1932

Abstract

In all human cells, human leukocyte antigen (HLA) class I glycoproteins assemble with a peptide and take it to the cell surface for surveillance by lymphocytes. These include natural killer (NK) cells and γδ T cells of innate immunity and αβ T cells of adaptive immunity. In healthy cells, the presented peptides derive from human proteins, to which lymphocytes are tolerant. In pathogen-infected cells, HLA class I expression is perturbed. Reduced HLA class I expression is detected by KIR and CD94:NKG2A receptors of NK cells. Almost any change in peptide presentation can be detected by αβ CD8+ T cells. In responding to extracellular pathogens, HLA class II glycoproteins, expressed by specialized antigen-presenting cells, present peptides to αβ CD4+ T cells. In comparison to the families of major histocompatibility complex (MHC) class I, MHC class II and αβ T cell receptors, the antigenic specificity of the γδ T cell receptors is incompletely understood.

Keyword(s): haplotypeHLAKIRlymphocytepolymorphismTCR
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-011520-102754
2020-06-20
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/biochem/89/1/annurev-biochem-011520-102754.html?itemId=/content/journals/10.1146/annurev-biochem-011520-102754&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Gorer PA. 1936. The detection of antigenic differences in mouse erythrocytes by the employment of immune sera. Br. J. Exp. Pathol. 17:142–50
    [Google Scholar]
  2. 2. 
    Gorer PA. 1937. The genetic and antigenic basis of tumour transplantation. J. Pathol. Bacteriol. 44:3691–97
    [Google Scholar]
  3. 3. 
    Gorer PA. 1937. Further studies on antigenic differences in mouse erythrocytes. Br. J. Exp. Pathol. 18:131–36
    [Google Scholar]
  4. 4. 
    Snell GD. 1948. Methods for the study of histocompatibility genes. J. Genet. 49:287–108
    [Google Scholar]
  5. 5. 
    Gorer PA, Lyman S, Snell GD 1948. Studies on the genetic and antigenic basis of tumour transplantation: linkage between a histocompatibility gene and “fused” in mice. Proc. R. Soc. B 135:881499–505
    [Google Scholar]
  6. 6. 
    Dausset J. 1984. The birth of MAC. Vox Sang 46:4235–37
    [Google Scholar]
  7. 7. 
    Payne R, Rolfs MR. 1958. Fetomaternal leukocyte incompatibility. J. Clin. Investig. 37:121756–63
    [Google Scholar]
  8. 8. 
    Payne R, Hackel E. 1961. Inheritance of human leukocyte antigens. Am. J. Hum. Genet. 13:306–19
    [Google Scholar]
  9. 9. 
    Van Rood JJ, Eernisse JG, Van Leeuwen A 1958. Leucocyte antibodies in sera from pregnant women. Nature 181:46251735–36
    [Google Scholar]
  10. 10. 
    Willcox BE, Willcox CR. 2019. γδ TCR ligands: the quest to solve a 500-million-year-old mystery. Nat. Immunol. 20:2121–28
    [Google Scholar]
  11. 11. 
    Braud VM, Allan DS, O'Callaghan CA, Söderström K, D'Andrea A et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:6669795–99
    [Google Scholar]
  12. 12. 
    Garcia-Beltran WF, Hölzemer A, Martrus G, Chung AW, Pacheco Y et al. 2016. Open conformers of HLA-F are high-affinity ligands of the activating NK-cell receptor KIR3DS1. Nat. Immunol. 17:91067–74
    [Google Scholar]
  13. 13. 
    Brown D, Trowsdale J, Allen R 2004. The LILR family: modulators of innate and adaptive immune pathways in health and disease. Tissue Antigens 64:3215–25
    [Google Scholar]
  14. 14. 
    Raulet DH. 2003. Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 3:10781–90
    [Google Scholar]
  15. 15. 
    Blum JS, Wearsch PA, Cresswell P 2013. Pathways of antigen processing. Annu. Rev. Immunol. 31:443–73
    [Google Scholar]
  16. 16. 
    Denzin LK, Fallas JL, Prendes M, Yi W 2005. Right place, right time, right peptide: DO keeps DM focused. Immunol. Rev. 207:279–92
    [Google Scholar]
  17. 17. 
    Cullen M, Perfetto SP, Klitz W, Nelson G, Carrington M 2002. High-resolution patterns of meiotic recombination across the human major histocompatibility complex. Am. J. Hum. Genet. 71:4759–76
    [Google Scholar]
  18. 18. 
    Yunis EJ, Larsen CE, Fernandez-Viña M, Awdeh ZL, Romero T et al. 2003. Inheritable variable sizes of DNA stretches in the human MHC: conserved extended haplotypes and their fragments or blocks. Tissue Antigens 62:11–20
    [Google Scholar]
  19. 19. 
    Abi-Rached L, Jobin MJ, Kulkarni S, McWhinnie A, Dalva K et al. 2011. The shaping of modern human immune systems by multiregional admixture with archaic humans. Science 334:605289–94
    [Google Scholar]
  20. 20. 
    Cheong KY, Allcock RJ, Eerligh P, Witt CS, Christiansen FT et al. 2001. Localization of central MHC genes influencing type I diabetes. Hum. Immunol. 62:121363–70
    [Google Scholar]
  21. 21. 
    Sollid LM, Thorsby E. 1993. HLA susceptibility genes in celiac disease: genetic mapping and role in pathogenesis. Gastroenterology 105:3910–22
    [Google Scholar]
  22. 22. 
    Christiansen FT, Zhang WJ, Griffiths M, Mallal SA, Dawkins RL 1991. Major histocompatibility complex (MHC) complement deficiency, ancestral haplotypes and systemic lupus erythematosus (SLE): C4 deficiency explains some but not all of the influence of the MHC. J. Rheumatol. 18:91350–58
    [Google Scholar]
  23. 23. 
    Horton R, Wilming L, Rand V, Lovering RC, Bruford EA et al. 2004. Gene map of the extended human MHC. Nat. Rev. Genet. 5:12889–99
    [Google Scholar]
  24. 24. 
    Harly C, Guillaume Y, Nedellec S, Peigné C-M, Mönkkönen H et al. 2012. Key implication of CD277/butyrophilin-3 (BTN3A) in cellular stress sensing by a major human γδ T-cell subset. Blood 120:112269–79
    [Google Scholar]
  25. 25. 
    Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC 1987. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329:6139512–18
    [Google Scholar]
  26. 26. 
    Neefjes J, Jongsma MLM, Paul P, Bakke O 2011. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 11:12823–36
    [Google Scholar]
  27. 27. 
    Koch J, Tampé R. 2006. The macromolecular peptide-loading complex in MHC class I-dependent antigen presentation. Cell. Mol. Life Sci. 63:6653–62
    [Google Scholar]
  28. 28. 
    Rock KL, Gamble S, Rothstein L 1990. Presentation of exogenous antigen with class I major histocompatibility complex molecules. Science 249:4971918–21
    [Google Scholar]
  29. 29. 
    Crotzer VL, Blum JS. 2010. Autophagy and adaptive immunity. Immunology 131:19–17
    [Google Scholar]
  30. 30. 
    van Agthoven A, Terhorst C, Reinherz E, Schlossman S 1981. Characterization of T cell surface glycoproteins T 1 and T 3 present on all human peripheral T lymphocytes and functionally mature thymocytes. Eur. J. Immunol. 11:118–21
    [Google Scholar]
  31. 31. 
    Borst J, Prendiville MA, Terhorst C 1982. Complexity of the human T lymphocyte-specific cell surface antigen T3. J. Immunol. 128:41560–65
    [Google Scholar]
  32. 32. 
    Borst J, Alexander S, Elder J, Terhorst C 1983. The T3 complex on human T lymphocytes involves four structurally distinct glycoproteins. J. Biol. Chem. 258:85135–41
    [Google Scholar]
  33. 33. 
    Kanellopoulos JM, Wigglesworth NM, Owen MJ, Crumpton MJ 1983. Biosynthesis and molecular nature of the T3 antigen of human T lymphocytes. EMBO J 2:101807–14
    [Google Scholar]
  34. 34. 
    Borst J, Prendiville MA, Terhorst C 1983. The T3 complex on human thymus-derived lymphocytes contains two different subunits of 20 kDa. Eur. J. Immunol. 13:7576–80
    [Google Scholar]
  35. 35. 
    Gaud G, Lesourne R, Love PE 2018. Regulatory mechanisms in T cell receptor signalling. Nat. Rev. Immunol. 18:8485–97
    [Google Scholar]
  36. 36. 
    Hesslein DG, Schatz DG. 2001. Factors and forces controlling V(D)J recombination. Adv. Immunol. 78:169–232
    [Google Scholar]
  37. 37. 
    Lefranc M-P, Lefranc G. 2001. The T Cell Receptor FactsBook San Diego: Elsevier413 pp.
  38. 38. 
    Satyanarayana K, Hata S, Devlin P, Roncarolo MG, De Vries JE et al. 1988. Genomic organization of the human T-cell antigen-receptor α/δ locus. PNAS 85:218166–70
    [Google Scholar]
  39. 39. 
    Lefranc MP, Giudicelli V, Ginestoux C, Bodmer J, Müller W et al. 1999. IMGT, the international ImMunoGeneTics database. Nucleic Acids Res 27:1209–12
    [Google Scholar]
  40. 40. 
    Elliott JF, Rock EP, Patten PA, Davis MM, Chien YH 1988. The adult T-cell receptor delta-chain is diverse and distinct from that of fetal thymocytes. Nature 331:6157627–31
    [Google Scholar]
  41. 41. 
    Arstila TP, Casrouge A, Baron V, Even J, Kanellopoulos J, Kourilsky P 1999. A direct estimate of the human αβ T cell receptor diversity. Science 286:5441958–61
    [Google Scholar]
  42. 42. 
    Davis MM, Bjorkman PJ. 1988. T-cell antigen receptor genes and T-cell recognition. Nature 334:6181395–402
    [Google Scholar]
  43. 43. 
    Littman DR. 1987. The structure of the CD4 and CD8 genes. Annu. Rev. Immunol. 5:561–84
    [Google Scholar]
  44. 44. 
    Norment AM, Salter RD, Parham P, Engelhard VH, Littman DR 1988. Cell-cell adhesion mediated by CD8 and MHC class I molecules. Nature 336:619479–81
    [Google Scholar]
  45. 45. 
    Doyle C, Strominger JL. 1987. Interaction between CD4 and class II MHC molecules mediates cell adhesion. Nature 330:6145256–59
    [Google Scholar]
  46. 46. 
    Anderson SJ, Levin SD, Perlmutter RM 1994. Involvement of the protein tyrosine kinase p56lck in T cell signaling and thymocyte development. Adv. Immunol. 56:151–78
    [Google Scholar]
  47. 47. 
    Treiner E, Duban L, Bahram S, Radosavljevic M, Wanner V et al. 2003. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 422:6928164–69
    [Google Scholar]
  48. 48. 
    Le Bourhis L, Martin E, Péguillet I, Guihot A, Froux N et al. 2010. Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol. 11:8701–8
    [Google Scholar]
  49. 49. 
    Beckman EM, Porcelli SA, Morita CT, Behar SM, Furlong ST, Brenner MB 1994. Recognition of a lipid antigen by CD1-restricted αβ+ T cells. Nature 372:6507691–94
    [Google Scholar]
  50. 50. 
    Van Rhijn I, Kasmar A, de Jong A, Gras S, Bhati M et al. 2013. A conserved human T cell population targets mycobacterial antigens presented by CD1b. Nat. Immunol. 14:7706–13
    [Google Scholar]
  51. 51. 
    Nielsen MM, Witherden DA, Havran WL 2017. γδ T cells in homeostasis and host defence of epithelial barrier tissues. Nat. Rev. Immunol. 17:12733–45
    [Google Scholar]
  52. 52. 
    Morita CT, Jin C, Sarikonda G, Wang H 2007. Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vγ2Vδ2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol. Rev. 215:59–76
    [Google Scholar]
  53. 53. 
    Tanaka Y, Sano S, Nieves E, De Libero G, Rosa D et al. 1994. Nonpeptide ligands for human γδ T cells. PNAS 91:178175–79
    [Google Scholar]
  54. 54. 
    Hintz M, Reichenberg A, Altincicek B, Bahr U, Gschwind RM et al. 2001. Identification of (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate as a major activator for human γδ T cells in Escherichia coli. FEBS Lett 509:2317–22
    [Google Scholar]
  55. 55. 
    Sandstrom A, Peigné C-M, Léger A, Crooks JE, Konczak F et al. 2014. The intracellular B30.2 domain of butyrophilin 3A1 binds phosphoantigens to mediate activation of human Vγ9Vδ2 T cells. Immunity 40:4490–500
    [Google Scholar]
  56. 56. 
    Vavassori S, Kumar A, Wan GS, Ramanjaneyulu GS, Cavallari M et al. 2013. Butyrophilin 3A1 binds phosphorylated antigens and stimulates human γδ T cells. Nat. Immunol. 14:9908–16
    [Google Scholar]
  57. 57. 
    Yang Y, Li L, Yuan L, Zhou X, Duan J et al. 2019. A structural change in butyrophilin upon phosphoantigen binding underlies phosphoantigen-mediated Vγ9Vδ2 T cell activation. Immunity 50:41043–53.e5
    [Google Scholar]
  58. 58. 
    Karunakaran MM, Göbel TW, Starick L, Walter L, Herrmann T 2014. Vγ9 and Vδ2 T cell antigen receptor genes and butyrophilin 3 (BTN3) emerged with placental mammals and are concomitantly preserved in selected species like alpaca (Vicugna pacos). Immunogenetics 66:4243–54
    [Google Scholar]
  59. 59. 
    Qin G, Liu Y, Zheng J, Ng IHY, Xiang Z et al. 2011. Type 1 responses of human Vγ9Vδ2 T cells to influenza A viruses. J. Virol. 85:1910109–16
    [Google Scholar]
  60. 60. 
    Fournié J-J, Sicard H, Poupot M, Bezombes C, Blanc A et al. 2013. What lessons can be learned from γδ T cell-based cancer immunotherapy trials. Cell. Mol. Immunol. 10:135–41
    [Google Scholar]
  61. 61. 
    Xiang Z, Liu Y, Zheng J, Liu M, Lv A et al. 2014. Targeted activation of human Vγ9Vδ2-T cells controls Epstein-Barr virus-induced B cell lymphoproliferative disease. Cancer Cell 26:4565–76
    [Google Scholar]
  62. 62. 
    Djaoud Z, Guethlein LA, Horowitz A, Azzi T, Nemat-Gorgani N et al. 2017. Two alternate strategies for innate immunity to Epstein-Barr virus: one using NK cells and the other NK cells and γδ T cells. J. Exp. Med. 214:61827–41
    [Google Scholar]
  63. 63. 
    Hochberg D, Middeldorp JM, Catalina M, Sullivan JL, Luzuriaga K, Thorley-Lawson DA 2004. Demonstration of the Burkitt's lymphoma Epstein-Barr virus phenotype in dividing latently infected memory cells in vivo. PNAS 101:1239–44
    [Google Scholar]
  64. 64. 
    Luoma AM, Castro CD, Adams EJ 2014. γδ T cell surveillance via CD1 molecules. Trends Immunol 35:12613–21
    [Google Scholar]
  65. 65. 
    Khairallah C, Déchanet-Merville J, Capone M 2017. γδ T cell-mediated immunity to cytomegalovirus infection. Front. Immunol. 8:105
    [Google Scholar]
  66. 66. 
    Pellicci DG, Uldrich AP, Le Nours J, Ross F, Chabrol E et al. 2014. The molecular bases of δ/αβ T cell-mediated antigen recognition. J. Exp. Med. 211:132599–615
    [Google Scholar]
  67. 67. 
    Allam A, Kabelitz D. 2006. TCR trans-rearrangements: biological significance in antigen recognition versus the role as lymphoma biomarker. J. Immunol. 176:105707–12
    [Google Scholar]
  68. 68. 
    Takada K, Takahama Y. 2015. Positive-selection-inducing self-peptides displayed by cortical thymic epithelial cells. Adv. Immunol. 125:87–110
    [Google Scholar]
  69. 69. 
    Stritesky GL, Jameson SC, Hogquist KA 2012. Selection of self-reactive T cells in the thymus. Annu. Rev. Immunol. 30:95–114
    [Google Scholar]
  70. 70. 
    Petrie HT, Scollay R, Shortman K 1992. Commitment to the T cell receptor-αβ or -γδ lineages can occur just prior to the onset of CD4 and CD8 expression among immature thymocytes. Eur. J. Immunol. 22:82185–88
    [Google Scholar]
  71. 71. 
    Haks MC, Lefebvre JM, Lauritsen JPH, Carleton M, Rhodes M et al. 2005. Attenuation of γδTCR signaling efficiently diverts thymocytes to the αβ lineage. Immunity 22:5595–606
    [Google Scholar]
  72. 72. 
    Hayes SM, Li L, Love PE 2005. TCR signal strength influences αβ/γδ lineage fate. Immunity 22:5583–93
    [Google Scholar]
  73. 73. 
    Lee N, Llano M, Carretero M, Ishitani A, Navarro F et al. 1998. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. PNAS 95:95199–204
    [Google Scholar]
  74. 74. 
    Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG 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. 187:5813–18
    [Google Scholar]
  75. 75. 
    Wagtmann N, Biassoni R, Cantoni C, Verdiani S, Malnati MS et al. 1995. Molecular clones of the p58 NK cell receptor reveal immunoglobulin-related molecules with diversity in both the extra- and intracellular domains. Immunity 2:5439–49
    [Google Scholar]
  76. 76. 
    Colonna M, Samaridis J. 1995. Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 268:5209405–8
    [Google Scholar]
  77. 77. 
    Carlyle JR, Mesci A, Fine JH, Chen P, Bélanger S et al. 2008. Evolution of the Ly49 and Nkrp1 recognition systems. Semin. Immunol. 20:6321–30
    [Google Scholar]
  78. 78. 
    Westgaard IH, Berg SF, Orstavik S, Fossum S, Dissen E 1998. Identification of a human member of the Ly-49 multigene family. Eur. J. Immunol. 28:61839–46
    [Google Scholar]
  79. 79. 
    Anfossi N, André P, Guia S, Falk CS, Roetynck S et al. 2006. Human NK cell education by inhibitory receptors for MHC class I. Immunity 25:2331–42
    [Google Scholar]
  80. 80. 
    Yawata M, Yawata N, Draghi M, Little A-M, Partheniou F, Parham P 2006. Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J. Exp. Med. 203:3633–45
    [Google Scholar]
  81. 81. 
    Yu J, Heller G, Chewning J, Kim S, Yokoyama WM, Hsu KC 2007. Hierarchy of the human natural killer cell response is determined by class and quantity of inhibitory receptors for self-HLA-B and HLA-C ligands. J. Immunol. 179:95977–89
    [Google Scholar]
  82. 82. 
    Horowitz A, Djaoud Z, Nemat-Gorgani N, Blokhuis J, Hilton HG et al. 2016. Class I HLA haplotypes form two schools that educate NK cells in different ways. Sci. Immunol. 1:3eaag1672
    [Google Scholar]
  83. 83. 
    Kulkarni S, Savan R, Qi Y, Gao X, Yuki Y et al. 2011. Differential microRNA regulation of HLA-C expression and its association with HIV control. Nature 472:7344495–98
    [Google Scholar]
  84. 84. 
    Battistini L, Borsellino G, Sawicki G, Poccia F, Salvetti M et al. 1997. Phenotypic and cytokine analysis of human peripheral blood gamma delta T cells expressing NK cell receptors. J. Immunol. 159:83723–30
    [Google Scholar]
  85. 85. 
    Anfossi N, Doisne J-M, Peyrat M-A, Ugolini S, Bonnaud O et al. 2004. Coordinated expression of Ig-like inhibitory MHC class I receptors and acquisition of cytotoxic function in human CD8+ T cells. J. Immunol. 173:127223–29
    [Google Scholar]
  86. 86. 
    van Bergen J, Kooy-Winkelaar EMC, van Dongen H, van Gaalen FA, Thompson A et al. 2009. Functional killer Ig-like receptors on human memory CD4+ T cells specific for cytomegalovirus. J. Immunol. 182:74175–82
    [Google Scholar]
  87. 87. 
    Valiante NM, Uhrberg M, Shilling HG, Lienert-Weidenbach K, Arnett KL et al. 1997. Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7:6739–51
    [Google Scholar]
  88. 88. 
    Vilches C, Parham P. 2002. KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu. Rev. Immunol. 20:217–51
    [Google Scholar]
  89. 89. 
    Döhring C, Scheidegger D, Samaridis J, Cella M, Colonna M 1996. A human killer inhibitory receptor specific for HLA-A1,2. J. Immunol. 156:93098–101
    [Google Scholar]
  90. 90. 
    Hansasuta P, Dong T, Thananchai H, Weekes M, Willberg C et al. 2004. Recognition of HLA-A3 and HLA-A11 by KIR3DL2 is peptide-specific. Eur. J. Immunol. 34:61673–79
    [Google Scholar]
  91. 91. 
    Cella M, Longo A, Ferrara GB, Strominger JL, Colonna M 1994. NK3-specific natural killer cells are selectively inhibited by Bw4-positive HLA alleles with isoleucine 80. J. Exp. Med. 180:41235–42
    [Google Scholar]
  92. 92. 
    Gumperz JE, Litwin V, Phillips JH, Lanier LL, Parham P 1995. 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. 181:31133–44
    [Google Scholar]
  93. 93. 
    Pando MJ, Gardiner CM, Gleimer M, McQueen KL, Parham P 2003. The protein made from a common allele of KIR3DL1 (3DL1*004) is poorly expressed at cell surfaces due to substitution at positions 86 in Ig domain 0 and 182 in Ig domain 1. J. Immunol. 171:126640–49
    [Google Scholar]
  94. 94. 
    Mulrooney TJ, Zhang AC, Goldgur Y, Boudreau JE, Hsu KC 2015. KIR3DS1-specific D0 domain polymorphisms disrupt KIR3DL1 surface expression and HLA binding. J. Immunol. 195:31242–50
    [Google Scholar]
  95. 95. 
    Saunders PM, Pymm P, Pietra G, Hughes VA, Hitchen C et al. 2016. Killer cell immunoglobulin-like receptor 3DL1 polymorphism defines distinct hierarchies of HLA class I recognition. J. Exp. Med. 213:5791–807
    [Google Scholar]
  96. 96. 
    Thananchai H, Gillespie G, Martin MP, Bashirova A, Yawata N et al. 2007. Cutting edge: allele-specific and peptide-dependent interactions between KIR3DL1 and HLA-A and HLA-B. J. Immunol. 178:133–37
    [Google Scholar]
  97. 97. 
    Sanjanwala B, Draghi M, Norman PJ, Guethlein LA, Parham P 2008. Polymorphic sites away from the Bw4 epitope that affect interaction of Bw4+ HLA-B with KIR3DL1. J. Immunol. 181:96293–300
    [Google Scholar]
  98. 98. 
    Fadda L, O'Connor GM, Kumar S, Piechocka-Trocha A, Gardiner CM et al. 2011. Common HIV-1 peptide variants mediate differential binding of KIR3DL1 to HLA-Bw4 molecules. J. Virol. 85:125970–74
    [Google Scholar]
  99. 99. 
    Biassoni R, Falco M, Cambiaggi A, Costa P, Verdiani S et al. 1995. Amino acid substitutions can influence the natural killer (NK)-mediated recognition of HLA-C molecules. Role of serine-77 and lysine-80 in the target cell protection from lysis mediated by “group 2” or “group 1” NK clones. J. Exp. Med. 182:2605–9
    [Google Scholar]
  100. 100. 
    Winter CC, Long EO. 1997. 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. 158:94026–28
    [Google Scholar]
  101. 101. 
    Moesta AK, Norman PJ, Yawata M, Yawata N, Gleimer M, Parham P 2008. Synergistic polymorphism at two positions distal to the ligand-binding site makes KIR2DL2 a stronger receptor for HLA-C than KIR2DL3. J. Immunol. 180:63969–79
    [Google Scholar]
  102. 102. 
    Fadda L, Borhis G, Ahmed P, Cheent K, Pageon SV et al. 2010. Peptide antagonism as a mechanism for NK cell activation. PNAS 107:2210160–65
    [Google Scholar]
  103. 103. 
    David G, Djaoud Z, Willem C, Legrand N, Rettman P et al. 2013. Large spectrum of HLA-C recognition by killer Ig-like receptor (KIR)2DL2 and KIR2DL3 and restricted C1 SPECIFICITY of KIR2DS2: dominant impact of KIR2DL2/KIR2DS2 on KIR2D NK cell repertoire formation. J. Immunol. 191:94778–88
    [Google Scholar]
  104. 104. 
    Bari R, Bell T, Leung W-H, Vong QP, Chan WK et al. 2009. Significant functional heterogeneity among KIR2DL1 alleles and a pivotal role of arginine 245. Blood 114:255182–90
    [Google Scholar]
  105. 105. 
    Hilton HG, Norman PJ, Nemat-Gorgani N, Goyos A, Hollenbach JA et al. 2015. Loss and gain of natural killer cell receptor function in an African hunter-gatherer population. PLOS Genet 11:8e1005439
    [Google Scholar]
  106. 106. 
    Gendzekhadze K, Norman PJ, Abi-Rached L, Graef T, Moesta AK et al. 2009. Co-evolution of KIR2DL3 with HLA-C in a human population retaining minimal essential diversity of KIR and HLA class I ligands. PNAS 106:4418692–97
    [Google Scholar]
  107. 107. 
    Bari R, Thapa R, Bao J, Li Y, Zheng J, Leung W 2016. KIR2DL2/2DL3-E(35) alleles are functionally stronger than -Q(35) alleles. Sci. Rep. 6:23689
    [Google Scholar]
  108. 108. 
    Hilton HG, Guethlein LA, Goyos A, Nemat-Gorgani N, Bushnell DA et al. 2015. Polymorphic HLA-C receptors balance the functional characteristics of KIR haplotypes. J. Immunol. 195:73160–70
    [Google Scholar]
  109. 109. 
    Morvan M, David G, Sébille V, Perrin A, Gagne K et al. 2008. Autologous and allogeneic HLA KIR ligand environments and activating KIR control KIR NK-cell functions. Eur. J. Immunol. 38:123474–86
    [Google Scholar]
  110. 110. 
    Liu J, Xiao Z, Ko HL, Shen M, Ren EC 2014. Activating killer cell immunoglobulin-like receptor 2DS2 binds to HLA-A*11. PNAS 111:72662–67
    [Google Scholar]
  111. 111. 
    Stewart CA, Laugier-Anfossi F, Vély F, Saulquin X, Riedmuller J et al. 2005. Recognition of peptide-MHC class I complexes by activating killer immunoglobulin-like receptors. PNAS 102:3713224–29
    [Google Scholar]
  112. 112. 
    Naiyer MM, Cassidy SA, Magri A, Cowton V, Chen K et al. 2017. KIR2DS2 recognizes conserved peptides derived from viral helicases in the context of HLA-C. Sci. Immunol. 2:15eaal5296
    [Google Scholar]
  113. 113. 
    Sim MJW, Rajagopalan S, Altmann DM, Boyton RJ, Sun PD, Long EO 2019. Human NK cell receptor KIR2DS4 detects a conserved bacterial epitope presented by HLA-C. PNAS 116:2612964–73
    [Google Scholar]
  114. 114. 
    Garcia CA, Robinson J, Guethlein LA, Parham P, Madrigal JA, Marsh SGE 2003. Human KIR sequences 2003. Immunogenetics 55:4227–39
    [Google Scholar]
  115. 115. 
    Wilson MJ, Torkar M, Haude A, Milne S, Jones T et al. 2000. Plasticity in the organization and sequences of human KIR/ILT gene families. PNAS 97:94778–83
    [Google Scholar]
  116. 116. 
    Parham P. 2005. MHC class I molecules and KIRs in human history, health and survival. Nat. Rev. Immunol. 5:3201–14
    [Google Scholar]
  117. 117. 
    Uhrberg M, Valiante NM, Shum BP, Shilling HG, Lienert-Weidenbach K et al. 1997. Human diversity in killer cell inhibitory receptor genes. Immunity 7:6753–63
    [Google Scholar]
  118. 118. 
    Maxwell LD, Wallace A, Middleton D, Curran MD 2002. A common KIR2DS4 deletion variant in the human that predicts a soluble KIR molecule analogous to the KIR1D molecule observed in the rhesus monkey. Tissue Antigens 60:3254–58
    [Google Scholar]
  119. 119. 
    Hollenbach JA, Nocedal I, Ladner MB, Single RM, Trachtenberg EA 2012. Killer cell immunoglobulin-like receptor (KIR) gene content variation in the HGDP-CEPH populations. Immunogenetics 64:10719–37
    [Google Scholar]
  120. 120. 
    Norman PJ, Hollenbach JA, Nemat-Gorgani N, Guethlein LA, Hilton HG et al. 2013. Co-evolution of human leukocyte antigen (HLA) class I ligands with killer-cell immunoglobulin-like receptors (KIR) in a genetically diverse population of sub-Saharan Africans. PLOS Genet 9:10e1003938
    [Google Scholar]
  121. 121. 
    Parham P, Norman PJ, Abi-Rached L, Guethlein LA 2012. Human-specific evolution of killer cell immunoglobulin-like receptor recognition of major histocompatibility complex class I molecules. Philos. Trans. R. Soc. B 367:1590800–11
    [Google Scholar]
  122. 122. 
    Parham P, Moffett A. 2013. Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat. Rev. Immunol. 13:2133–44
    [Google Scholar]
  123. 123. 
    Single RM, Martin MP, Gao X, Meyer D, Yeager M et al. 2007. Global diversity and evidence for coevolution of KIR and HLA. Nat. Genet. 39:91114–19
    [Google Scholar]
  124. 124. 
    Nemat-Gorgani N, Edinur HA, Hollenbach JA, Traherne JA, Dunn PPJ et al. 2014. KIR diversity in Māori and Polynesians: populations in which HLA-B is not a significant KIR ligand. Immunogenetics 66:11597–611
    [Google Scholar]
  125. 125. 
    Takeshita LYC, Gonzalez-Galarza FF, dos Santos EJM, Maia MHT, Rahman MM et al. 2013. A database for curating the associations between killer cell immunoglobulin-like receptors and diseases in worldwide populations. Database 2013.bat021
    [Google Scholar]
  126. 126. 
    King A, Burrows T, Loke YW 1996. Human uterine natural killer cells. Nat. Immun. 15:141–52
    [Google Scholar]
  127. 127. 
    Moffett A, Colucci F. 2015. Co-evolution of NK receptors and HLA ligands in humans is driven by reproduction. Immunol. Rev. 267:1283–97
    [Google Scholar]
  128. 128. 
    Hackmon R, Pinnaduwage L, Zhang J, Lye SJ, Geraghty DE, Dunk CE 2017. Definitive class I human leukocyte antigen expression in gestational placentation: HLA-F, HLA-E, HLA-C, and HLA-G in extravillous trophoblast invasion on placentation, pregnancy, and parturition. Am. J. Reprod. Immunol. 77:6e12643
    [Google Scholar]
  129. 129. 
    López-Botet M, Bellón T. 1999. Natural killer cell activation and inhibition by receptors for MHC class I. Curr. Opin. Immunol. 11:3301–7
    [Google Scholar]
  130. 130. 
    Rajagopalan S, Bryceson YT, Kuppusamy SP, Geraghty DE, van der Meer A et al. 2006. Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLOS Biol 4:1e9
    [Google Scholar]
  131. 131. 
    Vento-Tormo R, Efremova M, Botting RA, Turco MY, Vento-Tormo M et al. 2018. Single-cell reconstruction of the early maternal-fetal interface in humans. Nature 563:7731347–53
    [Google Scholar]
  132. 132. 
    Hiby SE, Walker JJ, O'Shaughnessy KM, Redman CWG, Carrington M et al. 2004. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 200:8957–65
    [Google Scholar]
  133. 133. 
    Hiby SE, Regan L, Lo W, Farrell L, Carrington M, Moffett A 2008. Association of maternal killer-cell immunoglobulin-like receptors and parental HLA-C genotypes with recurrent miscarriage. Hum. Reprod. 23:4972–76
    [Google Scholar]
  134. 134. 
    Hiby SE, Apps R, Sharkey AM, Farrell LE, Gardner L et al. 2010. Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J. Clin. Investig. 120:114102–10
    [Google Scholar]
  135. 135. 
    Xiong S, Sharkey AM, Kennedy PR, Gardner L, Farrell LE et al. 2013. Maternal uterine NK cell-activating receptor KIR2DS1 enhances placentation. J. Clin. Investig. 123:104264–72
    [Google Scholar]
  136. 136. 
    Nakimuli A, Chazara O, Hiby SE, Farrell L, Tukwasibwe S et al. 2015. A KIR B centromeric region present in Africans but not Europeans protects pregnant women from pre-eclampsia. PNAS 112:3845–50
    [Google Scholar]
  137. 137. 
    Hiby SE, Apps R, Chazara O, Farrell LE, Magnus P et al. 2014. Maternal KIR in combination with paternal HLA-C2 regulate human birth weight. J. Immunol. 192:115069–73
    [Google Scholar]
  138. 138. 
    Stewart-Jones GBE, McMichael AJ, Bell JI, Stuart DI, Jones EY 2003. A structural basis for immu-nodominant human T cell receptor recognition. Nat. Immunol. 4:7657–63
    [Google Scholar]
  139. 139. 
    Deng L, Langley RJ, Brown PH, Xu G, Teng L et al. 2007. Structural basis for the recognition of mutant self by a tumor-specific, MHC class II-restricted T cell receptor. Nat. Immunol. 8:4398–408
    [Google Scholar]
  140. 140. 
    Graef T, Moesta AK, Norman PJ, Abi-Rached L, Vago L et al. 2009. KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A*11 while diminishing avidity for HLA-C. J. Exp. Med. 206:112557–72
    [Google Scholar]
  141. 141. 
    Blokhuis JH, Hilton HG, Guethlein LA, Norman PJ, Nemat‐Gorgani N et al. 2017. KIR2DS5 allotypes that recognize the C2 epitope of HLA‐C are common among Africans and absent from Europeans. Immun. Inflamm. Dis. 5:4461–68
    [Google Scholar]
  142. 142. 
    Boyington JC, Motyka SA, Schuck P, Brooks AG, Sun PD 2000. Crystal structure of an NK cell immunoglobulin-like receptor in complex with its class I MHC ligand. Nature 405:6786537–43
    [Google Scholar]
  143. 143. 
    Robinson J, Halliwell JA, Hayhurst JD, Flicek P, Parham P, Marsh SGE 2015. The IPD and IMGT/HLA database: allele variant databases. Nucleic Acids Res 43:D423–31
    [Google Scholar]
/content/journals/10.1146/annurev-biochem-011520-102754
Loading
/content/journals/10.1146/annurev-biochem-011520-102754
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error