Structural features impose tight peptide binding specificity in the nonclassical MHC molecule HLA-E

Molecular Cell

Volumn 1, Issue 4, 1998, Pages 531-541

  O'Callaghan, Christopher A ^a   Tormo, José ^b,c,d   Willcox, Benjamin E ^a,b,c   Braud, Veronique M ^a   Jakobsen, Bent K ^a   Stuart, David I ^b,c   McMichael, Andrew J ^a   Bell, John I ^a   Jones, E Yvonne ^b,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HLA ANTIGEN; HLA ANTIGEN CLASS 1; HLA B8 ANTIGEN; HLA E ANTIGEN; HLA-E ANTIGEN; PEPTIDE FRAGMENT;

ARTICLE; CHEMISTRY; CRYSTALLOGRAPHY; HUMAN; HYDROGEN BOND; IMMUNOLOGY; METABOLISM; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

CRYSTALLOGRAPHY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HLA-B8 ANTIGEN; HUMANS; HYDROGEN BONDING; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 0032012455     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(00)80053-2     Document Type: Article

References (49)

1. Aldrich, C.J., DeCloux, A., Woods, A.S., Cotter, R.J., Soloski, M.J., and Forman, J. (1994). Identification of a Tap-dependent leader peptide recognized by alloreactive T cells specific for a class Ib antigen. Cell 79, 649-658.
2. Alvarez, M., Marinez-Laso, J., Varela, P., Diaz-Campos, N., Gomez-Casardo, E., Vargas-Alarcon, G., Garcia-Torre, C., and Arnaiz-Villena, A. (1997). High polymorphism of MHC-E locus in non human primates: alleles with identical exon 2 and 3 are found in two different species. Tissue Antigens 49, 160-167.
3. Bacon, D.J., and Anderson, W.F. (1988). A fast algorithm for rendering space filling molecule pictures. J. Mol. Graphics 6, 219-220.
4. Barnes, P.D., and Grundy, J.E. (1992). Down regulation of class I HLA heterodimer and beta 2-microglobulin on the surface of cells infected with cytomegalovirus. J. Gen. Virol. 73, 2395-2403.
5. Bjorkman, P.J., Saper, M.A., Samraoui, B., Bennett, W.S., Strominger, J.L., and Wiley, D.C. (1987a). Structure of the human class 1 histocompatibility antigen, HLA A2. Nature 329, 506-512.
6. Bjorkman, P.J., Saper, M.A., Samraoui, B., Bennett, W.S., Strominger, J.L., and Wiley, D.C. (1987b). The foreign antigen binding site and T cell recognition regions of class 1 histocompatibility antigens. Nature 329, 512-518.
7. Boyson, J.E., McAdam, S.N., Gallimore, A., Golos, T.G., Liu, X., Gotch, F.M., Hughes, A.L., and Watkins, D.I. (1995). The MHC-E locus in macaques is polymorphic and is conserved between macaques and humans. Immunogenetics 41, 59-68.
8. Braud, V.M., Jones, E.Y., and McMichael, A.J. (1997). The human major histocompatibility complex class Ib molecule HLA-E binds signal sequence derived peptides with primary anchor residues at positions 2 and 9. Eur. J. Immunol. 27, 1164-1169.
9. Braud, V., Allan, D.S., Wilson, D., and McMichael, A.J. (1998a). TAP and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Curr. Biol. 8, 1-10.
10. Braud, V.M., Allan, D.S.J., O'Callaghan, C.A., Soderstrom, K., Andrea, A.D., Ogg, G.S., Lazetic, S., Young, N.T., Bell, J.I., Phillips, J.H., Lanier, L.L., McMichael, A.J. (1998b). HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391, 795-799.
11. Brünger, A.T. (1992). XPLOR Version 3.1: a system for X-ray crystallography and NMR (New Haven, CT: Yale University Press).
12. Connolly, D.J., Coterill, L.A., Hederer, R.A., Thorpe, C.J., Travers, P.J., McVey, J.H., Dyson, J., and Robinson, P.J. (1993). A cDNA clone encoding the mouse Qa-1a histocompatibility antigen and proposed structure of the putative peptide binding site. J. Immunol. 151, 6089-6098.
13. Connolly, M.L. (1983). Solvent-accessible surfaces of proteins and nucleic acids. Science 221, 709-713.
14. Cotterill, L.A., Stauss, H.J., Millrain, M.M., Pappin, D.J.C., Rahman, D., Canas, B., Chandler, P., Stackpoole, A., Simpson, E., Robinson, P.J., and Dyson, P.J. (1997). Qa-1 interaction and T cell recognition of the Qa-1 determinant modifier peptide. Eur. J. Immunol. 27, 2123-2132.
15. DeCloux, A., Woods, A.S., Cotter, R.J., Soloski, M.J., and Forman, J. (1997). Dominance of a single peptide bound to the class Ib molecule Qa-1b. J. Immunol. 158, 2183-2191.
16. Esnouf, R.M. (1997). An extensively modified version of molscript which includes greatly enhanced colouring capabilities. J. Mol. Graphics 15, 132-134.
17. b. Science 257, 919-927.
18. Fruh, K., Ahn, K., Djaballah, H., Sempe, P., van Endert, P.M., Tampe, R., Peterson, P.A., and Yang, Y. (1995). A viral inhibitor of peptide transporters for antigen presentation. Nature 375, 415-418.
19. Gao, G.F., Tormo, J., Gerth, U.C., Wyer, J.R., McMichael, A.J., Stuart, D.I., Bell, J.I., Jones, E.Y., and Jakobsen, B.K. (1997). Crystal structure of the complex between CDS alpha-alpha and HLA-A2. Nature 387, 630-634.
20. Garboczi, D.N., Ghosh, P., Utz, U., Fan, Q.R., Biddison, W.E., and Wiley, D.C. (1996). Structure of the complex between the human T-cell receptor, viral peptide and HLA-A2. Nature 384, 134-141.
21. Garcia, K.C., Degano, M., Stanfield, R.L., Brunmark, A., Jackson, M.R., Peterson, P.A., Teyton, L., and Wilson, I.A. (1996). An alpha-beta T cell receptor structure at 2.5Å and its orientation in the TCR-MHC complex. Science 274, 209-219.
22. Garrett, T.P.J., Saper, M.A., Bjorkman, P.J., Strominger, J.L., and Wiley, D.C. (1989). Specificity pockets for the side chains of peptide antigens in HLA Aw68. Nature 342, 692-696.
23. Hubbard, S.J., Campbell, S.F., and Thornton, J.M. (1991). Molecular recognition: conformational analysis of limited proteolytic sites and serine proteinase protein inhibitors. J. Mol. Biol. 220, 507-530.
24. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst. A47, 110-119.
25. Kraulis, P.J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.
26. Kurepa, Z., and Forman, J. (1997). Peptide binding to the class Ib molecule Qa-1b. J. Immunol. 158, 3244-3251.
27. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. (1993). PROCHECK: a prog ram to check the stereochemical quality of protein structures. J. Appl. Cryst. 26, 283-291.
28. Loewenthal, R., Sancho, J., and Fersht, A.R. (1992). Histidine-aromatic interactions in barnase. Elevation of histidine pKa and contribution to protein stability. J. Mol. Biol. 224, 759-770.
29. Lowen, L.C., Aldrich, C.J., and Forman, J. (1993). Analysis of T cell receptors specific for recognition of class Ib antigens. J. Immunol. 151, 6155-6165.
30. Madden, D.R. (1995). The three-dimensional structure of peptide-MHC complexes. Annu. Rev. Immunol. 13, 587-622.
31. 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.
32. Madden, D.R., Gorga, J.C., Strominger, J.C., and Wiley, D.C. (1991). The structure of HLA-B27 reveals nonamer self peptides bound in an extended conformation. Nature 353, 321-325.
33. Merritt, E.A., and Murphy, M.E.P. (1994). Raster3D version 2.0. A program for photorealistic molecular graphics. Acta Cryst. D50, 869-873.
34. Navaza, J. (1994). AMoRe: an automated package for molecular replacement. Acta Cryst. A50, 157-163.
35. O'Callaghan, C.A., Tormo, J., Willcox, B.E., Blundell, C.D., Jakobsen, B.K., Stuart, D.I., McMichael, A.J., Bell, J.I., and Jones, E.Y. (1998). Production, crystallization and preliminary X-ray analysis of the human MHC class Ib molecule HLA-E. Prot. Sci., in press.
36. Otwinowski, Z., and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Meth. Enzymol. 276, 307-326.
37. Pamer, E.G., Wang, C.R., Flahert, L., Fishcer Lindahl, K., and Bevan, M.J. (1992). H-2M3 presents a Listeria monocytogenes peptide to CD8+ cytotoxic T lymphocytes. Cell 70, 215-223.
38. Perez-Villar, J.J., Melero, I., Navarro, F., Carretero, M., Bellon, T., Llano, M., Colonna, M., Geraghty, D.E., and Lopez-Botet, M. (1997). The CD94/NKG2-A inhibitory receptor complex is involved in natural killer cell-mediated recognition of cells expressing HLA-G1. J. Immunol. 158, 5736-5743.
39. Reid, S.W., McAdam, S., Smith, K.J., Klenerman, P., O'Callaghan, C.A., Harlos, K., Jakobsen, B.K., McMichael, A.J., Bell, J.I., Stuart, D.I., and Jones, E.Y. (1996). Antagonist HIV-1 Gag peptides induce structural changes in HLA B8. J. Exp. Med. 184, 2279-2286.
40. Saper, M.A., Bjorkman, P.J., and Wiley, D.C. (1991). Refined structure of human histocompatibility antigen HLA-A2 at 2.6 Angstrom resolution. J. Mol. Biol. 219, 277-319.
41. Shawar, S.M., Vyas, J.M., Rodgers, J.R., and Rich, R.R. (1994). Antigen presentation by major histocompatibility complex class Ib molecules. Annu. Rev. Immunol. 12, 839-880.
42. Smith, K.J., Reid, S.W., Stuart, D.I., McMichael, A.J., Jones, E.Y., and Bell, J.I. (1996a). An altered position of the alpha 2 helix of MHC class I is revealed by the crystal structure of HLA-B*3501. Immunity 4, 203-213.
43. Smith, K.J., Reid, S.W., Harlos, K., McMichael, A.J., Stuart, D.I., Bell, J.I., and Jones, E.Y. (1996b). Bound water structure and polymorphic amino acids act together to allow the binding of different peptides to MHC class I HLA-B53. Immunity 4, 215-228.
44. Stuart, D.I., Levine, M., Muirhead, M., and Stammers, D. (1979). The crystal structure of cat pyruvate kinase at a resolution of 2.6Å. J. Mol. Biol. 134, 109-142.
45. Townsend, A., and Bodmer, H. (1989). Antigen recognition by class-I restricted lymphocytes. Annu. Rev. Immunol. 7, 601-624.
46. Vidovic, D., Roglic, M., McKune, K., Guerder, S., MacKay, C., and Dembic, Z. (1989). Qa-1 restricted recognition of foreign antigen by a gamma-delta T-cell hybridoma. Nature 340, 646-648.
47. Wang, C.R., Castano, A.R., Peterson, P.A., Slaughter, C., Fischer Lindahl, K., and Deisenhofer, J. (1995). Nonclassical binding of formylated peptide in crystal structure of the MHC class Ib molecule H2-M3. Cell 82, 655-664.
48. b at 2.4Å resolution: implications for antigen-determinant selection. Cell 76, 39-50.
49. Zeng, Z.H., Castano, A.R., Segelke, B.W., Stura, E.A., Peterson, P.A., and Wilson, I.A. (1997). Crystal structure of mouse CD1: an MHC-like fold with a large hydrophobic binding groove. Science 277, 339-345.