The LILR family: Modulators of innate and adaptive immune pathways in health and disease

Tissue Antigens

Volumn 64, Issue 3, 2004, Pages 215-225

  Brown, D ^a   Trowsdale, J ^a   Allen, R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Autoimmunity; ILT; LILR; MHC; Tolerance

Indexed keywords

CELL RECEPTOR; HLA B27 ANTIGEN; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN RECEPTOR; LEUKOCYTE ANTIBODY; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; UNCLASSIFIED DRUG;

ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ARTHRITIS; BACTERIAL INFECTION; BONE MARROW CELL; CELL LINEAGE; CELLULAR IMMUNITY; DENDRITIC CELL; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; LEUKOCYTE; LYMPHOID CELL; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; RECEPTOR INTRINSIC ACTIVITY; REVIEW; SIGNAL TRANSDUCTION; SPONDYLOARTHROPATHY; T LYMPHOCYTE; TRANSPLANTATION; VIRUS INFECTION;

ANIMALS; HUMANS; IMMUNE SYSTEM; IMMUNE SYSTEM DISEASES; LEUKOCYTES; RECEPTORS, IMMUNOLOGIC;

BACTERIA (MICROORGANISMS);

EID: 4344677515     PISSN: 00012815     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0001-2815.2004.00290.x     Document Type: Review

References (73)

1. Cosman D, Fanger N, Borges L et al. A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 1997: 7: 273-82.
2. Colonna M, Navarro F, Bellon T et al. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J Exp Med 1997: 186: 1809-18.
3. 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.
4. Saverino D, Fabbi M, Ghiotto F et al. The CD85/LIR-1/ILT2 inhibitory receptor is expressed by all human T lymphocytes and down-regulates their functions. J Immunol 2000: 165: 3742-55.
5. Samaridis J, Colonna M. Cloning of novel immunoglobulin superfamily receptors expressed on human myeloid and lymphoid cells: structural evidence for new stimulatory and inhibitory pathways. Eur J Immunol 1997: 27: 660-5.
6. 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: 2514-21.
7. 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.
8. Cella M, Dohring C, Samaridis J et al. A novel inhibitory receptor (ILT3) expressed on monocytes, macrophages, and dendritic cells involved in antigen processing. J Exp Med 1997: 185: 1743-51.
9. Gergely J, Pecht I, Sarmay G. Immunoreceptor tyrosine-based inhibition motif-bearing receptors regulate the immunoreceptor tyrosine-based activation motif-induced activation of immune competent cells. Immunol Lett 1999: 68: 3-15.
10. Wilson MJ, Torkar M, Haude A et al. Plasticity in the organization and sequences of human KIR/ILT gene families. Proc Natl Acad Sci USA 2000: 97: 4778-83.
11. 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: 3655-32.
12. Young NT, Canavez F, Uhrberg M, Shum BP, Parham P. Conserved organization of the ILT/LIR gene family within the polymorphic human leukocyte receptor complex. Immunogenetics 2001: 53: 270-8.
13. Canavez F, Young NT, Guethlein LA et al. Comparison of chimpanzee and human leukocyte Ig-like receptor genes reveals framework and rapidly evolving genes. J Immunol 2001: 167: 5786-94.
14. Karre K. NK cells, MHC class I molecules and the missing self. Scand J Immunol 2002: 55: 221-8.
15. Lopez-Botet M, Llano M, Ortega M. Human cytomegalovirus and natural killer-mediated surveillance of HLA class I expression: a paradigm of host-pathogen adaptation. Immunol Rev 2001: 181: 193-202.
16. Vitale M, Castriconi R, Parolini S et al. The leukocyte Ig-like receptor (LIR)-1 for the cytomegalovirus UL18 protein displays a broad specificity for different HLA class I alleles: analysis of LIR-1 + NK cell clones. Int Immunol 1999: 11: 29-35.
17. 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: 603-13.
18. Willcox BE, Thomas LM, Chapman TL, Heikema AP, West AP Jr, Bjorkman PJ. Crystal structure of LIR-2 (ILT4) at 1.8 A: differences from LIR-1 (ILT2) in regions implicated in the binding of the human Cytomegalovirus class I MHC homolog UL18. BMC Struct Biol 2002: 2: 6.
19. 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: 3423-34.
20. Colonna M, Samaridis J, Cella M et al. Human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules. J Immunol 1998: 160: 3096-100.
21. 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: 277-83.
22. 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: 5543-7.
23. Allan DS, Colonna M, Lanier LL et al. Tetrameric complexes of human histocompatibility leukocyte antigen (HLA)-G bind to peripheral blood myelomonocytic cells. J Exp Med 1999: 189: 1149-56.
24. O'Callaghan CA, Bell JI. Structure and function of the human MHC class Ib molecules HLA-E, HLA-F and HLA-G. Immunol Rev 1998: 163: 129-38.
25. Lepin EJ, Bastin JM, Allan DS et al. Functional characterization of HLA-F and binding of HLA-F tetramers to ILT2 and ILT4 receptors. Eur J Immunol 2000: 30: 3552-61.
26. Shiroishi M, Tsumoto K, Amano K 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: 8856-61.
27. 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: 913-9.
28. Kollnberger S, Bird L, Sun MY et al. Cell-surface expression and immune receptor recognition of HLA-B27 homodimers. Arthritis Rheum 2002: 46: 2972-82.
29. Young NT, Uhrberg M, Phillips JH, Lanier LL, Parham P. Differential expression of leukocyte receptor complex-encoded Ig-like receptors correlates with the transition from effector to memory CTL. J Immunol 2001: 166: 3933-41.
30. 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: 161-6.
31. Tedla N, Bandeira-Melo C, Tassinari P et al. Activation of human eosinophils through leukocyte immunoglobulin-like receptor 7. Proc Natl Acad Sci USA 2003: 100: 1174-9.
32. 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: 1484-6.
33. Uehara T, Blery M, Kang DW et al. Inhibition of IgE-mediated mast cell activation by the paired Ig-like receptor PIR-B. J Clin Invest 2001: 108: 1041-50.
34. Forte P, Pazmany L, Matter-Reissmann UB, Stussi G, Schneider MK, Seebach JD. HLA-G inhibits rolling adhesion of activated human NK cells on porcine endothelial cells. J Immunol 2001: 167: 6002-8.
35. Bleharski JR, Li H, Meinken C et al. Use of genetic profiling in leprosy to discriminate clinical forms of the disease. Science 2003: 301: 1527-30.
36. Ju XS, Hacker C, Scherer B et al. Immunoglobulin-like transcripts ILT2, ILT3 and ILT7 are expressed by human dendritic cells and down-regulated following activation. Gene 2004: 331: 159-64.
37. Chang CC, Ciubotariu R, Manavalan JS et al. Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol 2002: 3: 237-43.
38. Cella M, Jarrossay D, Facchetti F et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 1999: 5: 919-23.
39. Penna G, Vulcano M, Roncari A, Facchetti F, Sozzani S, Adorini L. Cutting edge: differential chemokine production by myeloid and plasmacytoid dendritic cells. J Immunol 2002: 169: 6673-6.
40. Ujike A, Takeda K, Nakamura A, Ebihara S, Akiyama K, Takai T. Impaired dendritic cell maturation and increased T(H)2 responses in PIR-B(-/-) mice. Nat Immunol 2002: 3: 542-8.
41. Davis SJ, Ikemizu S, Evans EJ, Fugger L, Bakker TR, van der Merwe PA. The nature of molecular recognition by T cells. Nat Immunol 2003: 4: 217-24.
42. Nel AE, Slaughter N. T-cell activation through the antigen receptor. Part 2: role of signaling cascades in T-cell differentiation, anergy, immune senescence, and development of immunotherapy. J Allergy Clin Immunol 2002: 109: 901-15.
43. Beinhauer BG, McBride JM, Graf P 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.
44. Vlad G, Piazza F, Colovai A et al. Interleukin-10 induces the upregulation of the inhibitory receptor ILT4 in monocytes from HIV positive individuals. Hum Immunol 2003: 64: 483-9.
45. 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: 207-15.
46. Maeda A, Scharenberg AM, Tsukada S, Bolen JB, Kinet JP, Kurosaki T. Paired immunoglobulin-like receptor B (PIR-B) inhibits BCR-induced activation of Syk and Btk by SHP-1. Oncogene 1999: 18: 2291-7.
47. Rudge EU, Cutler AJ, Pritchard NR, Smith KG. Interleukin 4 reduces expression of inhibitory receptors on B cells and abolishes CD22 and Fc gamma RII-mediated B cell suppression. J Exp Med 2002: 195: 1079-85.
48. Berg L, Riise GC, Cosman D et al. LIR-1 expression on lymphocytes, and cytomegalovirus disease in lung-transplant recipients. Lancet 2003: 361: 1099-101.
49. Colonna M. Inhibitory receptors: friend or foe? Lancet 2003: 361: 1067-8.
50. Moreau P, Adrian-Cabestre F, Menier C et al. IL-10 selectively induces HLA-G expression in human trophoblasts and monocytes. Int Immunol 1999: 11: 803-11.
51. Hunt JS, Petroff MG, Morales P, Sedlmayr P, Geraghty DE, Ober C. HLA-G in reproduction: studies on the maternal-fetal interface. Hum Immunol 2000: 61: 1113-7.
52. Paul P, Cabestre FA, Le Gal FA et al. Heterogeneity of HLA-G gene transcription and protein expression in malignant melanoma biopsies. Cancer Res 1999: 59: 1954-60.
53. Lefebvre S, Antoine M, Uzan S et al. Specific activation of the non-classical class I histocompatibility HLA-G antigen and expression of the ILT2 inhibitory receptor in human breast cancer. J Pathol 2002: 196: 266-74.
54. Pangault C, Amiot L, Caulet-Maugendre S et al. HLA-G protein expression is not induced during malignant transformation. Tissue Antigens 1999: 53: 335-46.
55. Pangault C, Le Friec G, Caulet-Maugendre S et al. Lung macrophages and dendritic cells express HLA-G molecules in pulmonary diseases. Hum Immunol 2002: 63: 83-90.
56. Rouas-Freiss N, Moreau P, Menier C, Carosella ED. HLA-G in cancer: a way to turn off the immune system. Semin Cancer Biol 2003: 13: 325-36.
57. Urosevic M, Trojan A, Dummer R. HLA-G and its KIR ligands in cancer - another enigma yet to be solved? J Pathol 2002: 196: 252-3.
58. Bukur J, Rebmann V, Grosse-Wilde H et al. Functional role of human leukocyte antigen-G up-regulation in renal cell carcinoma. Cancer Res 2003: 63: 4107-11.
59. + cutaneous lymphomas. Am J Pathol 2001: 158: 1593-8.
60. Feldmann M, Maini RN. Anti-TNF alpha therapy of rheumatoid arthritis: what have we learned? Annu Rev Immunol 2001: 19: 163-96.
61. Tedla N, Gibson K, McNeil HP, Cosman D, Borges L, Arm JP. The co-expression of activating and inhibitory leukocyte immunoglobulin-like receptors in rheumatoid synovium. Am J Pathol 2002: 160: 425-31.
62. Allen RL, Bowness P, McMichael A. The role of HLA-B27 in spondyloarthritis. Immunogenetics 1999: 50: 220-7.
63. Allen RL, Trowsdale J. Recognition of classical and heavy chain forms of HLA-B27 by leukocyte receptors. Curr Mol Med 2004: 4: 59-65.
64. Moodie SJ, Norman PJ, King AL et al. Analysis of candidate genes on chromosome 19 in coeliac disease: an association study of the KIR and LILR gene clusters. Eur J Immunogenet 2002: 29: 287-91.
65. Liang S, Baibakov B, Horuzsko A. HLA-G inhibits the functions of murine dendritic cells via the PIR-B immune inhibitory receptor. Eur J Immunol 2002: 32: 2418-26.
66. Forte P, Matter-Reissmann UB, Strasser M, Schneider MK, Seebach JD. Porcine aortic endothelial cells transfected with HLA-G are partially protected from xenogeneic human NK cytotoxicity. Hum Immunol 2000: 61: 1066-73.
67. Ishitani A, Sageshima N, Lee N et al. Protein expression and peptide binding suggest unique and interacting functional roles for HLA-E, F, and G in maternal-placental immune recognition. J Immunol 2003: 171: 1376-84.
68. King A, Burrows TD, Hiby SE et al. Surface expression of HLA-C antigen by human extravillous trophoblast. Placenta 2000: 21: 376-87.
69. Rajagopalan S, Long EO. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J Exp Med 1999: 189: 1093-100.
70. Petroff MG, Sedlmayr P, Azzola D, Hunt JS. Decidual macrophages are potentially susceptible to inhibition by class Ia and class Ib HLA molecules. J Reprod Immunol 2002: 56: 3-17.
71. Ponte M, Cantoni C, Biassoni R et al. Inhibitory receptors sensing HLA-G1 molecules in pregnancy: decidua-associated natural killer cells express LIR-1 and CD94/NKG2A and acquire p49, an HLA-G1-specific receptor. Proc Natl Acad Sci USA 1999: 96: 5674-9.
72. Chapman TL, Heikema AP, West AP Jr, Bjorkman PJ. Crystal structure and ligand binding properties of the D1D2 region of the inhibitory receptor LIR-1 (ILT2). Immunity 2000: 13: 727-36.
73. 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: 5192-6.