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Receptors for MHC Class I Molecules in Human Natural Killer Cells

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MHC Molecules: Expression, Assembly and Function

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Abstract

Natural Killer (NK) cells constitute a subset of lymphocytes characterized by distinct functions, cell-surface markers, and morphology (Table 14.1).1 Functionally, NK cells are viewed as a first line of defense against tumor growth and infections due to their ability to kill tumor cells and cells infected by intracellular pathogens without prior antigen sensitization.2–4 NK cells also regulate B and T cell immune responses. They kill IgG antibody-coated targets by antibody dependent cytotoxicity (ADCC) and produce cytokines, such as interferon (IFN)-γ, tumor necrosis factor (TNF)-α and granulocyte-macrophage colony-stimulating factor (GM-CSF).5 Phenotypically, NK cells express neither surface immunoglobulins nor T cell antigen receptors (TCRs). Human NK cells express CD566,7 and/or CD16 (FcγRIII), which is associated either with CD3ξ or with the γ chain of FcεRI.8–12 In addition, NK cells share some cell surface markers with T cells, such as CD2, CD7 and CD813 and develop from an immediate progenitor cell that is in common with T lymphocytes.14,15 Morphologically, mature NK cells correspond to a population of lymphocytes known as large granular lymphocytes (LGL).16,17

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References

  1. Trinchieri G. Biology of natural killer cells. Adv Immunol 1989; 47: 187–376.

    Article  Google Scholar 

  2. Herberman RB. Natural killer cells. Annu Rev Med 1986; 37: 347–52.

    Article  Google Scholar 

  3. Bancroft GJ. The role of natural killer cells in innate resistance to infection. Curr Opin Immunol 1993; 5: 503–10.

    Article  Google Scholar 

  4. Scott P, Trinchieri G. The role of natural killer cells in host-parasite interactions. Curr Opin Immunol 1995; 7: 34–40.

    Article  Google Scholar 

  5. Perussia B. Lymphokine-activated killer cells, natural killer cells and cytokines. Curr Opin Immunol 1991; 3: 49–55.

    Article  Google Scholar 

  6. Lanier LL, Testi R, Bindl J et al. Identity of Leu-19 (CD56) leukocyte differentiation antigen and neural cell adhesion molecule. J Exp Med 1989; 169: 2233–8.

    Article  Google Scholar 

  7. Lanier LL, Chang C, Azuma M et al. Molecular and functional analysis of human natural killer cell-associated neural cell adhesion molecule (NCAM/CD56). J Immunol 1991; 146: 4421–6.

    Google Scholar 

  8. Anderson P, Caligiuri M, Ritz J et al. CD3-negative natural killer cells express zeta TCR as part of a novel molecular complex. Nature 1989; 341: 159–62.

    Article  Google Scholar 

  9. Lanier LL, Yu G, Phillips JH. Co-association of CD3 zeta with a receptor (CD16) for IgG Fc on human natural killer cells. Nature 1989; 342: 803–5.

    Article  Google Scholar 

  10. Vivier E, Rochet N, Kochan JP et al. Structural similarity between Fc receptors and T cell receptors. Expression of the gamma-subunit of Fc epsilon RI in human T cells, natural killer cells and thymocytes. J Immunol 1991; 147: 4263–70.

    Google Scholar 

  11. Lanier LL, Yu G, Phillips JH. Analysis of Fc gamma RIII (CD16) membrane expression and association with CD3 zeta and Fc epsilon RI-gamma by site-directed mutation. J Immunol 1991; 146: 1571–6.

    Google Scholar 

  12. Letourneur O, Kennedy IC, Brini AT et al. Characterization of the family of dimers associated with Fc receptors (Fc epsilon RI and Fc gamma RIII). J Immunol 1991; 147: 2652–6.

    Google Scholar 

  13. Lanier LL, Phillips JH, Hackett J Jr et al. Natural killer cells: definition of a cell type rather than a function. J Immunol 1986; 137: 2735–9.

    Google Scholar 

  14. Rodewald HR, Moingeon P, Lucich JL et al. A population of early fetal thymocytes expressing Fc gamma RII/III contains precursors of T lymphocytes and natural killer cells. Cell 1992; 69: 139–50.

    Article  Google Scholar 

  15. Spits H, Lanier LL, Phillips JH. Development of human T and natural killer cells. Blood 1995; 85: 2654–70.

    Google Scholar 

  16. Saksela E, Timonen T, Ranki A et al. Morphological and functional characterization of isolated effector cells responsible for human natural killer activity to fetal fibroblasts and to cultured cell line targets. Immunol Rev 1979; 44: 71.

    Article  Google Scholar 

  17. Timonen T, Saksela E, Ranki A et al. Fractionation, morphological and functional characterization of effector cells responsible for human natural killer activity against cell line targets. Cell Immunol 1979; 48: 133.

    Article  Google Scholar 

  18. Karre K, Ljunggren HG, Piontek G et al. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 1986; 319: 675–8.

    Article  Google Scholar 

  19. Piontek GE, Taniguchi K, Ljunggren HG et al. YAC-1 MHC class I variants reveal an association between decreased NK sensitivity and increased H-2 expression after interferon treatment or in vivo passage. J Immunol 1985; 135: 4281–8.

    Google Scholar 

  20. Quillet A, Presse F, Marchiol Fournigault C et al. Increased resistance to non-MHC-restricted cytotoxicity related to HLA-A, -B expression. Direct demonstration using beta 2-microglobulin-transfected Daudi cells. J Immunol 1988; 141: 17–20.

    Google Scholar 

  21. Liao NS, Bix M, Zijlstra M et al. MHC class I deficiency: susceptibility to natural killer (NK) cells and impaired NK activity. Science 1991; 253: 199–202.

    Article  Google Scholar 

  22. Hoglund P, Ohlen C, Carbone E et al. Recognition of beta 2-microglobulin-negative (beta 2m-) T cell blasts by natural killer cells from normal but not from beta 2m-mice: nonresponsiveness controlled by beta 2m-bone marrow in chimeric mice. Proc Natl Acad Sci USA 1991; 88: 10332–6.

    Article  Google Scholar 

  23. Bix M, Liao NS, Zijlstra M et al. Rejection of class I MHC-deficient haemopoietic cells by irradiated MHC-matched mice. Nature 1991; 349: 329–31.

    Article  Google Scholar 

  24. Storkus WJ, Howell DN, Salter RD et al. NK susceptibility varies inversely with target cell class I HLA antigen expression. J Immunol 1987; 138: 1657–9.

    Google Scholar 

  25. Storkus WJ, Alexander J, Payne JA et al. The alpha 1/alpha 2 domains of class I HLA molecules confer resistance to natural killing. J Immunol 1989; 143: 3853–7.

    Google Scholar 

  26. Storkus WJ, Alexander J, Payne JA et al. Reversal of natural killing susceptibility in target cells expressing transfected class I HLA genes. Proc Natl Acad Sci USA 1989; 86: 2361–4.

    Article  Google Scholar 

  27. Ljunggren HG, Karre K. In search of the `missing self’: MHC molecules and NK cell recognition. Immunol Today 1990; 11: 237–44.

    Google Scholar 

  28. Storkus WJ, Dawson JR. Target structures involved in natural killing (NK): characteristics, distribution, and candidate molecules. Crit Rev Immunol 1991; 10: 393–416.

    Google Scholar 

  29. Yokoyama WM. Recognition structures on natural killer cells. Curr Opin Immunol 1993; 5: 67–73.

    Article  Google Scholar 

  30. Yokoyama WM. Natural Killer cell receptors. Current Opinion in Immunology 1995; 7: 110–20.

    Article  Google Scholar 

  31. Karlhofer FM, Ribaudo RK, Yokoyama WM. MHC class I alloantigen specificity of Ly-49+ IL-2-activated natural killer cells. Nature 1992; 358: 66–70.

    Article  Google Scholar 

  32. Kane KP. Ly-49 mediates EL4 lymphoma adhesion to isolated class I major histocompatibility complex molecules. J Exp Med 1994; 179: 1011–5.

    Article  Google Scholar 

  33. Daniels BF, Karlhofer FM, Seaman WE et al. A natural killer cell receptor specific for a major histocompatibility complex class I molecule. J Exp Med 1994; 180: 687–92.

    Article  Google Scholar 

  34. Karlhofer FM, Hunziker R, Reichlin A et al. Host MHC class I molecules modulate in vivo expression of a NK cell receptor. J Immunol 1994; 15 3: 2407–16.

    Google Scholar 

  35. Daniels BF, Nakamura MC, Rosen SD et al. Ly-49A, a receptor for H-2Dd, has a functional carbohydrate recognition domain. Immunity 1994; 1: 785–92.

    Article  Google Scholar 

  36. Yokoyama WM, Ryan JC, Hunter JJ et al. cDNA cloning of mouse NKR-P1 and genetic linkage with Ly-49. Identification of a natural killer cell gene complex on mouse chromosome 6. J Immunol 1991; 147: 3229–36.

    Google Scholar 

  37. Yokoyama WM, Seaman WE. The Ly-49 and NKR-P1 gene families encoding lectin-like receptors on natural killer cells: the NK gene complex. Annu Rev Immunol 1993; 11: 613–35.

    Article  Google Scholar 

  38. Sentman CL, Hackett J Jr, Kumar V et al. Identification of a subset of murine natural killer cells that mediates rejection of Hh-Id but not Hh-lb bone marrow grafts. J Exp Med 1989; 170: 191–202.

    Article  Google Scholar 

  39. Stoneman E, Kumar V, Bennett M. Molecular cloning of an NK cell surface molecule expressed on a subset of cells that mediate specific rejection of Hh-Pi positive marrow cells. J Immunol 1993; 150: 257a.

    Google Scholar 

  40. Cudkowicz G. The immunogenetic basis of hybrid resistance to parental marrow grafts. In: Palm J, ed. Isoantigens and Cell Interactions. Philadelphia: Wistar Inst. Press; 1965: 37.

    Google Scholar 

  41. Bennett M. Biology and genetics of hybrid resistance. Adv Immunol 1987; 41: 333–445.

    Article  Google Scholar 

  42. Ohlen C, Kling G, Hoglund P et al. Prevention of allogeneic bone marrow graft rejection by H-2 transgene in donor mice. Science 1989; 246: 666–8.

    Article  Google Scholar 

  43. Mason L, Giardina SL, Hecht T et al. LGL-1: a non-polymorphic antigen expressed on a major population of mouse natural killer cells. J Immunol 1988; 140: 4403–12.

    Google Scholar 

  44. Mason LH, Mathieson BJ, Ortaldo JR. Natural killer (NK) cell subsets in the mouse. NK-1.1+/LGL-1+ cells restricted to lysing NK targets, whereas NK-1.1+/LGL-1- cells generate lymphokine-activated killer cells. J Immunol 1990; 145: 751–9.

    Google Scholar 

  45. Mason LH, Yagita H, Ortaldo JR. LGL-1: a potential triggering molecule on murine NK cells. J Leukoc Biol 1994; 55: 362–70.

    Google Scholar 

  46. Mason LM, Young HA, Ortaldo JR, Anderson SA. Cloning of LGL-1. Nat Immun 1994; 13: 221.

    Google Scholar 

  47. Moretta A, Tambussi G, Bottino C et al. A novel surface antigen expressed by a subset of human CD3- CD16+ natural killer cells. Role in cell activation and regulation of cytolytic function. J Exp Med 1990; 171: 695–714.

    Article  Google Scholar 

  48. Moretta A, Bottino C, Pende D et al. Identification of four subsets of human CD3–CD16+ natural killer (NK) cells by the expression of clonally distributed functional surface molecules: correlation between subset assignment of NK clones and ability to mediate specific alloantigen recognition. J Exp Med 1990; 172: 1589–98.

    Article  Google Scholar 

  49. Colonna M, Spies T, Strominger JL et al. Alloantigen recognition by two human natural killer cell clones is associated with HLA-C or a closely linked gene. Proc Natl Acad Sci USA 1992; 89: 7983–5.

    Article  Google Scholar 

  50. Ciccone E, Pende D, Viale O et al. 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 1992; 176: 963–71.

    Article  Google Scholar 

  51. Colonna M, Borsellino G, Falco M et al. 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 1993; 90: 12000–4.

    Article  Google Scholar 

  52. Moretta A, Vitale M, Bottino C et al. P58 molecules as putative receptors for major histocompatibility complex (MHC) class I molecules in human natural killer (NK) cells. Anti-p58 antibodies reconstitute lysis of MHC class I-protected cells in NK clones displaying different specificities. J Exp Med 1993; 178: 597–604.

    Article  Google Scholar 

  53. Melero I, Salmeron A, Balboa MA et al. Tyrosine kinase-dependent activation of human NK cell functions upon stimulation through a 58-kDa surface antigen selectively expressed on discrete subsets of NK cells and T lymphocytes. J Immunol 1994; 152: 1662–73.

    Google Scholar 

  54. Lanier LL, Gumperz JE, Parham P et al. The NKB1 and HP-3E4 NK cells receptors are structurally distinct glycoproteins and independently recognize polymorphic HLA-B and HLA-C molecules. J Immunol 1995; 154: 3320–7.

    Google Scholar 

  55. Litwin V, Gumperz J, Parham P et al. Specificity of HLA class I antigen recognition by human NK clones: evidence for clonal heterogeneity, protection by self and non-self alleles, and influence of the target cell type. J Exp Med 1993; 178: 1321–36.

    Article  Google Scholar 

  56. Litwin V, Gumperz J, Parham P et al. NKB1: a natural killer cell receptor involved in the recognition of polymorphic HLA-B molecules. J Exp Med 1994; 180: 537–43.

    Article  Google Scholar 

  57. Cella M, Longo A, Ferrara GB et al. NK3-specific natural killer cells are selectively inhibited by Bw4-positive HLA alleles with isoleucine 80. J Exp Med 1994; 180: 1235–42.

    Article  Google Scholar 

  58. Gumperz JE, Litwin V, Phillips JH et al. The Bw4 public epitope of HLA-B molecules confers reactivity with natural killer cell clones that express NKB1, a putative HLA receptor. J Exp Med 1995; 181: 1133–44.

    Article  Google Scholar 

  59. Wagtmann N, Biassoni N, Cantoni C et al. Molecular clones of the p58 NK cell receptor reveal immunoglobulin-related molecules with diversity in both extra-and intracellular domains. Immunity 1995; 2: 439–49.

    Article  Google Scholar 

  60. Kornbluth J, Flomenberg N, Dupont B. Cell surface phenotype of a cloned line of human natural killer cells. J Immunol 1982; 129: 2831–7.

    Google Scholar 

  61. Colonna M, Samaridis J. Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 1995; 268: 405–8.

    Article  Google Scholar 

  62. Maliszewski CR, March CJ, Schoenborn MA, Gimpel S, Shen L. Expression cloning of a human Fc receptor for IgA. J Exp Med 1990; 172: 1665–72.

    Article  Google Scholar 

  63. Arm JP, Gurish MF, Reynolds DS et al. Molecular cloning of gp49, a cell-surface antigen that is preferentially expressed by mouse mast cell progenitors and is a new member of the immunoglobulin superfamily. J Biol Chem 1991; 266: 15966–73.

    Google Scholar 

  64. Weiss A, Littman DR. Signal transduction by lymphocyte antigen receptors. Cell 1994; 76: 263–74.

    Article  Google Scholar 

  65. Thomas ML. Of ITAMs and ITIMs: turning on and off the B cell antigen receptor. J Exp Med 1995; 181: 1953–6.

    Article  Google Scholar 

  66. Max EE. Immunoglobulins: Molecular Genetics. In: Paul WE, ed. Fundamental Immunology. New York: Raven Press Ltd.; 1989: 235–90.

    Google Scholar 

  67. Davis MM. T cell receptor gene diversity and selection. Annu Rev Biochem 1990; 59: 475–96.

    Article  Google Scholar 

  68. Aramburu J, Balboa MA, Ramirez A et al. A novel functional cell surface dimer (Kp43) expressed by natural killer cells and T cell receptor-gamma/ delta+ T lymphocytes. I. Inhibition of the IL-2-dependent proliferation by anti-Kp43 monoclonal antibody. J Immunol 1990; 144: 3238–47.

    Google Scholar 

  69. Moretta A, Vitale M, Sivori S et al. Human natural killer cell receptors for HLA-class I molecules. Evidence that the Kp43 (CD94) molecule functions as receptor for HLA-B alleles. J Exp Med 1994; 180: 545–55.

    Article  Google Scholar 

  70. Lopez-Botet M. Structure and function of the CD94 NK cell lectin-like receptor. In: Lanzavecchia A, Arnold B, eds. ENII Conference 1995. Les Embiez, France: European Network of Immunology Institutes; 1995: 159.

    Google Scholar 

  71. Houchins JP, Yabe T, McSherry C et al. Isolation and characterization of NK cell or NK/T cell-specific cDNA clones. J Mol Cell Immunol 1990; 4: 295–304.

    Google Scholar 

  72. Yabe T, McSherry C, Bach FH et al. A multigene family on human chromosome 12 encodes natural killer-cell lectins. Immunogenetics 1993; 37: 455–60.

    Article  Google Scholar 

  73. Correa I, Raulet DH. Binding of diverse peptides to MHC class I molecules inhibits target cell lysis by activated Natural Killer cells. Immunity 1995; 2: 61–71.

    Article  Google Scholar 

  74. Storkus WJ, Salter RD, Alexander J et al. Class I-induced resistance to natural killing: identification of nonpermissive residues in HLA-A2. Proc Natl Acad Sci USA 1991; 88: 5989–92.

    Article  Google Scholar 

  75. Storkus WJ, Salter RD, Cresswell P et al. Peptide-induced modulation of target cell sensitivity to natural killing. J Immunol 1992; 149: 1185–90.

    Google Scholar 

  76. Chadwick BS, Sambhara SR, Sasakura Y et al. Effect of class I MHC binding peptides on recognition by natural killer cells. J Immunol 1992; 149: 3150–6.

    Google Scholar 

  77. Malnati MS, Peruzzi M, Parker KC et al. Peptide specificity in the recognition of MHC class I by natural killer cell clones. Science 1995; 267: 1016–8.

    Article  Google Scholar 

  78. De Magistris MT, Alexander J, Coggeshall M et al. Antigen analog-major histocompatibility complexes act as antagonists of the T cell receptor. Cell 1992; 68: 625–34.

    Article  Google Scholar 

  79. Ravetch JV, Kinet JP. Fc receptors. Annu Rev Immunol 1991; 9: 457–92.

    Article  Google Scholar 

  80. Bottino C, Vitale M, Olcese L et al. The human natural killer cell receptor for major histocompatibility complex class I molecules. Surface modulation of p58 molecules and their linkage to CD3 zeta chain, Fc epsilon RI gamma chain and the p561ck kinase. Eur J Immunol 1994; 24: 2527–34.

    Article  Google Scholar 

  81. Amigorena S, Bonnerot C, Drake JR et al. Cytoplasmic domain heterogeneity and functions of IgG Fc receptors in B lymphocytes. Science 1992; 256: 1808–12.

    Article  Google Scholar 

  82. Muta T, Kurosaki T, Misulovin Z et al. A 13-amino-acid motif in the cytoplasmic domain of Fc gamma RIIB modulates B cell receptor signalling. Nature 1994; 369: 340.

    Google Scholar 

  83. D’Ambrosio D, Hippen KH, Minskoff SA et al. Recruitment and activation of PTPIC in negative regulation of antigen receptor signaling by F y RIIBI. Science 1995; 268: 293–7.

    Article  Google Scholar 

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Colonna, M. (1996). Receptors for MHC Class I Molecules in Human Natural Killer Cells. In: MHC Molecules: Expression, Assembly and Function. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-6462-7_14

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  • DOI: https://doi.org/10.1007/978-1-4684-6462-7_14

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-6464-1

  • Online ISBN: 978-1-4684-6462-7

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