Surveillance of cell and tissue perturbation by receptors in the LRC

Immunological Reviews

Volumn 267, Issue 1, 2015, Pages 117-136

  Trowsdale, John ^a   Jones, Des C ^a   Barrow, Alexander D ^b   Traherne, James A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell activation; Cell surface molecules; Dendritic cells; Major histocompatibility complex; Monocytes macrophages; Natural killer cells

Indexed keywords

CELL RECEPTOR; EPITOPE; IMMUNOGLOBULIN; LEUKOCYTE RECEPTOR COMPLEX; UNCLASSIFIED DRUG; HLA ANTIGEN; HLA ANTIGEN CLASS 1; IMMUNOGLOBULIN RECEPTOR; LIGAND;

ALLELE; ARTICLE; CELL ACTIVATION; CELL SURFACE; COPY NUMBER VARIATION; DENDRITIC CELL; DISEASE SURVEILLANCE; GENE DOSAGE; HAPLOTYPE; HOMOLOGOUS RECOMBINATION; HUMAN; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; LEUKOCYTE; MAJOR HISTOCOMPATIBILITY COMPLEX; MONOCYTE; NATURAL KILLER CELL; PLACENTAL MAMMALS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTION; BIOLOGICAL MODEL; GENETIC VARIATION; GENETICS; IMMUNOLOGY; METABOLISM;

GENETIC VARIATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; KILLER CELLS, NATURAL; LEUKOCYTES; LIGANDS; MODELS, GENETIC; MODELS, IMMUNOLOGICAL; RECEPTORS, IMMUNOLOGIC;

EID: 84939527080     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12314     Document Type: Article

References (158)

1. Moffett A, Loke C. Immunology of placentation in eutherian mammals. Nat Rev Immunol 2006;6:584-594.
2. Parham P, Moffett A. Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat Rev Immunol 2013;13:133-144.
3. Cassidy SA, Cheent KS, Khakoo SI. Effects of peptide on NK cell-mediated MHC I recognition. Front Immunol 2014;5:133.
4. Martin MP, Bashirova A, Traherne J, Trowsdale J, Carrington M. Cutting edge: expansion of the KIR locus by unequal crossing over. J Immunol 2003;171:2192-2195.
5. Jiang W, et al. Copy number variation leads to considerable diversity for B but not A haplotypes of the human KIR genes encoding NK cell receptors. Genome Res 2012;22:1845-1854.
6. Traherne JA, et al. Mechanisms of copy number variation and hybrid gene formation in the KIR immune gene complex. Hum Mol Genet 2010;19:737-751.
7. Nakimuli A, et al. Killer cell immunoglobulin-like receptor (KIR) genes and their HLA-C ligands in a Ugandan population. Immunogenetics 2013;65:765-775.
8. Single RM, et al. Global diversity and evidence for coevolution of KIR and HLA. Nat Genet 2007;39:1114-1119.
9. Abi-Rached L, Parham P. Natural selection drives recurrent formation of activating killer cell immunoglobulin-like receptor and Ly49 from inhibitory homologues. J Exp Med 2005;201:1319-1332.
10. Hilton HG, et al. Mutation at positively selected positions in the binding site for HLA-C shows that KIR2DL1 is a more refined but less adaptable NK cell receptor than KIR2DL3. J Immunol 2012;189:1418-1430.
11. Khakoo SI, et al. HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 2004;305:872-874.
12. Pelak K, et al. Copy number variation of KIR genes influences HIV-1 control. PLoS Biol 2011;9:e1001208.
13. Beziat V, et al. Tracing dynamic expansion of human NK-cell subsets by high-resolution analysis of KIR repertoires and cellular differentiation. Eur J Immunol 2014;44:2192-2196.
14. Horowitz A, et al. Genetic and environmental determinants of human NK cell diversity revealed by mass cytometry. Sci Transl Med 2013;5:208ra145.
15. Dunphy SE, et al. 2DL1, 2DL2 and 2DL3 all contribute to KIR phenotype variability on human NK cells. Genes Immun 2015;16:301-310.
16. Beziat V, et al. Influence of KIR gene copy number on natural killer cell education. Blood 2013;121:4703-4707.
17. Pende D, et al. Anti-leukemia activity of alloreactive NK cells in KIR ligand-mismatched haploidentical HSCT for pediatric patients: evaluation of the functional role of activating KIR and redefinition of inhibitory KIR specificity. Blood 2009;113:3119-3129.
18. Felices M, et al. Functional NK cell repertoires are maintained through IL-2Ralpha and Fas ligand. J Immunol 2014;192:3889-3897.
19. Azzi T, et al. Role for early-differentiated natural killer cells in infectious mononucleosis. Blood 2014;124:2533-2543.
20. Jones DC, et al. Killer immunoglobulin-like receptor gene repertoire influences viral load of primary human cytomegalovirus infection in renal transplant patients. Genes Immun 2014;15:562-568.
21. Hadaya K, et al. Natural killer cell receptor repertoire and their ligands, and the risk of CMV infection after kidney transplantation. Am J Transplant 2008;8:2674-2683.
22. Stern M, et al. Telomeric rather than centromeric activating KIR genes protect from cytomegalovirus infection after kidney transplantation. Am J Transplant 2011;11:1302-1307.
23. Hiby SE, et al. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J Exp Med 2004;200:957-965.
24. Nakimuli A, et al. A KIR B centromeric region present in Africans but not Europeans protects pregnant women from pre-eclampsia. Proc Natl Acad Sci USA 2015;112:845-850.
25. Khakoo SI, Carrington M. KIR and disease: a model system or system of models? Immunol Rev 2006;214:186-201.
26. Moffett A, Hiby SE, Sharkey AM. The role of the maternal immune system in the regulation of human birthweight. Philos Trans R Soc Lond B Biol Sci 2015;370:1-9.
27. Roberts CH, Jiang W, Jayaraman J, Trowsdale J, Holland MJ, Traherne JA. Killer-cell immunoglobulin-like receptor gene linkage and copy number variation analysis by droplet digital PCR. Genome Med 2014;6:20.
28. Pontikos N, et al. A hybrid qPCR/SNP array approach allows cost efficient assessment of KIR gene copy numbers in large samples. BMC Genom 2014;15:274.
29. Nakajima H, Samaridis J, Angman L, Colonna M. Human myeloid cells express an activating ILT receptor (ILT1) that associates with Fc receptor gamma-chain. J Immunol 1999;162:5-8.
30. Cao W, et al. Plasmacytoid dendritic cell-specific receptor ILT7-Fc epsilonRI gamma inhibits Toll-like receptor-induced interferon production. J Exp Med 2006;203:1399-1405.
31. Colonna M, et al. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J Exp Med 1997;186:1809-1818.
32. Arm JP, Nwankwo C, Austen KF. Molecular identification of a novel family of human Ig superfamily members that possess immunoreceptor tyrosine-based inhibition motifs and homology to the mouse gp49B1 inhibitory receptor. J Immunol 1997;159:2342-2349.
33. Borges L, Hsu ML, Fanger N, Kubin M, Cosman D. A family of human lymphoid and myeloid Ig-like receptors, some of which bind to MHC class I molecules. J Immunol 1997;159:5192-5196.
34. An H, et al. Soluble LILRA3, a potential natural antiinflammatory protein, is increased in patients with rheumatoid arthritis and is tightly regulated by interleukin 10, tumor necrosis factor-alpha, and interferon-gamma. J Rheumatol 2010;37:1596-1606.
35. Jones DC, et al. Alternative mRNA splicing creates transcripts encoding soluble proteins from most LILR genes. Eur J Immunol 2009;39:3195-3206.
36. Hogan L, et al. Characterisation of bovine leukocyte Ig-like receptors. PLoS ONE 2012;7:e34291.
37. Dennis G Jr, Kubagawa H, Cooper MD. Paired Ig-like receptor homologs in birds and mammals share a common ancestor with mammalian Fc receptors. Proc Natl Acad Sci USA 2000;97:13245-13250.
38. Stafford JL, et al. A novel family of diversified immunoregulatory receptors in teleosts is homologous to both mammalian Fc receptors and molecules encoded within the leukocyte receptor complex. Immunogenetics 2006;58:758-773.
39. Viertlboeck BC, et al. The chicken leukocyte receptor complex encodes a primordial, activating, high-affinity IgY Fc receptor. Proc Natl Acad Sci USA 2007;104:11718-11723.
40. Taylor AI, Fabiane SM, Sutton BJ, Calvert RA. The crystal structure of an avian IgY-Fc fragment reveals conservation with both mammalian IgG and IgE. Biochemistry 2009;48:558-562.
41. Warr GW, Magor KE, Higgins DA. IgY: clues to the origins of modern antibodies. Immunol Today 1995;16:392-398.
42. Nakamura A, Kobayashi E, Takai T. Exacerbated graft-versus-host disease in Pirb-/- mice. Nat Immunol 2004;5:623-629.
43. Atwal JK, et al. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008;322:967-970.
44. Kim T, et al. Human LilrB2 is a beta-amyloid receptor and its murine homolog PirB regulates synaptic plasticity in an Alzheimer's model. Science 2013;341:1399-1404.
45. Zheng J, et al. Inhibitory receptors bind ANGPTLs and support blood stem cells and leukaemia development. Nature 2012;485:656-660.
46. Syken J, Grandpre T, Kanold PO, Shatz CJ. PirB restricts ocular-dominance plasticity in visual cortex. Science 2006;313:1795-1800.
47. Navarro F, Llano M, Bellon T, Colonna M, Geraghty DE, Lopez-Botet M. The ILT2(LIR1) and CD94/NKG2A NK cell receptors respectively recognize HLA-G1 and HLA-E molecules co-expressed on target cells. Eur J Immunol 1999;29:277-283.
48. - NK cells. J Immunol 2007;178:4473-4481.
49. Merlo A, et al. Inhibitory receptors CD85j, LAIR-1, and CD152 down-regulate immunoglobulin and cytokine production by human B lymphocytes. Clin Diagn Lab Immunol 2005;12:705-712.
50. Dietrich J, Cella M, Colonna M. Ig-like transcript 2 (ILT2)/leukocyte Ig-like receptor 1 (LIR1) inhibits TCR signaling and actin cytoskeleton reorganization. J Immunol 2001;166:2514-2521.
51. + T-cell clones specific for Mycobacterium tuberculosis. Infect Immun 2001;69:6022-6029.
52. Saverino D, Merlo A, Bruno S, Pistoia V, Grossi CE, Ciccone E. Dual effect of CD85/leukocyte Ig-like receptor-1/Ig-like transcript 2 and CD152 (CTLA-4) on cytokine production by antigen-stimulated human T cells. J Immunol 2002;168:207-215.
53. Shiroishi M, et al. Human inhibitory receptors Ig-like transcript 2 (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLA-G. Proc Natl Acad Sci USA 2003;100:8856-8861.
54. + T cells during the evolution of Epstein-Barr virus-specific immune responses in vivo. Viral Immunol 2005;18:513-522.
55. Tenca C, et al. CD85j (leukocyte Ig-like receptor-1/Ig-like transcript 2) inhibits human osteoclast-associated receptor-mediated activation of human dendritic cells. J Immunol 2005;174:6757-6763.
56. Young NT, Waller EC, Patel R, Roghanian A, Austyn JM, Trowsdale J. The inhibitory receptor LILRB1 modulates the differentiation and regulatory potential of human dendritic cells. Blood 2008;111:3090-3096.
57. Fanger NA, Cosman D, Peterson L, Braddy SC, Maliszewski CR, Borges L. The MHC class I binding proteins LIR-1 and LIR-2 inhibit Fc receptor-mediated signaling in monocytes. Eur J Immunol 1998;28:3423-3434.
58. Colonna M, et al. Human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules. J Immunol 1998;160:3096-3100.
59. Chang CC, et al. Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol 2002;3:237-243.
60. Suciu-Foca N, et al. Soluble Ig-like transcript 3 inhibits tumor allograft rejection in humanized SCID mice and T cell responses in cancer patients. J Immunol 2007;178:7432-7441.
61. Borges L, Kubin M, Kuhlman T. LIR9, an immunoglobulin-superfamily-activating receptor, is expressed as a transmembrane and as a secreted molecule. Blood 2003;101:1484-1486.
62. Lee DJ, et al. LILRA2 activation inhibits dendritic cell differentiation and antigen presentation to T cells. J Immunol 2007;179:8128-8136.
63. Cao W, et al. Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. J Exp Med 2009;206:1603-1614.
64. Barrow AD, Trowsdale J. You say ITAM and I say ITIM, let's call the whole thing off: the ambiguity of immunoreceptor signalling. Eur J Immunol 2006;36:1646-1653.
65. Bleharski JR, et al. Use of genetic profiling in leprosy to discriminate clinical forms of the disease. Science 2003;301:1527-1530.
66. Ju XS, et al. Immunoglobulin-like transcripts ILT2, ILT3 and ILT7 are expressed by human dendritic cells and down-regulated following activation. Gene 2004;331:159-164.
67. Cella M, Nakajima H, Facchetti F, Hoffmann T, Colonna M. ILT receptors at the interface between lymphoid and myeloid cells. Curr Top Microbiol Immunol 2000;251:161-166.
68. Velten FW, Duperrier K, Bohlender J, Metharom P, Goerdt S. A gene signature of inhibitory MHC receptors identifies a BDCA3(+) subset of IL-10-induced dendritic cells with reduced allostimulatory capacity in vitro. Eur J Immunol 2004;34:2800-2811.
69. Beinhauer BG, et al. Interleukin 10 regulates cell surface and soluble LIR-2 (CD85d) expression on dendritic cells resulting in T cell hyporesponsiveness in vitro. Eur J Immunol 2004;34:74-80.
70. Vlad G, et al. Interleukin-10 induces the upregulation of the inhibitory receptor ILT4 in monocytes from HIV positive individuals. Hum Immunol 2003;64:483-489.
71. Colonna M, Nakajima H, Cella M. Inhibitory and activating receptors involved in immune surveillance by human NK and myeloid cells. J Leukoc Biol 1999;66:718-722.
72. Willcox BE, Thomas LM, Bjorkman PJ. Crystal structure of HLA-A2 bound to LIR-1, a host and viral major histocompatibility complex receptor. Nat Immunol 2003;4:913-919.
73. Jones DC, et al. HLA class I allelic sequence and conformation regulate leukocyte Ig-like receptor binding. J Immunol 2011;186:2990-2997.
74. Allen RL, Raine T, Haude A, Trowsdale J, Wilson MJ. Leukocyte receptor complex-encoded immunomodulatory receptors show differing specificity for alternative HLA-B27 structures. J Immunol 2001;167:5543-5547.
75. Shiroishi M, et al. Structural basis for recognition of the nonclassical MHC molecule HLA-G by the leukocyte Ig-like receptor B2 (LILRB2/LIR2/ILT4/CD85d). Proc Natl Acad Sci USA 2006;103:16412-16417.
76. Lichterfeld M, et al. A viral CTL escape mutation leading to immunoglobulin-like transcript 4-mediated functional inhibition of myelomonocytic cells. J Exp Med 2007;204:2813-2824.
77. Shiroishi M, et al. Efficient leukocyte Ig-like receptor signaling and crystal structure of disulfide-linked HLA-G dimer. J Biol Chem 2006;281:10439-10447.
78. + human cord blood cells. Eur J Haematol 2012;89:198-205.
79. Maeda A, Kurosaki M, Ono M, Takai T, Kurosaki T. Requirement of SH2-containing protein tyrosine phosphatases SHP-1 and SHP-2 for paired immunoglobulin-like receptor B (PIR-B)-mediated inhibitory signal. J Exp Med 1998;187:1355-1360.
80. Blery M, Kubagawa H, Chen CC, Vely F, Cooper MD, Vivier E. The paired Ig-like receptor PIR-B is an inhibitory receptor that recruits the protein-tyrosine phosphatase SHP-1. Proc Natl Acad Sci USA 1998;95:2446-2451.
81. Liang S, Ristich V, Arase H, Dausset J, Carosella ED, Horuzsko A. Modulation of dendritic cell differentiation by HLA-G and ILT4 requires the IL-6-STAT3 signaling pathway. Proc Natl Acad Sci USA 2008;105:8357-8362.
82. Lampson L. Molecular bases of the immune response to neural antigens. Trends Neurosci 1987;10:211-216.
83. Deng M, et al. A motif in LILRB2 critical for Angptl2 binding and activation. Blood 2014;124:924-935.
84. Matsushita H, et al. Differential but competitive binding of Nogo protein and class i major histocompatibility complex (MHCI) to the PIR-B ectodomain provides an inhibition of cells. J Biol Chem 2011;286:25739-25747.
85. Masuda A, Nakamura A, Maeda T, Sakamoto Y, Takai T. Cis binding between inhibitory receptors and MHC class I can regulate mast cell activation. J Exp Med 2007;204:907-920.
86. Kupzig S, Korolchuk V, Rollason R, Sugden A, Wilde A, Banting G. Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic 2003;4:694-709.
87. Ohtomo T, et al. Molecular cloning and characterization of a surface antigen preferentially overexpressed on multiple myeloma cells. Biochem Biophys Res Commun 1999;258:583-591.
88. Walter-Yohrling J, et al. Identification of genes expressed in malignant cells that promote invasion. Cancer Res 2003;63:8939-8947.
89. Van Damme N, et al. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 2008;3:245-252.
90. Blasius AL, Giurisato E, Cella M, Schreiber RD, Shaw AS, Colonna M. Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J Immunol 2006;177:3260-3265.
91. Lebbink RJ, et al. Collagens are functional, high affinity ligands for the inhibitory immune receptor LAIR-1. J Exp Med 2006;203:1419-1425.
92. Barrow AD, et al. OSCAR is a collagen receptor that costimulates osteoclastogenesis in DAP12-deficient humans and mice. J Clin Invest 2011;121:3505-3516.
93. Jiang L, Barclay AN. New assay to detect low-affinity interactions and characterization of leukocyte receptors for collagen including leukocyte-associated Ig-like receptor-1 (LAIR-1). Eur J Immunol 2009;39:1167-1175.
94. Lopez-Alvarez MR, Jones DC, Jiang W, Traherne JA, Trowsdale J. Copy number and nucleotide variation of the LILR family of myelomonocytic cell activating and inhibitory receptors. Immunogenetics 2014;66:73-83.
95. Bashirova AA, Apps R, Vince N, Mochalova Y, Yu XG, Carrington M. Diversity of the human LILRB3/A6 locus encoding a myeloid inhibitory and activating receptor pair. Immunogenetics 2014;66:1-8.
96. Colonna M, Nakajima H, Navarro F, Lopez-Botet M. A novel family of Ig-like receptors for HLA class I molecules that modulate function of lymphoid and myeloid cells. J Leukoc Biol 1999;66:375-381.
97. Torkar M, Haude A, Milne S, Beck S, Trowsdale J, Wilson MJ. Arrangement of the ILT gene cluster: a common null allele of the ILT6 gene results from a 6.7-kbp deletion. Eur J Immunol 2000;30:3655-3662.
98. + NK cell clones. Int Immunol 1999;11:29-35.
99. Chapman TL, Heikeman AP, Bjorkman PJ. The inhibitory receptor LIR-1 uses a common binding interaction to recognize class I MHC molecules and the viral homolog UL18. Immunity 1999;11:603-613.
100. Jackson SE, Mason GM, Wills MR. Human cytomegalovirus immunity and immune evasion. Virus Res 2011;157:151-160.
101. Ljunggren HG, Karre K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol Today 1990;11:237-244.
102. Chan KR, et al. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc Natl Acad Sci USA 2014;111:2722-2727.
103. Halstead SB. In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect Dis 1979;140:527-533.
104. Halstead SB, Porterfield JS, O'Rourke EJ. Enhancement of dengue virus infection in monocytes by flavivirus antisera. Am J Trop Med Hyg 1980;29:638-642.
105. Kliks SC, Nisalak A, Brandt WE, Wahl L, Burke DS. Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. Am J Trop Med Hyg 1989;40:444-451.
106. Morens DM, Halstead SB. Measurement of antibody-dependent infection enhancement of four dengue virus serotypes by monoclonal and polyclonal antibodies. J Gen Virol 1990;71(Pt 12):2909-2914.
107. Brown MG, King CA, Sherren C, Marshall JS, Anderson R. A dominant role for FcgammaRII in antibody-enhanced dengue virus infection of human mast cells and associated CCL5 release. J Leukoc Biol 2006;80:1242-1250.
108. Huang KJ, et al. The dual-specific binding of dengue virus and target cells for the antibody-dependent enhancement of dengue virus infection. J Immunol 2006;176:2825-2832.
109. Littaua R, Kurane I, Ennis FA. Human IgG Fc receptor II mediates antibody-dependent enhancement of dengue virus infection. J Immunol 1990;144:3183-3186.
110. Rodrigo WW, Jin X, Blackley SD, Rose RC, Schlesinger JJ. Differential enhancement of dengue virus immune complex infectivity mediated by signaling-competent and signaling-incompetent human Fcgamma RIA (CD64) or FcgammaRIIA (CD32). J Virol 2006;80:10128-10138.
111. Barclay AN, Hatherley D. The counterbalance theory for evolution and function of paired receptors. Immunity 2008;29:675-678.
112. Koch S, et al. Association of multiple sclerosis with ILT6 deficiency. Genes Immun 2005;6:445-447.
113. Ordonez D, et al. Multiple sclerosis associates with LILRA3 deletion in Spanish patients. Genes Immun 2009;10:579-585.
114. Bonetti A, et al. A follow-up study of chromosome 19q13 in multiple sclerosis susceptibility. J Neuroimmunol 2009;208:119-124.
115. Wisniewski A, et al. 6.7-kbp deletion in LILRA3 (ILT6) gene is associated with later onset of the multiple sclerosis in a Polish population. Hum Immunol 2013;74:353-357.
116. Kabalak G, et al. Association of immunoglobulin-like transcript 6 deficiency with Sjogren's syndrome. Arthritis Rheum 2009;60:2923-2925.
117. Du Y, et al. Contribution of functional LILRA3, but not nonfunctional LILRA3, to sex bias in susceptibility and severity of anti-citrullinated protein antibody-positive rheumatoid arthritis. Arthritis Rheumatol 2014;66:822-830.
118. Lee JY, Petratos S. Multiple sclerosis: does Nogo play a role? Neuroscientist 2013;19:394-408.
119. Nakayama M, et al. Paired Ig-like receptors bind to bacteria and shape TLR-mediated cytokine production. J Immunol 2007;178:4250-4259.
120. Gibbins JM, Okuma M, Farndale R, Barnes M, Watson SP. Glycoprotein VI is the collagen receptor in platelets which underlies tyrosine phosphorylation of the Fc receptor gamma-chain. FEBS Lett 1997;413:255-259.
121. Verbrugge A, de Ruiter T, Geest C, Coffer PJ, Meyaard L. Differential expression of leukocyte-associated Ig-like receptor-1 during neutrophil differentiation and activation. J Leukoc Biol 2006;79:828-836.
122. Moroi M, Jung SM, Okuma M, Shinmyozu K. A patient with platelets deficient in glycoprotein VI that lack both collagen-induced aggregation and adhesion. J Clin Invest 1989;84:1440-1445.
123. Merck E, et al. OSCAR is an FcRgamma-associated receptor that is expressed by myeloid cells and is involved in antigen presentation and activation of human dendritic cells. Blood 2004;104:1386-1395.
124. Schultz HS, et al. Collagen induces maturation of human monocyte-derived dendritic cells by signaling through osteoclast-associated receptor. J Immunol 2015;194:3169-3179.
125. Lebbink RJ, Raynal N, de Ruiter T, Bihan DG, Farndale RW, Meyaard L. Identification of multiple potent binding sites for human leukocyte associated Ig-like receptor LAIR on collagens II and III. Matrix Biol 2009;28:202-210.
126. Tang X, et al. Leukocyte-associated Ig-like receptor-1-deficient mice have an altered immune cell phenotype. J Immunol 2012;188:548-558.
127. Fu Q, Tao Y, Piao H, Du MR, Li DJ. Trophoblasts and decidual stromal cells regulate decidual NK cell functions via interaction between collagen and LAIR-1. Am J Reprod Immunol 2014;71:368-378.
128. Founds SA, Fallert-Junecko B, Reinhart TA, Parks WT. LAIR2-expressing extravillous trophoblasts associate with maternal spiral arterioles undergoing physiologic conversion. Placenta 2013;34:248-255.
129. Apps R, et al. Genome-wide expression profile of first trimester villous and extravillous human trophoblast cells. Placenta 2011;32:33-43.
130. Oefner CM, Sharkey A, Gardner L, Critchley H, Oyen M, Moffett A. Collagen type IV at the fetal-maternal interface. Placenta 2015;36:59-68.
131. Olde Nordkamp MJ, van Eijk M, Urbanus RT, Bont L, Haagsman HP, Meyaard L. Leukocyte-associated Ig-like receptor-1 is a novel inhibitory receptor for surfactant protein D. J Leukoc Biol 2014;96:105-111.
132. Holmskov U, Thiel S, Jensenius JC. Collections and ficolins: humoral lectins of the innate immune defense. Annu Rev Immunol 2003;21:547-578.
133. Snyder GD, et al. Surfactant protein D is expressed and modulates inflammatory responses in human coronary artery smooth muscle cells. Am J Physiol Heart Circ Physiol 2008;294:H2053-H2059.
134. Sorensen GL, et al. Surfactant protein D is proatherogenic in mice. Am J Physiol Heart Circ Physiol 2006;290:H2286-H2294.
135. + inflammatory monocytes. J Immunol 2015;194:3317-3326.
136. Meyaard L. LAIR-1, a widely distributed human ITIM-bearing receptor on hematopoietic cells. Curr Top Microbiol Immunol 1999;244:151-157.
137. Son M, Santiago-Schwarz F, Al-Abed Y, Diamond B. C1q limits dendritic cell differentiation and activation by engaging LAIR-1. Proc Natl Acad Sci USA 2012;109:E3160-E3167.
138. Olde Nordkamp MJ, et al. Inhibition of the classical and lectin pathway of the complement system by recombinant LAIR-2. J Innate Immun 2014;6:284-292.
139. Son M, Diamond B. C1q-mediated repression of human monocytes is regulated by LAIR-1. Mol Med 2015;20:559-568.
140. Pessino A, et al. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J Exp Med 1998;188:953-960.
141. Sawa S, et al. RORgammat+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat Immunol 2011;12:320-326.
142. Mandelboim O, et al. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 2001;409:1055-1060.
143. Jarahian M, et al. Activation of natural killer cells by newcastle disease virus hemagglutinin-neuraminidase. J Virol 2009;83:8108-8121.
144. Arnon TI, Lev M, Katz G, Chernobrov Y, Porgador A, Mandelboim O. Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur J Immunol 2001;31:2680-2689.
145. Garg A, et al. Vimentin expressed on Mycobacterium tuberculosis-infected human monocytes is involved in binding to the NKp46 receptor. J Immunol 2006;177:6192-6198.
146. Zilka A, et al. Characterization of the heparin/heparan sulfate binding site of the natural cytotoxicity receptor NKp46. Biochemistry 2005;44:14477-14485.
147. Hecht ML, et al. Natural cytotoxicity receptors NKp30, NKp44 and NKp46 bind to different heparan sulfate/heparin sequences. J Proteome Res 2009;8:712-720.
148. Ito K, et al. Binding of natural cytotoxicity receptor NKp46 to sulfate- and alpha2, 3-NeuAc-containing glycans and its mutagenesis. Biochem Biophys Res Commun 2011;406:377-382.
149. Mavoungou E, Held J, Mewono L, Kremsner PG. A Duffy binding-like domain is involved in the NKp30-mediated recognition of Plasmodium falciparum-parasitized erythrocytes by natural killer cells. J Infect Dis 2007;195:1521-1531.
150. Chaushu S, et al. Direct recognition of Fusobacterium nucleatum by the NK cell natural cytotoxicity receptor NKp46 aggravates periodontal disease. PLoS Pathog 2012;8:e1002601.
151. Gur C, et al. Recognition and killing of human and murine pancreatic beta cells by the NK receptor NKp46. J Immunol 2011;187:3096-3103.
152. Gur C, et al. The expression of the beta cell-derived autoimmune ligand for the killer receptor nkp46 is attenuated in type 2 diabetes. PLoS ONE 2013;8:e74033.
153. Pasquier B, et al. Identification of FcalphaRI as an inhibitory receptor that controls inflammation: dual role of FcRgamma ITAM. Immunity 2005;22:31-42.
154. Pfirsch-Maisonnas S, et al. Inhibitory ITAM signaling traps activating receptors with the phosphatase SHP-1 to form polarized "inhibisome" clusters. Sci Signal 2011;4:ra24.
155. Ben Mkaddem S, et al. Shifting FcgammaRIIA-ITAM from activation to inhibitory configuration ameliorates arthritis. J Clin Invest 2014;124:3945-3959.
156. Steevels TA, Lebbink RJ, Westerlaken GH, Coffer PJ, Meyaard L. Signal inhibitory receptor on leukocytes-1 is a novel functional inhibitory immune receptor expressed on human phagocytes. J Immunol 2010;184:4741-4748.
157. Van Avondt K, Fritsch-Stork R, Derksen RH, Meyaard L. Ligation of signal inhibitory receptor on leukocytes-1 suppresses the release of neutrophil extracellular traps in systemic lupus erythematosus. PLoS ONE 2013;8:e78459.
158. Steevels TA, et al. Signal inhibitory receptor on leukocytes-1 (SIRL-1) negatively regulates the oxidative burst in human phagocytes. Eur J Immunol 2013;43:1297-1308.