Complexity and diversity of the NKR-P1: Clr (Klrb1: Clec2) recognition systems

Frontiers in Immunology

Volumn 5, Issue JUN, 2014, Pages

  Kirkham, Christina L ^a   Carlyle, James R ^a  

^a Canada   (Canada)

Author keywords

C type lectin like; CD161; Clr; Innate immunity; LLT1; Natural killer cell; Nkrp1; Ocil

Indexed keywords

EID: 84905671445     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00214     Document Type: Review

References (156)

1. Lanier LL. NK cell recognition. Annu Rev Immunol (2005) 23:225-74. doi: 10.1146/annurev.immunol.23.021704.115526
2. Karre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature (1986) 319:675-8. doi:10.1038/319675a0
3. Raulet DH, Vance RE. Self-tolerance of natural killer cells. Nat Rev Immunol (2006) 6:520-31. doi:10.1038/nri1863
4. Orr MT, Lanier LL. Natural killer cell education and tolerance. Cell (2010) 142:847-56. doi:10.1016/j.cell.2010.08.031
5. 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. doi:10.1146/annurev.immunol.11.1.613
6. Dissen E, Ryan JC, Seaman WE, Fossum S. An autosomal dominant locus, Nka, mapping to the Ly-49 region of a rat natural killer (NK) gene complex, controls NK cell lysis of allogeneic lymphocytes. J Exp Med (1996) 183:2197-207. doi:10.1084/jem.183.5.2197
7. Hao L, Klein J, Nei M. Heterogeneous but conserved natural killer receptor gene complexes in four major orders of mammals. Proc Natl Acad Sci U S A (2006) 103:3192-7. doi:10.1073/pnas.0511280103
8. Rogers SL, Gobel TW, Viertlboeck BC, Milne S, Beck S, Kaufman J. Characterization of the chicken C-type lectin-like receptors B-NK and B-lec suggests that the NK complex and the MHC share a common ancestral region. J Immunol (2005) 174:3475-83. doi:10.4049/jimmunol.174.6.3475
9. Wagtmann N, Rojo S, Eichler E, Mohrenweiser H, Long EO. A new human gene complex encoding the killer cell inhibitory receptors and related monocyte/macrophage receptors. Curr Biol (1997) 7:615-8. doi:10.1016/S0960-9822(06)00263-6
10. Wende H, Colonna M, Ziegler A, Volz A. Organization of the leukocyte receptor cluster (LRC) on human chromosome 19q13.4. Mamm Genome (1999) 10:154-60. doi:10.1007/s003359900961
11. Trowsdale J. Genetic and functional relationships between MHC and NK receptor genes. Immunity (2001) 15:363-74. doi:10.1016/S1074-7613(01)00197-2
12. Martin AM, Kulski JK, Witt C, Pontarotti P, Christiansen FT. Leukocyte Ig-like receptor complex (LRC) in mice and men. Trends Immunol (2002) 23:81-8. doi:10.1016/S1471-4906(01)02155-X
13. Dong Z, Veillette A. How do SAP family deficiencies compromise immunity? Trends Immunol (2010) 31:295-302. doi:10.1016/j.it.2010.05.008
14. Cannons JL, Tangye SG, Schwartzberg PL. SLAM family receptors and SAP adaptors in immunity. Annu Rev Immunol (2011) 29:665-705. doi:10.1146/annurev-immunol-030409-101302
15. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, et al. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol (2001) 19:197-223. doi:10.1146/annurev.immunol.19.1.197
16. Biassoni R, Bottino C, Cantoni C, Moretta A. Human natural killer receptors and their ligands. Curr Protoc Immunol (2002) Chapter 14(Unit 14):10. doi:10.1002/0471142735.im1410s46
17. Carlyle JR, Mesci A, Fine JH, Chen P, Belanger S, Tai LH, et al. Evolution of the Ly49 and Nkrp1 recognition systems. Semin Immunol (2008) 20:321-30. doi:10.1016/j.smim.2008.05.004
18. Iizuka K, Naidenko OV, Plougastel BF, Fremont DH, Yokoyama WM. Genetically linked C-type lectin-related ligands for the NKRP1 family of natural killer cell receptors. Nat Immunol (2003) 4:801-7. doi:10.1038/ni954
19. Yokoyama WM, Plougastel BF. Immune functions encoded by the natural killer gene complex. Nat Rev Immunol (2003) 3:304-16. doi:10.1038/nri1055
20. Carlyle JR, Jamieson AM, Gasser S, Clingan CS, Arase H, Raulet DH. Missing self-recognition of Ocil/Clr-b by inhibitory NKR-P1 natural killer cell receptors. Proc Natl Acad Sci U S A (2004) 101:3527-32. doi:10.1073/pnas.0308304101
21. Chen P, Belanger S, Aguilar OA, Zhang Q, St-Laurent A, Rahim MM, et al. Analysis of the mouse 129-strain Nkrp1-Clr gene cluster reveals conservation of genomic organization and functional receptor-ligand interactions despite significant allelic polymorphism. Immunogenetics (2011) 63:627-40. doi:10.1007/s00251-011-0542-8
22. Kveberg L, Dai KZ, Inngjerdingen M, Brooks CG, Fossum S, Vaage JT. Phylogenetic and functional conservation of the NKR-P1F and NKR-P1G receptors in rat and mouse. Immunogenetics (2011) 63:429-36. doi:10.1007/s00251-011-0520-1
23. Vogler I, Steinle A. Vis-a-vis in the NKC: genetically linked natural killer cell receptor/ligand pairs in the natural killer gene complex (NKC). J Innate Immun (2011) 3:227-35. doi:10.1159/000324112
24. Glimcher L, Shen FW, Cantor H. Identification of a cell-surface antigen selectively expressed on the natural killer cell. J Exp Med (1977) 145:1-9. doi:10.1084/jem.145.1.1
25. Brooks CG, Burton RC, Pollack SB, Henney CS. The presence of NK alloantigens on cloned cytotoxic T lymphocytes. J Immunol (1983) 131:1391-5.
26. Koo GC, Peppard JR. Establishment of monoclonal anti-Nk-1.1 antibody. Hybridoma (1984) 3:301-3. doi:10.1089/hyb.1984.3.301
27. Hackett J Jr, Tutt M, Lipscomb M, Bennett M, Koo G, Kumar V. Origin and differentiation of natural killer cells. II. Functional and morphologic studies of purified NK-1.1+ cells. J Immunol (1986) 136:3124-31.
28. Karlhofer FM, Yokoyama WM. Stimulation of murine natural killer (NK) cells by a monoclonal antibody specific for the NK1.1 antigen. IL-2-activated NK cells possess additional specific stimulation pathways. J Immunol (1991) 146:3662-73.
29. Ryan JC, Niemi EC, Nakamura MC, Seaman WE. NKR-P1A is a target-specific receptor that activates natural killer cell cytotoxicity. J Exp Med (1995) 181:1911-5. doi:10.1084/jem.181.5.1911
30. Sentman CL, Hackett J Jr, Moore TA, Tutt MM, Bennett M, Kumar V. Pan natural killer cell monoclonal antibodies and their relationship to the NK1.1 antigen. Hybridoma (1989) 8:605-14. doi:10.1089/hyb.1989.8.605
31. Chambers WH, Vujanovic NL, Deleo AB, Olszowy MW, Herberman RB, Hiserodt JC. Monoclonal antibody to a triggering structure expressed on rat natural killer cells and adherent lymphokine-activated killer cells. J Exp Med (1989) 169:1373-89. doi:10.1084/jem.169.4.1373
32. Giorda R, Rudert WA, Vavassori C, Chambers WH, Hiserodt JC, Trucco M. NKR-P1, a signal transduction molecule on natural killer cells. Science (1990) 249:1298-300. doi:10.1126/science.2399464
33. Giorda R, Trucco M. Mouse NKR-P1. A family of genes selectively coexpressed in adherent lymphokine-activated killer cells. J Immunol (1991) 147:1701-8.
34. Yokoyama WM, Ryan JC, Hunter JJ, Smith HR, Stark M, Seaman WE. 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.
35. Ryan JC, Turck J, Niemi EC, Yokoyama WM, Seaman WE. Molecular cloning of the NK1.1 antigen, a member of the NKR-P1 family of natural killer cell activation molecules. J Immunol (1992) 149:1631-5.
36. Carlyle JR, Martin A, Mehra A, Attisano L, Tsui FW, Zuniga-Pflucker JC. Mouse NKR-P1B, a novel NK1.1 antigen with inhibitory function. J Immunol (1999) 162:5917-23.
37. Kung SK, Su RC, Shannon J, Miller RG. The NKR-P1B gene product is an inhibitory receptor on SJL/J NK cells. J Immunol (1999) 162:5876-87.
38. Plougastel B, Matsumoto K, Dubbelde C, Yokoyama WM. Analysis of a 1-Mb BAC contig overlapping the mouse Nkrp1 cluster of genes: cloning of three new Nkrp1 members, Nkrp1d, Nkrp1e, and Nkrp1f. Immunogenetics (2001) 53:592-8. doi:10.1007/s002510100367
39. Carlyle JR, Mesci A, Ljutic B, Belanger S, Tai LH, Rousselle E, et al. Molecular and genetic basis for strain-dependent NK1.1 alloreactivity of mouse NK cells. J Immunol (2006) 176:7511-24. doi:10.4049/jimmunol.176.12.7511
40. Aust JG, Gays F, Mickiewicz KM, Buchanan E, Brooks CG. The expression and function of the NKRP1 receptor family in C57BL/6 mice. J Immunol (2009) 183:106-16. doi:10.4049/jimmunol.0804281
41. Liu J, Morris MA, Nguyen P, George TC, Koulich E, Lai WC, et al. Ly49I NK cell receptor transgene inhibition of rejection of H2b mouse bone marrow transplants. J Immunol (2000) 164:1793-9. doi:10.4049/jimmunol.164.4.1793
42. Higuchi DA, Cahan P, Gao J, Ferris ST, Poursine-Laurent J, Graubert TA, et al. Structural variation of the mouse natural killer gene complex. Genes Immun (2010) 11:637-48. doi:10.1038/gene.2010.48
43. Kveberg L, Back CJ, Dai KZ, Inngjerdingen M, Rolstad B, Ryan JC, et al. The novel inhibitory NKR-P1C receptor and Ly49s3 identify two complementary, functionally distinct NK cell subsets in rats. J Immunol (2006) 176:4133-40. doi:10.4049/jimmunol.176.7.4133
44. Li J, Rabinovich BA, Hurren R, Shannon J, Miller RG. Expression cloning and function of the rat NK activating and inhibitory receptors NKR-P1A and -P1B. Int Immunol (2003) 15:411-6. doi:10.1093/intimm/dxg046
45. Voigt S, Mesci A, Ettinger J, Fine JH, Chen P, Chou W, et al. Cytomegalovirus evasion of innate immunity by subversion of the NKR-P1B:Clr-b missing-self axis. Immunity (2007) 26:617-27. doi:10.1016/j.immuni.2007.03.013
46. Lanier LL, Chang C, Phillips JH. Human NKR-P1A. A disulfide-linked homodimer of the C-type lectin superfamily expressed by a subset of NK and T lymphocytes. J Immunol (1994) 153:2417-28.
47. Aldemir H, Prod'homme V, Dumaurier MJ, Retiere C, Poupon G, Cazareth J, et al. Cutting edge: lectin-like transcript 1 is a ligand for the CD161 receptor. J Immunol (2005) 175:7791-5. doi:10.4049/jimmunol.175.12.7791
48. Rosen DB, Bettadapura J, Alsharifi M, Mathew PA, Warren HS, Lanier LL. Cutting edge: lectin-like transcript-1 is a ligand for the inhibitory human NKR-P1A receptor. J Immunol (2005) 175:7796-9. doi:10.4049/jimmunol.175.12.7796
49. Giorda R, Weisberg EP, Ip TK, Trucco M. Genomic structure and strain-specific expression of the natural killer cell receptor NKR-P1. J Immunol (1992) 149:1957-63.
50. Zhou H, Kartsogiannis V, Hu YS, Elliott J, Quinn JM, McKinstry WJ, et al. A novel osteoblast-derived C-type lectin that inhibits osteoclast formation. J Biol Chem (2001) 276:14916-23. doi:10.1074/jbc.M011554200
51. Zhou H, Kartsogiannis V, Quinn JM, Ly C, Gange C, Elliott J, et al. Osteoclast inhibitory lectin, a family of new osteoclast inhibitors. J Biol Chem (2002) 277:48808-15. doi:10.1074/jbc.M209059200
52. Plougastel B, Dubbelde C, Yokoyama WM. Cloning of Clr, a new family of lectin-like genes localized between mouse Nkrp1a and Cd69. Immunogenetics (2001) 53:209-14. doi:10.1007/s002510100319
53. Zhang Q, Rahim MM, Allan DS, Tu MM, Belanger S, Abou-Samra E, et al. Mouse Nkrp1-Clr gene cluster sequence and expression analyses reveal conservation of tissue-specific MHC-independent immunosurveillance. PLoS One (2012) 7:e50561. doi:10.1371/journal.pone.0050561
54. Bezouska K, Vlahas G, Horvath O, Jinochova G, Fiserova A, Giorda R, et al. Rat natural killer cell antigen, NKR-P1, related to C-type animal lectins is a carbohydrate-binding protein. J Biol Chem (1994) 269:16945-52.
55. Bezouska K, Yuen CT, O'Brien J, Childs RA, Chai W, Lawson AM, et al. Oligosaccharide ligands for NKR-P1 protein activate NK cells and cytotoxicity. Nature (1994) 372:150-7. doi:10.1038/372150a0
56. Voigt S, Sandford GR, Ding L, Burns WH. Identification and characterization of a spliced C-type lectin-like gene encoded by rat cytomegalovirus. J Virol (2001) 75:603-11. doi:10.1128/JVI.75.2.603-611.2001
57. Ettinger J, Geyer H, Nitsche A, Zimmermann A, Brune W, Sandford GR, et al. Complete genome sequence of the English isolate of rat cytomegalovirus (Murid herpesvirus 8). J Virol (2012) 86:13838. doi:10.1128/JVI.02614-12
58. Quan JX, Zheng F, Li XX, Hu LL, Sun ZY, Jiao YL, et al. Cloning and analysis of rat osteoclast inhibitory lectin gene promoter. J Cell Biochem (2009) 106:599-607. doi:10.1002/jcb.22036
59. Kveberg L, Dai KZ, Westgaard IH, Daws MR, Fossum S, Naper C, et al. Two major groups of rat NKR-P1 receptors can be distinguished based on chromosomal localization, phylogenetic analysis and Clr ligand binding. Eur J Immunol (2009) 39:541-51. doi:10.1002/eji.200838891
60. Boles KS, Barten R, Kumaresan PR, Trowsdale J, Mathew PA. Cloning of a new lectin-like receptor expressed on human NK cells. Immunogenetics (1999) 50:1-7. doi:10.1007/s002510050679
61. Mathew PA, Chuang SS, Vaidya SV, Kumaresan PR, Boles KS, Pham HT. The LLT1 receptor induces IFN-gamma production by human natural killer cells. Mol Immunol (2004) 40:1157-63. doi:10.1016/j.molimm.2003.11.024
62. Hamann J, Montgomery KT, Lau S, Kucherlapati R, Van Lier RA. AICL: a new activation-induced antigen encoded by the human NK gene complex. Immunogenetics (1997) 45:295-300. doi:10.1007/s002510050208
63. Spreu J, Kienle EC, Schrage B, Steinle A. CLEC2A: a novel, alternatively spliced and skin-associated member of the NKC-encoded AICL-CD69-LLT1 family. Immunogenetics (2007) 59:903-12. doi:10.1007/s00251-007-0263-1
64. Hu YS, Zhou H, Myers D, Quinn JM, Atkins GJ, Ly C, et al. Isolation of a human homolog of osteoclast inhibitory lectin that inhibits the formation and function of osteoclasts. J Bone Miner Res (2004) 19:89-99. doi:10.1359/jbmr.0301215
65. Germain C, Bihl F, Zahn S, Poupon G, Dumaurier MJ, Rampanarivo HH, et al. Characterization of alternatively spliced transcript variants of CLEC2D gene. J Biol Chem (2010) 285:36207-15. doi:10.1074/jbc.M110.179622
66. Lysenko O, Schulte D, Mittelbronn M, Steinle A. BACL is a novel brain-associated, non-NKC-encoded mammalian C-type lectin-like receptor of the CLEC2 family. PLoS One (2013) 8:e65345. doi:10.1371/journal.pone.0065345
67. Colonna M, Samaridis J, Angman L. Molecular characterization of two novel C-type lectin-like receptors, one of which is selectively expressed in human dendritic cells. Eur J Immunol (2000) 30:697-704. doi:10.1002/1521-4141(200002)30:2<697::AID-IMMU697>3.0.CO;2-M
68. Ryan JC, Seaman WE. Divergent functions of lectin-like receptors on NK cells. Immunol Rev (1997) 155:79-89. doi:10.1111/j.1600-065X.1997.tb00941.x
69. Flornes LM, Nylenna O, Saether PC, Daws MR, Dissen E, Fossum S. The complete inventory of receptors encoded by the rat natural killer cell gene complex. Immunogenetics (2010) 62:521-30. doi:10.1007/s00251-010-0455-y
70. Welte S, Kuttruff S, Waldhauer I, Steinle A. Mutual activation of natural killer cells and monocytes mediated by NKp80-AICL interaction. Nat Immunol (2006) 7:1334-42. doi:10.1038/ni1402
71. Spreu J, Kuttruff S, Stejfova V, Dennehy KM, Schittek B, Steinle A. Interaction of C-type lectin-like receptors NKp65 and KACL facilitates dedicated immune recognition of human keratinocytes. Proc Natl Acad Sci U S A (2010) 107:5100-5. doi:10.1073/pnas.0913108107
72. Tian W, Feng B, Liou HC. Silencing OCILRP2 leads to intrinsic defects in T cells in response to antigenic stimulation. Cell Immunol (2005) 235:72-84. doi:10.1016/j.cellimm.2005.07.004
73. Tian W, Nunez R, Cheng S, Ding Y, Tumang J, Lyddane C, et al. C-type lectin OCILRP2/Clr-g and its ligand NKRP1f costimulate T cell proliferation and IL-2 production. Cell Immunol (2005) 234:39-53. doi:10.1016/j.cellimm.2005.04.021
74. Denning TL, Granger SW, Mucida D, Graddy R, Leclercq G, Zhang W, et al. Mouse TCRalphabeta+CD8alphaalpha intraepithelial lymphocytes express genes that down-regulate their antigen reactivity and suppress immune responses. J Immunol (2007) 178:4230-9. doi:10.4049/jimmunol.178.10.6654-a
75. Assarsson E, Kambayashi T, Sandberg JK, Hong S, Taniguchi M, Van Kaer L, et al. CD8+ T cells rapidly acquire NK1.1 and NK cell-associated molecules upon stimulation in vitro and in vivo. J Immunol (2000) 165:3673-9. doi:10.4049/jimmunol.165.7.3673
76. Kambayashi T, Assarsson E, Michaelsson J, Berglund P, Diehl AD, Chambers BJ, et al. Emergence of CD8+ T cells expressing NK cell receptors in influenza A virus-infected mice. J Immunol (2000) 165:4964-9. doi:10.4049/jimmunol.165.9.4964
77. Slifka MK, Whitton JL. Activated and memory CD8+ T cells can be distinguished by their cytokine profiles and phenotypic markers. J Immunol (2000) 164:208-16. doi:10.4049/jimmunol.164.1.208
78. McMahon CW, Zajac AJ, Jamieson AM, Corral L, Hammer GE, Ahmed R, et al. Viral and bacterial infections induce expression of multiple NK cell receptors in responding CD8(+) T cells. J Immunol (2002) 169:1444-52. doi:10.4049/jimmunol.169.3.1444
79. 44hi, TCR-V beta 8+ subset. J Immunol (1990) 145:1039-45.
80. Carlyle JR, Michie AM, Furlonger C, Nakano T, Lenardo MJ, Paige CJ, et al. Identification of a novel developmental stage marking lineage commitment of progenitor thymocytes. J Exp Med (1997) 186:173-82. doi:10.1084/jem.186.2.173
81. Carlyle JR, Michie AM, Cho SK, Zuniga-Pflucker JC. Natural killer cell development and function precede alpha beta T cell differentiation in mouse fetal thymic ontogeny. J Immunol (1998) 160:744-53.
82. Carlyle JR, Zuniga-Pflucker JC. Requirement for the thymus in alphabeta T lymphocyte lineage commitment. Immunity (1998) 9:187-97. doi:10.1016/S1074-7613(00)80601-9
83. Carlyle JR, Zuniga-Pflucker JC. Lineage commitment and differentiation of T and natural killer lymphocytes in the fetal mouse. Immunol Rev (1998) 165:63-74. doi:10.1111/j.1600-065X.1998.tb01230.x
84. Carlyle JR, Zuniga-Pflucker JC. Regulation of NK1.1 expression during lineage commitment of progenitor thymocytes. J Immunol (1998) 161:6544-51.
85. Guy-Grand D, Azogui O, Celli S, Darche S, Nussenzweig MC, Kourilsky P, et al. Extrathymic T cell lymphopoiesis: ontogeny and contribution to gut intraepithelial lymphocytes in athymic and euthymic mice. J Exp Med (2003) 197:333-41. doi:10.1084/jem.20021639
86. Vivier E, Spits H, Cupedo T. Interleukin-22-producing innate immune cells: new players in mucosal immunity and tissue repair? Nat Rev Immunol (2009) 9:229-34. doi:10.1038/nri2522
87. Fine JH, Chen P, Mesci A, Allan DS, Gasser S, Raulet DH, et al. Chemotherapy-induced genotoxic stress promotes sensitivity to natural killer cell cytotoxicity by enabling missing-self recognition. Cancer Res (2010) 70:7102-13. doi:10.1158/0008-5472.CAN-10-1316
88. Kveberg L, Dai KZ, Dissen E, Ryan JC, Rolstad B, Vaage JT, et al. Strain-dependent expression of four structurally related rat Ly49 receptors; correlation with NK gene complex haplotype and NK alloreactivity. Immunogenetics (2006) 58:905-16. doi:10.1007/s00251-006-0154-x
89. Kveberg L, Jimenez-Royo P, Naper C, Rolstad B, Butcher GW, Vaage JT, et al. Two complementary rat NK cell subsets, Ly49s3+ and NKR-P1B+, differ in phenotypic characteristics and responsiveness to cytokines. J Leukoc Biol (2010) 88:87-93. doi:10.1189/jlb.0110039
90. Inngjerdingen M, Kveberg L, Vaage JT. A novel NKR-P1B(bright) NK cell subset expresses an activated CD25(+)CX(3)CR1(+)CD62L(-)CD11b(-) CD27(-) phenotype and is prevalent in blood, liver, and gut-associated lymphoid organs of rats. J Immunol (2012) 188:2499-508. doi:10.4049/jimmunol.1003939
91. Rosen DB, Cao W, Avery DT, Tangye SG, Liu YJ, Houchins JP, et al. Functional consequences of interactions between human NKR-P1A and its ligand LLT1 expressed on activated dendritic cells and B cells. J Immunol (2008) 180:6508-17. doi:10.4049/jimmunol.180.10.6508
92. Fergusson JR, Fleming VM, Klenerman P. CD161-expressing human T cells. Front Immunol (2011) 2:36. doi:10.3389/fimmu.2011.00036
93. Poggi A, Zocchi MR, Costa P, Ferrero E, Borsellino G, Placido R, et al. IL-12-mediated NKRP1A up-regulation and consequent enhancement of endothelial transmigration of V delta 2+ TCR gamma delta+ T lymphocytes from healthy donors and multiple sclerosis patients. J Immunol (1999) 162:4349-54.
94. Bennett IM, Zatsepina O, Zamai L, Azzoni L, Mikheeva T, Perussia B. Definition of a natural killer NKR-P1A+/CD56-/CD16- functionally immature human NK cell subset that differentiates in vitro in the presence of interleukin 12. J Exp Med (1996) 184:1845-56. doi:10.1084/jem.184.5.1845
95. Loza MJ, Zamai L, Azzoni L, Rosati E, Perussia B. Expression of type 1 (interferon gamma) and type 2 (interleukin-13, interleukin-5) cytokines at distinct stages of natural killer cell differentiation from progenitor cells. Blood (2002) 99:1273-81. doi:10.1182/blood.V99.4.1273
96. Farag SS, Caligiuri MA. Human natural killer cell development and biology. Blood Rev (2006) 20:123-37. doi:10.1016/j.blre.2005.10.001
97. Freud AG, Caligiuri MA. Human natural killer cell development. Immunol Rev (2006) 214:56-72. doi:10.1111/j.1600-065X.2006.00451.x
98. Poggi A, Costa P, Morelli L, Cantoni C, Pella N, Spada F, et al. Expression of human NKRP1A by CD34+ immature thymocytes: NKRP1A-mediated regulation of proliferation and cytolytic activity. Eur J Immunol (1996) 26:1266-72. doi:10.1002/eji.1830260613
99. Azzoni L, Zatsepina O, Abebe B, Bennett IM, Kanakaraj P, Perussia B. Differential transcriptional regulation of CD161 and a novel gene, 197/15a, by IL-2, IL-15, and IL-12 in NK and T cells. J Immunol (1998) 161:3493-500.
100. Poggi A, Costa P, Tomasello E, Moretta L. IL-12-induced up-regulation of NKRP1A expression in human NK cells and consequent NKRP1A-mediated down-regulation of NK cell activation. Eur J Immunol (1998) 28:1611-6. doi:10.1002/(SICI)1521-4141(199805)28:05<1611::AID-IMMU1611>3.0.CO;2-6
101. Maggi L, Santarlasci V, Capone M, Peired A, Frosali F, Crome SQ, et al. CD161 is a marker of all human IL-17-producing T-cell subsets and is induced by RORC. Eur J Immunol (2010) 40:2174-81. doi:10.1002/eji.200940257
102. Mjosberg JM, Trifari S, Crellin NK, Peters CP, Van Drunen CM, Piet B, et al. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat Immunol (2011) 12:1055-62. doi:10.1038/ni.2104
103. Crellin NK, Trifari S, Kaplan CD, Cupedo T, Spits H. Human NKp44+IL-22+ cells and LTi-like cells constitute a stable RORC+ lineage distinct from conventional natural killer cells. J Exp Med (2010) 207:281-90. doi:10.1084/jem.20091509
104. Pesenacker AM, Bending D, Ursu S, Wu Q, Nistala K, Wedderburn LR. CD161 defines the subset of FoxP3+ T cells capable of producing proinflammatory cytokines. Blood (2013) 121:2647-58. doi:10.1182/blood-2012-08-443473
105. 4+ NKRP1A+ human T lymphocytes. Direct evidence that the NKRP1A molecule is involved in transendothelial migration. Eur J Immunol (1997) 27:2345-50. doi:10.1002/eji.1830270932
106. Poggi A, Rubartelli A, Moretta L, Zocchi MR. Expression and function of NKRP1A molecule on human monocytes and dendritic cells. Eur J Immunol (1997) 27:2965-70. doi:10.1002/eji.1830271132
107. Germain C, Meier A, Jensen T, Knapnougel P, Poupon G, Lazzari A, et al. Induction of lectin-like transcript 1 (LLT1) protein cell surface expression by pathogens and interferon-gamma contributes to modulate immune responses. J Biol Chem (2011) 286:37964-75. doi:10.1074/jbc.M111.285312
108. Back J, Malchiodi EL, Cho S, Scarpellino L, Schneider P, Kerzic MC, et al. Distinct conformations of Ly49 natural killer cell receptors mediate MHC class I recognition in trans and cis. Immunity (2009) 31:598-608. doi:10.1016/j.immuni.2009.07.007
109. Ito D, Iizuka YM, Katepalli MP, Iizuka K. Essential role of the Ly49A stalk region for immunological synapse formation and signaling. Proc Natl Acad Sci U S A (2009) 106:11264-9. doi:10.1073/pnas.0900664106
110. Bartel Y, Bauer B, Steinle A. Modulation of NK cell function by genetically coupled C-type lectin-like receptor/ligand pairs encoded in the human natural killer gene complex. Front Immunol (2013) 4:362. doi:10.3389/fimmu.2013.00362
111. Ljutic B, Carlyle JR, Zuniga-Pflucker JC. Identification of upstream cis-acting regulatory elements controlling lineage-specific expression of the mouse NK cell activation receptor, NKR-P1C. J Biol Chem (2003) 278:31909-17. doi:10.1074/jbc.M212869200
112. Anderson SK. Transcriptional regulation of NK cell receptors. Curr Top Microbiol Immunol (2006) 298:59-75.
113. Drickamer K. Two distinct classes of carbohydrate-recognition domains in animal lectins. J Biol Chem (1988) 263:9557-60.
114. Sovova Z, Kopecky V Jr, Pazderka T, Hofbauerova K, Rozbesky D, Vanek O, et al. Structural analysis of natural killer cell receptor protein 1 (NKR-P1) extracellular domains suggests a conserved long loop region involved in ligand specificity. J Mol Model (2011) 17:1353-70. doi:10.1007/s00894-010-0837-y
115. Rozbesky D, Kavan D, Chmelik J, Novak P, Vanek O, Bezouska K. High-level expression of soluble form of mouse natural killer cell receptor NKR-P1C(B6) in Escherichia coli. Protein Expr Purif (2011) 77:178-84. doi:10.1016/j.pep.2011.01.013
116. Kolenko P, Rozbesky D, Vanek O, Bezouska K, Hasek J, Dohnalek J. Structure of the H107R variant of the extracellular domain of mouse NKR-P1A at 2.3 A resolution. Acta Crystallogr Sect F Struct Biol Cryst Commun (2011) 67:1519-23. doi:10.1107/S1744309111046203
117. Kamishikiryo J, Fukuhara H, Okabe Y, Kuroki K, Maenaka K. Molecular basis for LLT1 protein recognition by human CD161 protein (NKRP1A/KLRB1). J Biol Chem (2011) 286:23823-30. doi:10.1074/jbc.M110.214254
118. Li Y, Wang Q, Chen S, Brown PH, Mariuzza RA. Structure of NKp65 bound to its keratinocyte ligand reveals basis for genetically linked recognition in natural killer gene complex. Proc Natl Acad Sci U S A (2013) 110:11505-10. doi:10.1073/pnas.1303300110
119. Dam J, Guan R, Natarajan K, Dimasi N, Chlewicki LK, Kranz DM, et al. Variable MHC class I engagement by Ly49 natural killer cell receptors demonstrated by the crystal structure of Ly49C bound to H-2K(b). Nat Immunol (2003) 4:1213-22. doi:10.1038/ni1006
120. Skalova T, Kotynkova K, Duskova J, Hasek J, Koval T, Kolenko P, et al. Mouse Clr-g, a ligand for NK cell activation receptor NKR-P1F: crystal structure and biophysical properties. J Immunol (2012) 189:4881-9. doi:10.4049/jimmunol.1200880
121. Brumbaugh KM, Binstadt BA, Billadeau DD, Schoon RA, Dick CJ, Ten RM, et al. Functional role for Syk tyrosine kinase in natural killer cell-mediated natural cytotoxicity. J Exp Med (1997) 186:1965-74. doi:10.1084/jem.186.12.1965
122. Colucci F, Di Santo JP, Leibson PJ. Natural killer cell activation in mice and men: different triggers for similar weapons? Nat Immunol (2002) 3:807-13. doi:10.1038/ni0902-807
123. Colucci F, Schweighoffer E, Tomasello E, Turner M, Ortaldo JR, Vivier E, et al. Natural cytotoxicity uncoupled from the Syk and ZAP-70 intracellular kinases. Nat Immunol (2002) 3:288-94. doi:10.1038/ni764
124. Zompi S, Hamerman JA, Ogasawara K, Schweighoffer E, Tybulewicz VL, Di Santo JP, et al. NKG2D triggers cytotoxicity in mouse NK cells lacking DAP12 or Syk family kinases. Nat Immunol (2003) 4:565-72. doi:10.1038/ni930
125. Arase N, Arase H, Park SY, Ohno H, Ra C, Saito T. Association with FcRgamma is essential for activation signal through NKR-P1 (CD161) in natural killer (NK) cells and NK1.1+ T cells. J Exp Med (1997) 186:1957-63. doi:10.1084/jem.186.12.1957
126. Arase H, Suenaga T, Arase N, Kimura Y, Ito K, Shiina R, et al. Negative regulation of expression and function of Fc gamma RIII by CD3 zeta in murine NK cells. J Immunol (2001) 166:21-5. doi:10.4049/jimmunol.166.1.21
127. Ryan JC, Niemi EC, Goldfien RD, Hiserodt JC, Seaman WE. NKR-P1, an activating molecule on rat natural killer cells, stimulates phosphoinositide turnover and a rise in intracellular calcium. J Immunol (1991) 147:3244-50.
128. Al-Aoukaty A, Rolstad B, Maghazachi AA. Functional coupling of NKR-P1 receptors to various heterotrimeric G proteins in rat interleukin-2-activated natural killer cells. J Biol Chem (1997) 272:31604-8. doi:10.1074/jbc.272.50.31604
129. Grazia Cifone M, Roncaioli P, Cironi L, Festuccia C, Meccia A, D'Alo S, et al. NKR-P1A stimulation of arachidonate-generating enzymes in rat NK cells is associated with granule release and cytotoxic activity. J Immunol (1997) 159:309-17.
130. Mesci A, Ljutic B, Makrigiannis AP, Carlyle JR. NKR-P1 biology: from prototype to missing self. Immunol Res (2006) 35:13-26. doi:10.1385/IR:35:1:13
131. Campbell KS, Giorda R. The cytoplasmic domain of rat NKR-P1 receptor interacts with the N-terminal domain of p56(lck) via cysteine residues. Eur J Immunol (1997) 27:72-7. doi:10.1002/eji.1830270111
132. Ljutic B, Carlyle JR, Filipp D, Nakagawa R, Julius M, Zuniga-Pflucker JC. Functional requirements for signaling through the stimulatory and inhibitory mouse NKR-P1 (CD161) NK cell receptors. J Immunol (2005) 174:4789-96. doi:10.4049/jimmunol.174.8.4789
133. Burshtyn DN, Yang W, Yi T, Long EO. A novel phosphotyrosine motif with a critical amino acid at position -2 for the SH2 domain-mediated activation of the tyrosine phosphatase SHP-1. J Biol Chem (1997) 272:13066-72. doi:10.1074/jbc.272.20.13066
134. Tassi I, Cella M, Gilfillan S, Turnbull I, Diacovo TG, Penninger JM, et al. p110gamma and p110delta phosphoinositide 3-kinase signaling pathways synergize to control development and functions of murine NK cells. Immunity (2007) 27:214-27. doi:10.1016/j.immuni.2007.07.014
135. Gilfillan S, Ho EL, Cella M, Yokoyama WM, Colonna M. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat Immunol (2002) 3:1150-5. doi:10.1038/ni857
136. Diefenbach A, Tomasello E, Lucas M, Jamieson AM, Hsia JK, Vivier E, et al. Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nat Immunol (2002) 3:1142-9. doi:10.1038/ni858
137. Karimi M, Cao TM, Baker JA, Verneris MR, Soares L, Negrin RS. Silencing human NKG2D, DAP10, and DAP12 reduces cytotoxicity of activated CD8+ T cells and NK cells. J Immunol (2005) 175:7819-28. doi:10.4049/jimmunol.175.12.7819
138. Rabinovich B, Li J, Wolfson M, Lawrence W, Beers C, Chalupny J, et al. NKG2D splice variants: a reexamination of adaptor molecule associations. Immunogenetics (2006) 58:81-8. doi:10.1007/s00251-005-0078-x
139. Chang CS, Brossay L, Kronenberg M, Kane KP. The murine nonclassical class I major histocompatibility complex-like CD1.1 molecule protects target cells from lymphokine-activated killer cell cytolysis. J Exp Med (1999) 189:483-91. doi:10.1084/jem.189.3.483
140. Huang MM, Borszcz P, Sidobre S, Kronenberg M, Kane KP. CD1d1 displayed on cell size beads identifies and enriches an NK cell population negatively regulated by CD1d1. J Immunol (2004) 172:5304-12. doi:10.4049/jimmunol.172.9.5304
141. Cerny J, Fiserova A, Horvath O, Bezouska K, Pospisil M, Horejsi V. Association of human NK cell surface receptors NKR-P1 and CD94 with Src-family protein kinases. Immunogenetics (1997) 46:231-6. doi:10.1007/s002510050267
142. Exley M, Porcelli S, Furman M, Garcia J, Balk S. CD161 (NKR-P1A) costimulation of CD1d-dependent activation of human T cells expressing invariant V alpha 24 J alpha Q T cell receptor alpha chains. J Exp Med (1998) 188:867-76. doi:10.1084/jem.188.5.867
143. Pozo D, Vales-Gomez M, Mavaddat N, Williamson SC, Chisholm SE, Reyburn H. CD161 (human NKR-P1A) signaling in NK cells involves the activation of acid sphingomyelinase. J Immunol (2006) 176:2397-406. doi:10.4049/jimmunol.176.4.2397
144. 4+ T cell precursor. J Exp Med (2008) 205:1903-16. doi:10.1084/jem.20080397
145. Dusseaux M, Martin E, Serriari N, Peguillet I, Premel V, Louis D, et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood (2011) 117:1250-9. doi:10.1182/blood-2010-08-303339
146. Lock C, Hermans G, Pedotti R, Brendolan A, Schadt E, Garren H, et al. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med (2002) 8:500-8. doi:10.1038/nm0502-500
147. Kleinschek MA, Boniface K, Sadekova S, Grein J, Murphy EE, Turner SP, et al. Circulating and gut-resident human Th17 cells express CD161 and promote intestinal inflammation. J Exp Med (2009) 206:525-34. doi:10.1084/jem.20081712
148. Wolfkamp SC, Verstege MI, Vogels EW, Meisner S, Verseijden C, Stokkers PC, et al. Single nucleotide polymorphisms in C-type lectin genes, clustered in the IBD2 and IBD6 susceptibility loci, may play a role in the pathogenesis of inflammatory bowel diseases. Eur J Gastroenterol Hepatol (2012) 24:965-70. doi:10.1097/MEG.0b013e328354f3d5
149. Pineda B, Laporta P, Cano A, Garcia-Perez MA. The Asn19Lys substitution in the osteoclast inhibitory lectin (OCIL) gene is associated with a reduction of bone mineral density in postmenopausal women. Calcif Tissue Int (2008) 82:348-53. doi:10.1007/s00223-008-9135-4
150. Williams KJ, Wilson E, Davidson CL, Aguilar OA, Fu L, Carlyle JR, et al. Poxvirus infection-associated downregulation of C-type lectin-related-b prevents NK cell inhibition by NK receptor protein-1B. J Immunol (2012) 188:4980-91. doi:10.4049/jimmunol.1103425
151. Brocchieri L, Kledal TN, Karlin S, Mocarski ES. Predicting coding potential from genome sequence: application to betaherpesviruses infecting rats and mice. J Virol (2005) 79:7570-96. doi:10.1128/JVI.79.12.7570-7596.2005
152. Bambard ND, Mathew SO, Mathew PA. LLT1-mediated activation of IFN-gamma production in human natural killer cells involves ERK signalling pathway. Scand J Immunol (2010) 71:210-9. doi:10.1111/j.1365-3083.2009.02367.x
153. Martick M, Horan LH, Noller HF, Scott WG. A discontinuous hammerhead ribozyme embedded in a mammalian messenger RNA. Nature (2008) 454:899-902. doi:10.1038/nature07117
154. Birikh KR, Heaton PA, Eckstein F. The structure, function and application of the hammerhead ribozyme. Eur J Biochem (1997) 245:1-16. doi:10.1111/j.1432-1033.1997.t01-3-00001.x
155. Hammann C, Luptak A, Perreault J, De La Pena M. The ubiquitous hammerhead ribozyme. RNA (2012) 18:871-85. doi:10.1261/rna.031401.111
156. Scott WG, Horan LH, Martick M. The hammerhead ribozyme: structure, catalysis, and gene regulation. Prog Mol Biol Transl Sci (2013) 120:1-23. doi:10.1016/B978-0-12-381286-5.00001-9