Activating and Inhibitory NK Cell Receptors

  • Lewis L. Lanier
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 452)

Abstract

Kärre and colleagues observed that tumors lacking H-2 molecules were more susceptible to NK cell-mediated lysis than tumors expressing class I and proposed a unique mechanism of immune surveillance for ‘missing self’ (1). The molecular mechanism responsible for this phenomenon has been defined by the identification of membrane receptors on NK cells that bind to MHC class I on potential target cells. While the NK cell receptors initiating a cell-mediated response against tumors or virus-infected cells are not yet understood, killing of certain target cells can be partially or totally inhibited if the cells express MHC class I molecules that engage inhibitory receptors on the NK cell. Surprisingly, four distinct types of NK cell receptors for MHC class I that inhibit NK cell-mediated cytotoxicity have been identified.

Keywords

Natural Killer Cell Major Histocompatibility Complex Class Major Histocompatibility Complex Molecule Human Natural Killer Cell Natural Killer Cell Receptor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Karre K, Ljunggren HG, Piontek G, Kiessling R: Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defense strategy. Nature 319:675–678, 1986.PubMedCrossRefGoogle Scholar
  2. 2.
    Brown MG, Scalzo AA, Matsumoto K, Yokoyama WM: The natural killer gene complex: a genetic basis for understanding natural killer cell function and innate immunity. Immunol. Rev. 155:53–65, 1997.PubMedCrossRefGoogle Scholar
  3. 3.
    Kane KP: Ly-49 mediates EL4 lymphoma adhesion to isolated class I major histocompatibility complex molecules. J. Exp. Med. 179:1011–1015, 1994.PubMedCrossRefGoogle Scholar
  4. 4.
    Daniels B, Karlhofer FM, Seaman WE, Yokoyama WM: A natural killer cell receptor specific for a major histocompatibility complex class I molecule. J. Exp. Med. 180:687–692, 1994.PubMedCrossRefGoogle Scholar
  5. 5.
    Brennan J, Mahon G, Mager DL, Jefferies WA, Takei F: Recognition of class I major histocompatibility complex molecules by Ly-49: Specificities and domain interactions. J. Exp. Med. 183:1553–1559, 1996.PubMedCrossRefGoogle Scholar
  6. 6.
    Chang CS, Shen LJ, Gong DE, Kane KP: Major histocompatibility complex class I-dependent cell binding to isolated Ly-49A: Evidence for high-avidity interaction. Eur J Immunol 26:3219–3223, 1996.PubMedCrossRefGoogle Scholar
  7. 7.
    Matsumoto N, Ribaudo RK, Abastado J-P, Marguiles DH, Yokoyama WM: The lectin-like NK cell receptor Ly-49A recognizes a carbohydrate-independent epitope on its MHC class I ligand. Immunity 8:245–254, 1998.PubMedCrossRefGoogle Scholar
  8. 8.
    Daniels BF, Nakamura MC, Rosen SD, Yokoyama WM, Seaman WE: Ly-49A, a receptor for H-2Dd, has a functional carbohydrate recognition domain. Immunity 1:785–792, 1994.PubMedCrossRefGoogle Scholar
  9. 9.
    Brennan J, Takei F, Wong S, Mager DL: Carbohydrate recognition by a natural killer cell receptor, Ly-49C. J. Biol. Chem. 270:9691–9694, 1995.PubMedCrossRefGoogle Scholar
  10. 10.
    Orihuela M, Margulies DH, Yokoyama WM: The NK cell receptor Ly-49A recognizes a peptide-induced conformational determinant on its MHC class I ligand. Proc. Natl. Acad. Sci. USA 93:11792–11797, 1996.PubMedCrossRefGoogle Scholar
  11. 11.
    Correa I, Raulet DH: Binding of diverse peptides to MHC class I molecules inhibits target cell lysis by activated natural killer cells. Immunity 2:61–71, 1995.PubMedCrossRefGoogle Scholar
  12. 12.
    Chang C, Rodriguez A, Carretero M, Lopez-Botet M, Phillips JH, Lanier LL: Molecular characterization of human CD94: a type II membrane glycoprotein related to the C-type lectin superfamily. Eur. J. Immunol. 25:2433–2437, 1995.PubMedCrossRefGoogle Scholar
  13. 13.
    Houchins JP, Yabe T, McSherry C, Bach FH: DNA sequence analysis of NKG2, a family of related cDNA clones encoding type II integral membrane proteins on human natural killer cells. J. Exp. Med. 173:1017–1020, 1991.PubMedCrossRefGoogle Scholar
  14. 14.
    Dissen E, Ber SF, Westgaard IH, Fossum S: Molecular characterization of a gene in the rat homologous to human CD94. Eur. J. Immunol. 27:2080–2086, 1997.PubMedCrossRefGoogle Scholar
  15. 15.
    Vance RE, Tanamachi DM, Hanke T, Raulet DH: Cloning of a mouse homolog of CD94 extends the family of C-type lectins on murine natural killer cells. Eur. J. Immunol. 27:3236–3241, 1997.PubMedCrossRefGoogle Scholar
  16. 16.
    Berg SF, Dissen E, Westgaard IH, Fossum S: Two genes in the rat homologous to human NKG2. Eur. J. Immunol. 28:1998.Google Scholar
  17. 17.
    Braud VM, Allan DSJ, O’Callaghan CA, Soderstrom K, D’Andrea A, Ogg GS, Lazetic S, et al.: HLA-E binds to natural killer cell receptors CD94/NKG2A, B, and C. Nature 391:795–798, 1998.PubMedCrossRefGoogle Scholar
  18. 18.
    Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG: 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, 1998.PubMedCrossRefGoogle Scholar
  19. 19.
    Lee N, Llano M, Carretero M, Ishitani A, Navarro F, Lopez-Botet M, Geraghty DE: HLA-E is a major li-gand for the NK inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA In press, 1998.Google Scholar
  20. 20.
    Braud V, Jones EY, McMichael A: 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, 1997.PubMedCrossRefGoogle Scholar
  21. 21.
    Braud VM, Allan DSJ, Wilson D, McMichael AJ: TAP-and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Current Biology 8:1–10, 1998.PubMedCrossRefGoogle Scholar
  22. 22.
    Lee N, Goodlett DR, Ishitani A, Marquardt H, Geraghty DE: HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J. Immunol. In press, 1998.Google Scholar
  23. 23.
    Aldrich CJ, DeCloux A, Woods AS, Cotter RJ, Soloski MJ, Forman J: Identification of a TAP-dependent leader peptide recognized by alloreactive T cells specific for a class Ib antigen. Cell 79:649–658, 1994.PubMedCrossRefGoogle Scholar
  24. 24.
    Colonna M, Samaridis J: Cloning of Ig-superfamily members associated with HLA-C and HLA-B recognition by human NK cells. Science 268:405–408, 1995.PubMedCrossRefGoogle Scholar
  25. 25.
    Wagtmann N, Biassoni R, Cantoni C, Verdiani S, Malnati MS, Vitale M, Bottino C, et al.: Molecular clones of the p58 natural killer cell receptor reveal Ig-related molecules with diversity in both the extra-and intracellular domains. Immunity 2:439–449, 1995.PubMedCrossRefGoogle Scholar
  26. 26.
    D’Andrea A, Chang C, Franz-Bacon K, McClanahan T, Phillips JH, Lanier LL: Molecular cloning of NKB1: A natural killer cell receptor for HLA-B allotypes. J. Immunol. 155:2306–2310, 1995.PubMedGoogle Scholar
  27. 27.
    Wagtmann N, Rajagopalan S, Winter CC, Peruzzi M, Long EO: Killer cell inhibitory receptors specific for HLA-C and HLA-B identified by direct binding and by functional transfer. Immunity 3:801–809, 1995.PubMedCrossRefGoogle Scholar
  28. 28.
    Dohring C, Colonna M: Human natural killer cell inhibitory receptors bind to HLA class I molecules. Eur. J. Immunol. 26:365–369, 1996.PubMedCrossRefGoogle Scholar
  29. 29.
    Fan QR, Garboczi DN, Winter CC, Wagtmann N, Long EO, Wiley DC: 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, 1996.PubMedCrossRefGoogle Scholar
  30. 30.
    Rojo S, Wagtmann N, Long EO: Binding of a soluble p70 killer cell inhibitory receptor to HLA-B*5101: requirement for all three p70 immunoglobulin domains. Eur. J. Immunol. 27:568–571, 1997.PubMedCrossRefGoogle Scholar
  31. 31.
    Winter CC, Long EO: A single amino acid in the p58 killer cell inhibitory receptor controls the ability of natural killer cells to discriminate between the two groups of HLA-C allotypes. J. Immunol. 158:4026–4028, 1997.PubMedGoogle Scholar
  32. 32.
    Rajagopalan S, Long EO: The direct binding of a p58 killer cell inhibitory receptor to human histocompatibility leukocyte antigen (HLA)-Cw4 exhibits peptide specificity. J. Exp. Med. 185:1523–1528, 1997.PubMedCrossRefGoogle Scholar
  33. 33.
    Peruzzi M, Parker KC, Long EO, Malnati MS: Peptide sequence requirements for the recognition of HLA-B*2705 by specific natural killer cells. J. Immunol. 157:3350–3356, 1996.PubMedGoogle Scholar
  34. 34.
    Valiante NM, Lienert K, Shilling HG, Smits BJ, Parham P: Killer cell receptors: keeping pace with MHC class I evolution. Immunol. Rev. 155:155–164, 1997.PubMedCrossRefGoogle Scholar
  35. 35.
    Samaridis J, Colonna M: Cloning of novel immunoglobulin superfamily receptors expressed on human myeloid and lymphoid cells: structural evidence for new stimulatory and inhibitory pathways. Eur. J. Immunol. 27:660–665, 1997.PubMedCrossRefGoogle Scholar
  36. 36.
    Colonna M, Navarro F, Bellon T, Llano M, Garcia P, Samaridis J, Angman L, et al.: A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med. 186:1809–1818, 1997.PubMedCrossRefGoogle Scholar
  37. 37.
    Cosman D, Fanger N, Borges L, Kibin M, Chin W, Peterson L, Hus M-L: A novel immunoglobulin super-family receptor for cellular and viral MHC class I molecules. Immunity 7:273–282, 1997.PubMedCrossRefGoogle Scholar
  38. 38.
    Thomas ML: Of ITAMS and ITIMs: Turning on and off the B cell antigen receptor. J. Exp. Med. 181:1953–1956, 1995.PubMedCrossRefGoogle Scholar
  39. 39.
    Burshtyn DN, Scharenberg AM, Wagtmann N, Rajagopalan S, Berrada K, Yi T, Kinet J-P, et al.: Recruitment of tyrosine phosphatase HCP by the killer cell inhibitory receptor. Immunity 4:77–85, 1996.PubMedCrossRefGoogle Scholar
  40. 40.
    Fry A, Lanier LL, Weiss A: Phosphotyrosines in the KIR motif of NKB1 are required for negative signaling and for association with PTP1C. J. Exp. Med. 184:295–300, 1996.PubMedCrossRefGoogle Scholar
  41. 41.
    Olcese L, Lang P, Vely F, Cambiaggi A, Marguet D, Blery M, Hippen KL, et al.: Human and mouse killer-cell inhibitory receptors recruit PTP1C and PTP1D protein tyrosine phosphatases. J. Immunol. 156:4531–4534, 1996.PubMedGoogle Scholar
  42. 42.
    Campbell KS, Dessing M, Lopez-Botet M, Cella M, Colonna M: Tyrosine phosphorylation of a human killer inhibitory receptor recruits protein tyrosine phosphatase 1C. J. Exp. Med. 184:93–100, 1996.PubMedCrossRefGoogle Scholar
  43. 43.
    Binstadt BA, Brumbaugh KM, Dick CJ, Scharenberg AM, Williams BL, Colonna M, Lanier LL, et al.: Sequential Involvement of Lck and SHP-1 with MHC-Recognizing Receptors on NK Cells Inhibits FcR-Initi-ated Tyrosine Kinase Activation. Immunity 5:629–638, 1996.PubMedCrossRefGoogle Scholar
  44. 44.
    Valiante NM, Phillips JH, Lanier LL, Parham P: Killer cell inhibitory receptor recognition of human leukocyte antigen (HLA) class I blocks formation of a pp36/PLC-g signaling complex in human natural killer (NK) cells. J. Exp. Med. 184:2243–2250, 1996.PubMedCrossRefGoogle Scholar
  45. 45.
    Vely F, Olivero S, Olcese L, Moretta A, Damen JE, Liu L, Krystal G, et al.: Differential association of phosphatases with hematopoietic co-receptors bearing immunoreceptor tyrosine-based inhibition motifs. Eur. J. Immunol. 27:1994–2000, 1997.PubMedCrossRefGoogle Scholar
  46. 46.
    Le Drean E, Vely F, Olcese L, Cambiaggi A, Guia S, Krystal G, Gervois N, et al.: 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 phosphatase. Eur. J. Immunol. 28:264–276, 1998.PubMedCrossRefGoogle Scholar
  47. 47.
    Vaage JT, Dissen E, Ager A, Fossum S, Rolstad B: Allospecific recognition of hemic cells in vitro by natural killer cells from athymic rats: evidence that allodeterminants coded for by single major histocompatibility complex haplotypes are recognized. Eur. J. Immunol. 21:2167–2175, 1991.PubMedCrossRefGoogle Scholar
  48. 48.
    Rolstad B, Fossum S: Allogeneic lymphocyte cytotoxicity (ALC) in rats: establishment of an in vitro assay, and direct evidence that cells with natural killer (NK) activity are involved in ALC. Immunology 60:151–157, 1987.PubMedGoogle Scholar
  49. 49.
    Rolstad B, Fossum S: Non-adaptive cellular immune responses as studied in euthymic and athymic nude rats: Spontaneous rejection of allogeneic lymphoid cell grafts by natural killer (NK) cells. Anat. Embryol. 181:215–226,1990.PubMedCrossRefGoogle Scholar
  50. 50.
    Mason LH, Anderson SK, Yokoyama WM, Smith HRC, Winkler-Pickett R, Ortaldo JR: The Ly-49D receptor activates murine natural killer cells. J. Exp. Med. 184:2119–2128, 1996.PubMedCrossRefGoogle Scholar
  51. 51.
    Biassoni R, Cantoni C, Falco M, Verdiani S, Bottino C, Vitale M, Conte R, et al.: The human leukocyte antigen (HLA)-C-specific “activatory” or “inhibitory” natural killer cell receptors display highly homologous extracellular domains but differ in their transmembrane and intracytoplasmic portions. J. Exp. Med. 183:645–650, 1996.PubMedCrossRefGoogle Scholar
  52. 52.
    Moretta L, Sivori S, Vitale M, Pende D, Morelli L, Augugliaro R, Bottino C, et al.: Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J. Exp. Med. 182:875–884, 1995.PubMedCrossRefGoogle Scholar
  53. 53.
    Houchins JP, Lanier LL, Niemi E, Phillips JH, Ryan JC: Natural killer cell cytolytic activity is inhibited by NKG2-A and activated by NKG2-C. J. Immunol. 158:3603–3609, 1997.PubMedGoogle Scholar
  54. 54.
    Mason LH, Willette-Brown J, Anderson SK, Gosselin P, Shores EW, Love PE, Ortaldo JR, et al.: Characterization of an associated 16 kDA tyrosine phosphoprotein required for Ly-49D signal transduction. J. Immunol. In press, 1998.Google Scholar
  55. 55.
    Lanier LL, Corliss BC, Wu J, Leong C, Phillips JH: Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391:703–707, 1998.PubMedCrossRefGoogle Scholar
  56. 56.
    Valiante NM, Uhrberg M, Shilling HG, Lienert-Weidenbach K, Arnett KL, D’Andrea A, Phillips JH, et al.: Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7:739–751, 1997.PubMedCrossRefGoogle Scholar
  57. 57.
    Uhrberg M, Valiante NM, Shum BP, Shilling HG, Lienert-Weidenbach K, Corliss B, Tyan D, et al.: Human diversity in killer cell inhibitory receptor (KIR) genes. Immunity 7:753–763, 1997.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1998

Authors and Affiliations

  • Lewis L. Lanier
    • 1
  1. 1.Department of ImmunobiologyDNAX Research InstitutePalo AltoUSA

Personalised recommendations