Analysis of HLA-E peptide-binding specificity and contact residues in bound peptide required for recognition by CD94/NKG2

Journal of Immunology

Volumn 171, Issue 3, 2003, Pages 1369-1375

  Miller, Joseph D ^a   Weber, Dominique A ^a   Ibegbu, Chris ^a   Pohl, Jan ^a   Altman, John D ^a   Jensen, Peter E ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD94 ANTIGEN; HLA E ANTIGEN; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; SYNTHETIC PEPTIDE; T LYMPHOCYTE RECEPTOR;

AMINO ACID ANALYSIS; ANIMAL CELL; ANTIGEN BINDING; ARTICLE; CRYSTAL STRUCTURE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HLA SYSTEM; HUMAN; HUMAN CELL; IMMUNOASSAY; MAJOR HISTOCOMPATIBILITY COMPLEX; MONONUCLEAR CELL; NATURAL KILLER CELL; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; SPLEEN CELL; T LYMPHOCYTE SUBPOPULATION;

EID: 0041344437     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.3.1369     Document Type: Article

References (46)

1. Koller, B. H., D. E. Geraghty, Y. Shimizu, R. DeMars, and H. T. Orr. 1988. HLA-E: a novel HLA class I gene expressed in resting T lymphocytes. J. Immunol. 141:897.
2. Geraghty, D. E., M. Stockschleader, A. Ishitani, and J. A. Hansen. 1992. Polymorphism at the HLA-E locus predates most HLA-A and -B polymorphism. Hum. Immunol. 33:174.
3. Wei, X. H., and H. T. Orr. 1990. Differential expression of HLA-E, HLA-F, and HLA-G transcripts in human tissue. Hum. Immunol. 29:131.
4. Ulbrecht, M., T. Honka, S. Person, J. P. Johnson, and E. H. Weiss. 1992. The HLA-E gene encodes two differentially regulated transcripts and a cell surface protein. J. Immunol. 149:2945.
5. Braud, V., E. Y. Jones, and A. McMichael. 1997. The human major histocompatibility complex class lb molecule HLA-E binds signal sequence-derived peptides with primary anchor residues at positions 2 and 9. Eur. J. Immunol. 27:1164.
6. Braud, V. M., D. S. Allan, C. A. O'Callaghan, K. Soderstrom, A. D'Andrea, G. S. Ogg, S. Lazetic, N. T. Young, J. I. Bell, J. H. Phillips, et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:795.
7. Lee, N., M. Llano, M. Carretero, A. Ishitani, F. Navarro, M. Lopez-Botet, and D. E. Geraghty. 1998. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA 95:5199.
8. Lemberg, M. K., F. A. Bland, A. Weihofen, V. M. Braud, and B. Martoglio. 2001. Intramembrane proteolysis of signal peptides: an essential step in the generation of HLA-E epitopes. J. Immunol. 167:6441.
9. Braud, V. M., D. S. Allan, D. Wilson, and A. J. McMichael. 1998. TAP- and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Curr. Biol. 8:1.
10. Borrego, F., M. Ulbrecht, E. H. Weiss, J. E. Coligan, and A. G. Brooks. 1998. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J. Exp. Med. 187:813.
11. Moretta, L., R. Biassoni, C. Bottino, M. C. Mingari, and A. Moretta. 2000. Human NK-cell receptors. Immunol. Today 21:420.
12. Lopez-Botet, M., T. Bellon, M. Llano, F. Navarro, P. Garcia, and M. de Miguel. 2000. Paired inhibitory and triggering NK cell receptors for HLA class I molecules. Hum. Immunol. 61:7.
13. Lanier, L. L. 2000. Turning on natural killer cells. J. Exp. Med. 191:1259.
14. Michaelsson, J., C. Teixeira de Matos, A. Achour, L. L. Lanier, K. Karre, and K. Soderstrom. 2002. A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J. Exp. Med. 196:1403.
15. Karre, K., H. G. Ljunggren, G. Piontek, and R. Kiessling. 1986. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defense strategy. Nature 319:675.
16. Ljunggren, H. G., and K. Karre. 1990. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol. Today 11:237.
17. Llano, M., N. Lee, F. Navarro, P. Garcia, J. P. Albar, D. E. Geraghty, and M. Lopez-Botet. 1998. HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur. J. Immunol. 28:2854.
18. Vales-Gomez, M., H. T. Reyburn, R. A. Erskine, M. Lopez-Botet, and J. L. Strominger. 1999. Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/NKG2-C to HLA-E. EMBO J. 18:4250.
19. Brooks, A. G., F. Borrego, P. E. Posch, A. Patamawenu, C. J. Scorzelli, M. Ulbrecht, E. H. Weiss, and J. E. Coligan. 1999. Specific recognition of HLA-E, but not classical, HLA class I molecules by soluble CD94/NKG2A and NK cells. J. Immunol. 162:305.
20. Tomasec, P., V. M. Braud, C. Rickards, M. B. Powell, B. P. McSharry, S. Gadola, V. Cerundolo, L. K. Borysiewicz, A. J. McMichael, and G. W. Wilkinson. 2000. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287:1031.
21. Ulbrecht, M., S. Martinozzi, M. Grzeschik, H. Hengel, J. W. Ellwart, M. Pla, and E. H. Weiss. 2000. Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J. Immunol. 164:5019.
22. b. J. Exp. Med. 188:1841.
23. b by putative activating receptors CD94/NKG2C and CD94/NKG2E on mouse natural killer cells. J. Exp. Med. 190:1801.
24. b molecule binds to a large subpopulation of murine NK cells. Eur. J. Immunol. 28:4356.
25. Aldrich, C. J., A. DeCloux, A. S. Woods, R. J. Cotter, M. J. Soloski, and J. Forman. 1994. Identification of a Tap-dependent leader peptide recognized by alloreactive T cells specific for a class Ib antigen. Cell 79:649.
26. b peptide binding specificity and the capacity of CD94/NKG2A to discriminate between Qa-1-peptide complexes. J. Exp. Med. 192:613.
27. Pacasova, R., S. Martinozzi, H. J. Boulouis, M. Ulbrecht, J. C. Vieville, F. Sigaux, E. H. Weiss, and M. Pla. 1999. Cell-surface expression and alloantigenic function of a human nonclassical class I molecule (HLA-E) in transgenic mice. J. Immunol. 162:5190.
28. Pietra, G., C. Romagnani, M. Falco, M. Vitale, R. Castriconi, D. Pende, E. Millo, S. Anfossi, R. Biassoni, L. Moretta, and M. C. Mingari. 2001. The analysis of the natural killer-like activity of human cytolytic T lymphocytes revealed HLA-E as a novel target for TCR α/β-mediated recognition. Eur. J. Immunol. 31:3687.
29. Romagnani, C., G. Pietra, M. Falco, E. Millo, P. Mazzarino, R. Biassoni, A. Moretta, L. Moretta, and M. C. Mingari. 2002. Identification of HLA-E-specific alloreactive T lymphocytes: a cell subset that undergoes preferential expansion in mixed lymphocyte culture and displays a broad cytolytic activity against allogeneic cells. Proc. Natl. Acad. Sci. USA 99:11328.
30. Garcia, P., M. Llano. A. B. de Heredia, C. B. Willberg, E. Caparros, P. Aparicio, V. M. Braud, and M. Lopez-Botet. 2002. Human T cell receptor-mediated recognition of HLA-E. Eur. J. Immunol. 32:936.
31. + CTLs by TCR Vβ-derived peptides bound to HLA-E. J. Immunol. 167:3800.
32. + T cells. J. Exp. Med. 196:1473.
33. O'Callaghan, C. A., J. Tormo, B. E. Willcox, V. M. Braud, B. K. Jakobsen, D. I. Stuart, A. J. McMichael, J. I. Bell, and E. Y. Jones. 1998. Structural features impose tight peptide binding specificity in the nonclassical MHC molecule HLA-E. Mol. Cell 1:531.
34. Ulbrecht, M., S. Modrow, R. Srivastava, P. A. Peterson, and E. H. Weiss. 1998. Interaction of HLA-E with peptides and the peptide transporter in vitro: implications for its function in antigen presentation. J. Immunol. 160:4375.
35. Altman, J. D., P. A. Moss, P. J. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274:94.
36. Jensen, P. E., J. C. Moore, and A. E. Lukacher. 1998. A europium fluoroimmunoassay for measuring peptide binding to MHC class I molecules. J. Immunol. Methods 215:71.
37. Pohl, J. 1994. Sequence analysis of peptide resins from Boc/benzyl solid-phase synthesis. Methods Mol. Biol. 36:107.
38. Lee, N., D. R. Goodlett, A. Ishitani, H. Marquardt, and D. E. Geraghty. 1998. HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J. Immunol. 160:4951.
39. Gays, F., K. P. Fraser, J. A. Toomey, A. G. Diamond, M. M. Millrain, P. J. Dyson, and C. G. Brooks. 2001. Functional analysis of the molecular factors controlling Qa1-mediated protection of target cells from NK lysis. J. Immunol. 166:1601.
40. Stevens, J., E. Joly, J. Trowsdale, and G. W. Butcher. 2001. Peptide binding characteristics of the non-classical class Ib MHC molecule HLA-E assessed by a recombinant random peptide approach. BMC Immunol. 2:5.
41. Khakoo, S. I., R. Rajalingam, B. P. Shum, K. Weidenbach, L. Flodin, D. G. Muir, F. Canavez, S. L. Cooper, N. M. Valiante, L. L. Lanier, and P. Parham. 2000. Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 12:687.
42. Arnaiz-Villena, A., J. Martinez-Laso, M. Alvarez, M. J. Castro, P. Varela, E. Gomez-Casado, B. Suarez, M. J. Recio, G. Vargas-Alarcon, and P. Morales. 1997. Primate Mhc-E and -G alleles. Immunogenetics 46:251.
43. Boyson, J. E., S. N. McAdam, A. Gallimore, T. G. Golos, X. Liu, F. M. Gotch, A. L. Hughes, and D. I. Watkins. 1995. The MHC E locus in macaques is polymorphic and is conserved between macaques and humans. Immunogenetics 41:59.
44. Cooper, S., E. J. Adams, R. S. Wells, C. M. Walker, and P. Parham. 1998. A major histocompatibility complex class I allele shared by two species of chimpanzee. Immunogenetics 47:212.
45. Yeager, M., S. Kumar, and A. L. Hughes. 1997. Sequence convergence in the peptide-binding region of primate and rodent MHC class Ib molecules. Mol. Biol. Evol. 14:1035.
46. Trowsdale, J. 2001. Genetic and functional relationships between MHC and NK receptor genes. Immunity 15:363.