Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NIKG2-A and the activating receptor CD94/NKG2-C to HLA-E

EMBO Journal

Volumn 18, Issue 15, 1999, Pages 4250-4260

  Valés Gómez, Mar ^a   Reyburn, Hugh T ^b   Erskine, Robert A ^a   López Botet, Miguel ^c   Strominger, Jack L ^a  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

HLA E; Kinetics; NK receptors; Peptide dependence

Indexed keywords

CD94 ANTIGEN; HLA ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; RECOMBINANT PROTEIN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CYTOLYSIS; LIGAND BINDING; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING;

AMINO ACID SEQUENCE; ANTIGENS, CD; ANTIGENS, CD94; BASE SEQUENCE; CIRCULAR DICHROISM; DIMERIZATION; DNA, COMPLEMENTARY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; KILLER CELLS, NATURAL; KINETICS; LECTINS, C-TYPE; MEMBRANE GLYCOPROTEINS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN SORTING SIGNALS; RECEPTORS, IMMUNOLOGIC; RECOMBINANT PROTEINS; SURFACE PLASMON RESONANCE;

EID: 0345583696     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.15.4250     Document Type: Article

References (57)

1. Aramburu, J., Balboa, M.A., Ramirez, A., Silva, A., Acevedo, A., Sanchez-Madrid, F., De Landazuri, M.O. and Lopez-Botet, M. (1990) A novel functional cell surface dimer (Kp43) expressed by natural killer cells and T cell receptor-γ/δ+ T lymphocytes. I. Inhibition of the IL-2 dependent proliferation by anti-Kp43 monoclonal antibody. J. Immunol., 144, 3238-3247.
2. Bai, A., Broen, J. and Forman, J. (1998) The pathway for processing leader-derived peptides that regulate the maturation and expression of Qa-1b. Immunity, 9, 413-421.
3. Bell, G.I. (1978) Models for the specific adhesion of cells to cells. Science, 200, 618-627.
4. Borrego, F., Ulbrecht, M., Weiss, E.H., Coligan, J.E. and Brooks, A.G. (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, 813-818.
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. Boyington, J.C., Riaz, A.N., Patamawenu, A., Coligan, J.E., Brooks, A.G. and Sun, P.D. (1999) Structure of CD94 reveals a novel C-type lectin fold: implications for the NK cell-associated CD94/NKG2 receptors. Immunity, 10, 75-82.
7. Braud, V., Jones, E.Y. and McMichael, A. (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.
8. Braud, V.M. et al. (1998) HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature, 391, 795-799.
9. Brooks, A.G., Posch, P.E., Scorzelli, C.J., Borrego, F. and Coligan, J.E. (1997) NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J. Exp. Med., 185, 795-800.
10. Brooks, A.G., Borrego, F., Posch, P.E., Patamawenu, A., Scorzelli, C.J., Ulbrecht, M., Weiss, E.H. and Coligan, J.E. (1999) Specific recognition of HLA-E, but not classical, HLA class I molecules by soluble CD94/ NKG2A and NK cells. J. Immunol., 162, 305-313.
11. Brumbaugh, K.M., Binstadt, B.A., Billadeau, D.D., Schoon, R.A., Dick, C.J., Ten, R.M. and Leibson, P.J. (1997) Functional role for Syk tyrosine kinase in natural killer cell-mediated cytotoxicity. J. Exp. Med., 186, 1965-1974.
12. Bunce, M., Barnardo, M.C., Procter, J., Marsh, S.G., Vilches, C. and Welsh, K.I. (1997) High resolution HLA-C typing by PCR-SSP: identification of allelic frequencies and linkage disequilibria in 604 unrelated random UK Caucasoids and a comparison with serology [corrected and republished article originally printed in Tissue Antigens 1996 Dec; 48 (6): 680-91]. Tissue Antigens, 50, 100-111.
13. Carretero, M. et al. (1997) The CD94 and NKG2-A C-type lectins covalently assemble to form a natural killer cell inhibitory receptor for HLA class I molecules. Eur. J. Immunol., 27, 563-567.
14. Carretero, M., Palmieri, G., Llano, M., Tullio, V., Santoni, A., Geraghty, D.E. and Lopez-Botet, M. (1998) Specific engagement of the CD94/NKG2-A killer inhibitory receptor by the HLA-E class Ib molecule induces SHP-1 phosphatase recruitment to tyrosine-phosphorylated NKG2-A: evidence for receptor function in heterologous transfectants. Eur. J. Immunol., 28, 1280-1291.
15. Ciccone, E. et al. (1992) Involvement of HLA class I alleles in natural killer (NK) cell-specific functions: expression of HLA-Cw3 confers selective protection from lysis by alloreactive NK clones displaying a defined specificity (specificity 2). J. Exp. Med., 176, 963-971.
16. Cohen, G.B., Gandhi, R.T., Davis, D.M., Mandelboim, O., Chen, B.K., Strominger, J.L. and Baltimore, D. (1999) The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity, 10, 661-671.
17. Colonna, M. (1997) Specificity and function of immunoglobulin superfamily NK cell inhibitory and stimulatory receptors. Immunol. Rev., 155, 127-133.
18. Colonna, M., Borsellino, G., Falco, M., Ferrara, G.B. and Strominger, J.L. (1993) HLA-C is the inhibitory ligand that determines dominant resistance to lysis by NK1-and NK2-specific natural killer cells. Proc. Natl Acad. Sci. USA, 90, 12000-12004.
19. Dohring, C., Scheidegger, D., Samaridis, J., Cella, M. and Colonna, M. (1996) A human killer inhibitory receptor specific for HLA-A. J. Immunol., 156, 3098-3101.
20. Fan, Q.O.R., Garboczi, D.N., Winter, C.C., Wagtmann, N., Long, E.O. and Wiley, D.C. (1996) Direct binding of a soluble natural killer cell inhibitory receptor to a soluble human leukocyte antigen-Cw4 class I major histocompatibility complex molecule. Proc. Natl Acad. Sci. USA, 93, 7178-7183.
21. Garboczi, D.N., Hung, D.T. and Wiley, D.C. (1992) HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Escherichia coli and complexed with single antigenic peptides. Proc. Natl Acad. Sci. USA, 89, 3429-3433.
22. Houchins, J.P., Lanier, L.L., Niemi, E.C., Phillips, J.H. and Ryan, J.C. (1997) Natural killer cell cytolytic activity is inhibited by NKG2-A and activated by NKG2-C. J. Immunol., 158, 3603-3609.
23. Lanier, L.L. (1998a) Follow the leader: NK cell receptors for classical and nonclassical MHC class I. Cell, 92, 705-707.
24. Lanier, L.L. (1998b) NK cell receptors. Annu. Rev. Immunol., 16, 359-393.
25. Lanier, L.L., Corliss, B. and Phillips, J.H. (1997) Arousal and inhibition of human NK cells. Immunol. Rev., 155, 145-154.
26. Lanier, L.L., Corliss, B., Wu, J. and Phillips, J.H. (1998a) Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity, 8, 693-701.
27. Lanier, L.L., Corliss, B.C., Wu, J., Leong, C. and Phillips, J.H. (1998b) Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature, 391, 703-707.
28. Lazetic, S., Chang, C., Houchins, J.P., Lanier, L.L. and Phillips, J.H. (1996) Human natural killer cell receptors involved in MHC class I recognition are disulfide-linked heterodimers of CD94 and NKG2 subunits. J. Immunol., 157, 4741-4745.
29. Le Drean, E. et al. (1998) Inhibition of antigen-induced T cell response and antibody-induced NK cell cytotoxicity by NKG2A: association of NKG2A with SHP-1 and SHP-2 protein-tyrosine phosphatases. Eur. J. Immunol., 28, 264-276.
30. Lee, N., Goodlett, D.R., Ishitani, A., Marquardt, H. and Geraghty, D.E. (1998a) HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J. Immunol., 160, 4951-4960.
31. Lee, N., Llano, M., Carretero, M., Ishitani, A., Navarro, F., Lopez-Botet, M. and Geraghty, D.E. (1998b) HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl Acad. Sci. USA, 95, 5199-5204.
32. Le Gall, S., Erdtmann, L., Benichou, S., Berlioz-Torrent, C., Liu, L., Benarous, R., Heard, J.M. and Schwartz, O. (1998) Nef interacts with the mu subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules. Immunity, 8, 483-495.
33. Leibson, P.J. (1997) Signal transduction during natural killer cell activation: inside the mind of a killer. Immunity, 6, 655-661.
34. Llano, M., Lee, N., Navarro, F., Garcia, P., Albar, J.P., Geraghty, D.E. and Lopez-Botet, M. (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, 2854-2863.
35. McCutcheon, J.A., Gumperz, J., Smith, K.D., Lutz, C.T. and Parham, P. (1995) Low HLA-C expression at cell surfaces correlates with increased turnover of heavy chain mRNA. J. Exp. Med., 181, 2085-2095.
36. Moretta, A., Sivori, S., Vitale, M., Pende, D., Morelli, L., Augugliaro, R., Bottino, C. and Moretta, L. (1995) Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J. Exp. Med., 182, 875-884.
37. Moretta, A., Bottino, C., Vitale, M., Pende, D., Biassoni, R., Mingari, M.C. and Moretta, L. (1996) Receptors for HLA class-I molecules in human natural killer cells. Annu. Rev. Immunol., 14, 619-648.
38. Neefjes, J.J. and Ploegh, H.L. (1988) Allele and locus-specific differences in cell surface expression and the association of HLA class I heavy chain with beta 2-microglobulin: differential effects of inhibition of glycosylation on class I subunit association. Eur. J. Immunol., 18, 801-810.
39. Neisig, A., Melief, C.J. and Neefjes, J. (1998) Reduced cell surface expression of HLA-C molecules correlates with restricted peptide binding and stable TAP interaction. J. Immunol., 160, 171-179.
40. 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. (1998a) Production, crystallization and preliminary X-ray analysis of the human MHC class Ib molecule HLA-E. Protein Sci., 7, 1264-1266.
41. O'Callaghan, C.A., Tormo, J., Willcox, B.E., Braud, V.M., Jakobsen, B.K., Stuart, D.I., McMichael, A.J., Bell, J.I. and Jones, E.Y. (1998b) Structural features impose tight peptide binding specificity in the nonclassical MHC molecule HLA-E. Mol. Cell, 1, 531-541.
42. Olcese, L., Cambiaggi, A., Semenzato, G., Bottino, C., Moretta, A. and Vivier, E. (1997) Human killer cell activatory receptors for MHC class I molecules are included in a multimeric complex expressed by natural killer cells. J. Immunol., 158, 5083-5086.
43. Parham, P. (1997) NK cells, MHC Class I Antigens and Missing Self. Immunological Reviews. Vol. 155, Munksgaard, Copenhagen.
44. Pende, D. et al. (1996) The natural killer cell receptor specific for HLA-A allotypes: a novel member of the p58/p70 family of inhibitory receptors that is characterised by three immunoglobulin like domains and is expressed as a 140-kd disulphide linked dimer. J. Exp. Med., 184, 505-518.
45. Phillips, J.H., Chang, C., Mattson, J., Gumperz, J.E., Parham, P. and Lanier, L.L. (1996) CD94 and a novel associated protein (94AP) form a NK cell receptor involved in the recognition of HLA-A, HLA-B and HLA-C allotypes. Immunity, 5, 163-172.
46. Reid, S.W. et al. (1996) Production and crystallization of MHC class I B allele single peptide complexes. FEBS Lett., 383, 119-123.
47. Renard, V., Cambiaggi, A., Vely, F., Blery, M., Olcese, L., Olivero, S., Bouchet, M. and Vivier, E. (1997) Transduction of cytotoxic signals in natural killer cells: a general model of fine tuning between activatory and inhibitory pathways in lymphocytes. Immunol. Rev., 155, 205-221.
48. Schust, D.J., Tortorella, D., Seebach, J., Phan, C. and Ploegh, H.L. (1998) Trophoblast class I major histocompatibility complex (MHC) products are resistant to rapid degradation imposed by the human cytomegalovirus (HCMV) gene products US2 and US11. J. Exp. Med., 188, 497-503.
49. Sivori, S., Vitale, M., Bottino, C., Marcenaro, E., Sanseverino, L., Parolini, S., Moretta, L. and Moretta, A. (1996) CD94 functions as a natural killer cell inhibitory receptor for different HLA class I alleles: identification of the inhibitory form of CD94 by the use of novel monoclonal antibodies. Eur. J. Immunol., 26, 2487-2492.
50. Studier, F.W., Rosenburg, A.H., Dunn, J.J. and Dubendorff, J.W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol., 185, 60-89.
51. Ulbrecht, M., Modrow, S., Srivastava, R., Peterson, P.A. and Weiss, E.H. (1998) Interaction of HLA-E with peptides and the peptide transporter in vitro: implications for its function in antigen presentation. J. Immunol., 160, 4375-4385.
52. Valés-Gómez, M., Reyburn, H.T., Erskine, R.A. and Strominger, J.L. (1998a) Differential binding to HLA-C of p50-activating and p58-inhibitory natural killer cell receptors. Proc. Natl Acad. Sci. USA, 95, 14326-14331.
53. Valés-Gómez, M., Reyburn, H.T., Mandelboim, M. and Strominger, J.L. (1998b) Kinetics of interaction of HLA-C ligands with natural killer cell inhibitory receptors [published erratum appears in Immunity, 9, 892]. Immunity, 9, 337-344.
54. Vivier, E. and Daeron, M. (1997) Immunoreceptor tyrosine-based inhibition motifs. Immunol. Today, 18, 286-291.
55. Vyas, Y., Selvakumar, A., Steffens, U. and Dupont, B. (1998) Multiple transcripts of the killer cell immunoglobulin-like receptor family, KIR3DL1 (NKB1), are expressed by natural killer cells of a single individual. Tissue Antigens, 52, 510-519.
56. Wagtmann, N., Rajagopalan, S., Winter, C.C., Peruzzi, M. and Long, E.O. (1995) Killer cell inhibitory receptors specific for HLA-C and HLA-B identified by direct binding and functional transfer. Immunity, 3, 801-809.
57. Yokoyama, W. (1993) Recognition structures on natural killer cells. Curr. Opin. Immunol., 5, 67-73.