Binding of longer peptides to the H-2Kb heterodimer is restricted to peptides extended at their C terminus: Refinement of the inherent MHC class I peptide binding criteria

Journal of Immunology

Volumn 163, Issue 8, 1999, Pages 4434-4441

  Hörig, Heidi ^a   Young, Aideen C M ^a,b   Papadopoulos, Nicholas J ^a,c   DiLorenzo, Teresa P ^a   Nathenson, Stanley G ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b PPS International Communications Ltd   (United Kingdom)

^c REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIGEN BINDING; ANTIGEN PRESENTATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL;

EID: 0345493812     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (42)

1. Madden, D. R. 1995. The three-dimensional structures of peptide-MHC complexes. Annu. Rev. Immunol 13: 587.
2. Pamer, E., and P. Cresswell. 1998. Mechanism of MHC class I-restricted antigen processing. Annu. Rev. Immunol. 16:323.
3. Young, A. C. M., S. G. Nathenson, and J. C. Sacchettini. 1995. Structural studies of class I major histocompatibility complex proteins: insights into antigen presentation. FASEB J. 9:26.
4. Rammensee, H.-G., J. Bachmann, and S. Stevanović. 1997. The function. In MHC Ligands and Peptides Motifs. H.-G. Rammensee, J. Bachmann, and S. Stevanović, eds. Springer-Verlag, Heidelberg, Germany, p. 217.
5. b) associated with unusually long peptides: implications for antigen processing and presentation. Proc. Natl. Acad. Sci. USA 91:4145.
6. Urban, R. G., R. M. Chicz, W. S. Lane, J. L. Strominger, A. Rehm, M. J. H. Kenter, F. G. C. M. UytdeHaag, H. Ploegh, B. Uchanska-Ziegler, and A. Ziegler. 1994. A subset of HLA-B27 molecules contains peptides much longer than nonamers. Proc. Natl. Acad. Sci. USA 91:1534.
7. Engelhard, V. H., E. Appella, D. C. Benjamin, W. M. Bodnar, A. L. Cox, Y. Chen, R. A. Henderson, E. L. Huczko, H. Michel, K. Sakaguichi, et al. 1993. Mass spectrometric analysis of peptides associated with the human class I MHC molecules HLA-A2.1 and HLA-B7 and identification of structural features that determine binding. In Naturally Processed Peptides, Vol. 57: Chemical Immunology. A. Sette, ed., Karger, Basel, p. 39.
8. Henderson, R. A., H. Michel, K. Sakaguchi, J. Shabanowitz, E. Appella, D. F. Hunt, and V. H. Engelhard. 1992. HLA-A2.1-associated peptides from a mutant cell line: a second pathway of antigen presentation. Science 255:1264.
9. Bouvier, M., and D. C. Wiley. 1994. Importance of peptide amino and carboxyl termini to the stability of MHC class I molecules. Science 265:398.
10. Guo, H.-C, T. S. Jardetzky, T. P. J. Garrett, W. S. Lane, J. L. Strominger, and D. C. Wiley. 1992. Different length peptides bind to HLA-Aw68 similarly at their ends but bulge out in the middle. Nature 360:364.
11. Madden, D. R., D. N. Garboczi, and D. C. Wiley. 1993. The antigenic identity of peptide-MHC complexes: a comparison of the conformations of five viral peptides presented by HLA-A2. Cell 75:693.
12. b-ovalbumin peptide complex reveals the interplay of primary and secondary anchor positions in the major histocompatibility complex binding groove. Proc. Natl. Acad. Sci. USA 92:2479.
13. Collins, E. J., D. N. Garboczi, and D. C. Wiley. 1994. Three-dimensional structure of a peptide extending from one end of a class I MHC binding site. Nature 371:626.
14. Androlewicz, M. J., and P. Cresswell. 1996. How selective is the transporter associated with antigen processing? Immunity 5:1.
15. Schuhmacher, T. N., D. V. Kantesaria, M.-T. Heemels, P. G. Ashton-Rickardt, J. C. Shepherd, K. Fruh, Y. Yang, P. A. Peterson, S. Tonegawa, and H. L. Ploegh. 1994. Peptide length and sequence specificity of the mouse TAP1/TAP2 translocator. J. Exp. Med. 179:533.
16. Momburg, F., J. Roelse, G. J. Hämmerling, and J. J. Neefjes. 1994. Peptide size selection by the major histocompatibility complex-encoded peptide transporter. J. Exp. Med. 179:1613.
17. Hughes, E. A., B. Ortmann, M. Surman, and P. Cresswell. 1996. The protease inhibitor, N-acetyl-L-leucyl-L-leucyl-L-norleucinal, decreases the pool of major histocompatibility complex class I-binding peptides and inhibits peptide trimming in the endoplasmic reticulum. J. Exp. Med. 183:1569.
18. Elliott, T., A. Willis, V. Cerundolo, and A. Townsend. 1995. Processing of major histocompatibility class I-restricted antigens in the endoplasmic reticulum. J. Exp. Med. 181:1481.
19. Roelse, J., M. Gromme, F. Momburg, G. Hämmerling, and J. Neefjes. 1994. Trimming of TAP-translocated peptides in the endoplasmic reticulum and in the cytosol during recycling. J. Exp. Med. 180:1591.
20. Ojcius, D. M., P. Langlade-Demoyen, G. Gachelin, and P. Kourilsky. 1994. Role for MHC class I molecules in selecting and protecting high affinity peptides in the presence of proteases. J. Immunol. 152:2798.
21. Spee, P., and J. Neefjes. 1997. TAP-translocaled peptides specifically bind proteins in the endoplasmic reticulum, including gp96, protein disulfide isomerase and calreticulin. Eur. J. Immunol. 27:2441.
22. Arnold, D., C. Wahl, S. Faath, H. G. Rammensee, and H. Schild. 1997. Influences of transporter associated with antigen processing (TAP) on the repertoire of peptides associated with the endoplasmic reticulum-resident stress protein gp96. J. Exp. Med. 186:461.
23. Lammert, E., S. Stevanović, J. Brunner, H. G. Rammensee, and H. Schild. 1997. Protein disulfide isomerase is the dominant acceptor for peptides translocated into the endoplasmic reticulum. Eur. J. Immunol. 27:1685.
24. Srivastava, P. K., H. Udono, N. E. Blachere, and Z. Li. 1994. Heat shock proteins transfer peptides during antigen processing and CTL priming. Immunogenetics 39:93.
25. 2-microglobulin complexes associate with TAP transporters before peptide binding. Nature 386:864.
26. Suh, W. K., E. K. Mitchell, Y. Yang, P. A. Peterson, G. L. Waneck, and D. B. Williams. 1996. MHC class I molecules form ternary complexes with calnexin and TAP and undergo peptide-regulated interaction with TAP via their extracellular domains. J. Exp. Med 184:337.
27. Lewis, J. W., and T. Elliott. 1998. Evidence for successive peptide binding and quality control stages during MHC class I assembly. Curr. Biol. 8:717.
28. Elliott, T. 1997. How does TAP associate with MHC class I molecules? Immunol. Today 18:375.
29. Papadopoulos, N. J., J. C. Sacchettini, S. G. Nathenson, and R. H. Angeletti. 1995. Rapid in vitro assembly of class I major histocompatibility complex. In Techniques in Protein Chemistry VI. J. W. Crabb, ed. Academic Press, New York, p. 375.
30. b molecule containing a single viral peptide: implications for peptide binding and T-cell receptor recognition. Proc. Natl. Acad. Sci. USA 89:8403.
31. Jones, T. A. 1985. Interactive computer graphics: FRODO. In Diffraction Methods for Biological Macromolecules, Part B: Methods in Enzymology, Vol. 115. H. W. Wyckoff, C. H. W. Hirs, and S. N. Timasheff, eds. Academic Press, New York, p. 157.
32. Laskowski, R. A., M. W. Macarthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check stereochemical quality of protein structures. J. Appl. Cryst. 26:283.
33. Matsumura, M., Y. Saito, M. R. Jackson, E. S. Song, and P. A Peterson. 1992. In vitro peptide binding to soluble empty class I major histocompatibility complex molecules isolated from transfected Drosophila melanogaster cells. J. Biol. Chem. 267:23589.
34. Chen, Y., J. Sidney, S. Southwood, A. L. Cox, K. Sakaguchi, R. A. Henderson, E. Appella, D. F. Hunt, A. Sette, and V. H. Engelhard. 1994. Naturally processed peptides longer than nine ammo acid residues bind to the class I MHC molecule HLA-A2.1 with high affinity and in different conformations. J. Immunol. 152: 2874.
35. Olsen, A. C., L. O. Pedersen, A. S. Hansen, M. H. Nissen, M. Olsen, P. R. Hansen, A. Holm, and S. Buus. 1994. A quantitative assay to measure the interaction between immunogenic peptides and purified class I major histocompatibility complex molecules. Eur. J. Immunol 24:385.
36. Carreno, B. M., J. C. Solheim, M. Harris, I. Stroynowski, J. M. Connolly, and T. H. Hansen. 1995. TAP associates with a unique class I conformation, whereas calnexin associates with multiple class I forms in mouse and man. J. Immunol. 155:4726.
37. Kulig, K., D. Nandi, I. Bacik, J. J. Monaco, and S. Vukmanović 1998. Physical and functional association of the major histocompatibility complex class I heavy chain α3 domain with the transporter associated with antigen processing. J. Exp. Med. 187:865.
38. Smith, K. J., S. W. Reid, D. I. Stuart, A. J. McMichael, E. Y. Jones, and J. I. Bell. 1996. An altered position of the α2 helix of MHC class I is revealed by the crystal structure of HLA-B*3501. Immunity 4:203.
39. Sijts, A. J. A. M., and E. G. Pamer. 1997. Enhanced intracellular dissociation of major histocompatibility complex class I-associated peptides: a mechanism for optimizing the spectrum of cell surface-presented cytotoxic T lymphocyte epitopes. J. Exp. Med. 185:1403.
40. Hörig, H., N. J. Papadopoulos, Z. Vegh, E. Palmieri, R. H. Angeletti, and S. G. Nathenson. 1997. An in vitro study on the dynamic features of the major histocompatibility complex class I complex relevant to its role as a versatile peptide-receptive molecule. Proc. Natl. Acad. Sci. USA 94:13826.
41. b molecules are noncooperative. J. Immunol. 157:2256.
42. Rock, K. L., L. Rothstein, and B. Benacerraf. 1992. Analysis of the association of peptides of optimal length to class I molecules on the surface of cells. Proc. Natl. Acad. Sci. USA 89:8918.