-amino acid, D-amino acid, and N-substituted glycine peptide and peptoid oligomers. Drug Dev. Res. 35, 20-32.
36. Moore, G. J. (1994) Designing peptide mimetics. Trends Pharmacol. Sci. 15, 124-129.
37. Moore, G. J., Smith, J. R., Baylis, B. W. and Matsoukas, J. M. (1995) Design and pharmacology of peptide mimetics. Adv. Pharmacol.33, 91-141.
38. Muller, S., Guichard, G., Benkirane, N., Brown, F., Van Regenmortel, M. H. and Briand, J. P. (1995) Enhanced immunogenicity and cross-reactivity of retro-inverso peptidomimetics of the major antigenic site of foot-and-mouth disease virus. Pept. Res. 8, 138-144.
39. Neefjes, J. J., Dierx, J. and Ploegh, H. L. (1993) The effect of anchor residue modifications on the stability of major histocompatibility complex class I-peptide interactions. Eur. J. Immunol. 23, 840-845.
40. Olson, G. L., Bolin, D. R., Bonner, M. P., Bos, M., Cook, C. M., Fry, D. C., Graves, B. J., Hatada, M., Hill, D. E., Kahn, M., et al. (1993) Concepts and progress in the development of peptide mimetics. J. Med. Chem. 36, 3039-3049.
41. Patel, D. V. and Ryono, D. E. (1992) Retro-inverso tripeptide renin inhibitors. Bioorg. Med. Chem. Lett. 2, 1089-1092.
42. Puddington, L., Bevan, M. J., Rose, J. K. and Lefrancois, L. (1986) N protein is the predominant antigen recognized by vesicular stomatitis virus-specific cytotoxic T cells. J. Virol. 60, 708-717.
43. Ruvo, M. and Fassina, G. (1995) End-group modified retroinverso isomers of tripeptide oxytocin analogues: binding to neurophysin II and enhancement of its self-association properties. Int. J. Pept. Prot. Res. 45, 356-365.
44. Saito, Y., Peterson, P. A. and Matsumura, M. (1993) Quantitation of peptide anchor residue contributions to class I major histocompatibility complex molecule binding. J. Biol. Chem. 268, 21309-21317.
45. b-restricted anti-vesicular stomatitus virus and alloreactive cytotoxic T cells. J. Immunol. 138, 3654-3660.
46. b molecule by the side chains of three amino acids and the main-chain atoms of the amino terminus. Proc. Natl. Acad. Sci. U.S.A. 89, 3135-3139.
47. Silver, M. L., Guo, H. C., Strominger, J. L. and Wiley, D. C. (1992) Atomic structure of a human MHC molecule presenting an influenza virus peptide. Nature 360, 367-369.
48. Townsend, A. R., Gotch, F. M. and Davey, J. (1985) Cytotoxic T cells recognize fragments of the influenza nucleoprotein. Cell 42, 457-467.
49. Townsend, A. R., Rothbard, J., Gotch, F. M., Bahadur, G., Wraith, D. and McMichael, A. J. (1986) The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell 44, 959-968.
50. b molecule. Nature 348, 213-216.
51. Verdoliva, A., Ruvo, M., Cassani, G. and Fassina, G. (1995a) Topological mimicry of cross-reacting enantiomeric peptide antigens. J. Biol. Chem. 270, 30422-30427.
52. Verdoliva, A., Ruvo, M., Villain, M., Cassani, G. and Fassina, G. (1995b) Antigenicity of topochemically related peptides. Biochim. Biophys. Acta 1253, 57-62.
53. Wunderlich, J. and Shearer, G. (1991) Assays for T cell function. In Current Protocols in Immunology, eds J. E. Coligan, A. M. Kruisbeek, D. J. Margulies, E. M. Shevach and W. Strober, pp. 3.11.1-3.11.15. Greene Publishing and Wiley-Interscience, New York.
54. Yaksh, T. L., Malmberg, A. B., Ro, S., Schiller, P. and Goodman, M. ( 1995) Characterization of the spiral antinociceptive activity of constrained peptidomimetic opicids. J. Pharmacol. Exp. Ther. 275, 63-72.
55. b at 2.4 Å resolution: implications for antigendeterminant selection. Cell 76, 39-50.
56. b molecule containing a single viral peptide: implications for peptide binding and T-cell receptor recognition. Proc. Natl. Acad. Sci. U.S.A. 89, 8403-8407.