LILRA2 activation inhibits dendritic cell differentiation and antigen presentation to T cells

Journal of Immunology

Volumn 179, Issue 12, 2007, Pages 8128-8136

  Lee, Delphine J ^a   Sieling, Peter A ^a   Ochoa, Maria Teresa ^a   Krutzik, Stephan R ^a   Guo, Beichu ^b   Hernandez, Maristela ^d   Rea, Thomas H ^c   Cheng, Genhong ^a,b   Colonna, Marco ^d   Modlin, Robert L ^a,b,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD1B ANTIGEN; CD40 ANTIGEN; CHLORDANE; IMMUNOGLOBULIN RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; INTERLEUKIN 8; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTOR A2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ANTIBODY; CYTOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; LILRA2 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ANTIBODY LABELING; ANTIGEN PRESENTATION; ARTICLE; BLOOD SAMPLING; CELL DIFFERENTIATION; CELL PROLIFERATION; COLONY FORMING UNIT GM; DENDRITIC CELL; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INNATE IMMUNITY; LEPROSY; MACROPHAGE; MONOCYTE; MYCOBACTERIUM LEPRAE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN BIOPSY; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; CELL CULTURE; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM;

ANTIBODIES; ANTIGEN PRESENTATION; CELL DIFFERENTIATION; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; LYMPHOCYTE ACTIVATION; MONOCYTES; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTES;

EID: 40049098041     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.12.8128     Document Type: Article

References (59)

1. Martin-Fontecha, A., S. Sebastiani, U. E. Hopken, M. Uguccioni, M. Lipp, A. Lanzavecchia, and F. Sallusto. 2003. Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J. Exp. Med. 198: 615-621.
2. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
3. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor α. J. Exp. Med. 179: 1109-1118.
4. Ochoa, M. T., S. Stenger, P. A. Sieling, S. Thoma-Uszynski, S. Sabet, S. Cho, A. M. Krensky, M. Rollinghoff, S. E. Nunes, A. E. Burdick, et al. 2001. T-cell release of granulysin contributes to host defense in leprosy. Nat. Med. 7: 174-179.
5. Sieling, P. A., J. B. Torrelles, S. Stenger, W. Chung, A. E. Burdick, T. H. Rea, P. J. Brennan, J. T. Belisle, S. A. Porcelli, and R. L. Modlin. 2005. The human CD1-restricted T cell repertoire is limited to cross-reactive antigens: implications for host responses against immunologically related pathogens. J. Immunol. 174: 2637-2644.
6. Ridley, D. S., and W. H. Jopling. 1966. Classification of leprosy according to immunity: a five-group system. Int. J. Lepr. Other Mycobact. Dis. 34: 255-273.
7. Samaridis, J., and M. Colonna. 1997. Cloning of novel immunoglobulin superfamily receptors expressed on human myeloid and lymphoid cells: structural evidence for new stimulatory and inhibitory pathways. Eur. J. Immunol. 27: 660-665.
8. Borges, L., M. L. Hsu, N. Fanger, M. Kubin, and D. Cosman. 1997. A family of human lymphoid and myeloid Ig-like receptors, some of which bind to MHC class I molecules. J. Immunol. 159: 5192-5196.
9. Wagtmann, N., S. Rojo, E. Eichler, H. Mohrenweiser, and E. O. Long. 1997. A new human gene complex encoding the killer cell inhibitory receptors and related monocyte/macrophage receptors. Curr. Biol. 7: 615-618.
10. Bleharski, J. R., H. Li, C. Meinken, T. G. Graeber, M. T. Ochoa, M. Yamamura, A. Burdick, E. N. Sarno, M. Wagner, M. Rollinghoff, et al. 2003. Use of genetic profiling in leprosy to discriminate clinical forms of the disease. Science 301: 1527-1530.
11. Borges, L., and D. Cosman. 2000. LIRs/ILTs/MIRs, inhibitory and stimulatory Ig-superfamily receptors expressed in myeloid and lymphoid cells. Cytokine Growth Factor Rev. 11: 209-217.
12. Arm, J. P., C. Nwankwo, and K. F. Austen. 1997. 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. 159: 2342-2349.
13. Cella, M., D. Jarrossay, F. Facchetti, O. Alebardi, H. Nakajima, A. Lanzavecchia, and M. Colonna. 1999. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med. 5: 919-923.
14. Brown, D., J. Trowsdale, and R. Allen. 2004. The LILR family: modulators of innate and adaptive immune pathways in health and disease. Tissue Antigens 64: 215-225.
15. Beckman, E. M., A. Melian, S. M. Behar, P. A. Sieling, D. Chatterjee, S. T. Furlong, R. Matsumoto, J. P. Rosat, R. L. Modlin, and S. A. Porcelli. 1996. CD1c restricts responses of mycobacteria-specific T cells: evidence for antigen presentation by a second member of the human CD1 family. J. Immunol. 157: 2795-2803.
16. Kim, J., A. Sette, S. Rodda, S. Southwood, P. A. Sieling, V. Mehra, J. D. Ohmen, J. Oliveros, E. Appella, Y. Higashimoto, et al. 1997. Determinants of T cell reactivity to the Mycobacterium leprae GroES homologue. J. Immunol. 159: 335-343.
17. Colonna, M., F. Navarro, T. Bellon, M. Llano, P. Garcia, J. Samaridis, L. Angman, M. Cella, and M. Lopez-Botet. 1997. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med. 186: 1809-1818.
18. Behar, S. M., S. A. Porcelli, E. M. Beckman, and M. B. Brenner. 1995. A pathway of costimulation that prevents anergy in CD28-T cells: B7-independent costimulation of CD1-restricted T cells. J. Exp. Med. 182: 2007-2018.
19. Modlin, R. L., F. M. Hofman, D. A. Horwitz, L. A. Husmann, S. Gillis, C. R. Taylor, and T. H. Rea. 1984. In situ identification of cells in human leprosy granulomas with monoclonal antibodies to interleukin 2 and its receptor. J. Immunol. 132: 3085-3090.
20. Sieling, P. A., D. Chatterjee, S. A. Porcelli, T. I. Prigozy, R. J. Mazzaccaro, T. Soriano, B. R. Bloom, M. B. Brenner, M. Kronenberg, and P. J. Brennan. 1995. CD1-restricted T cell recognition of microbial lipoglycan antigens. Science 269: 227-230.
21. Mehra, V., B. R. Bloom, A. C. Bajardi, C. L. Grisso, P. A. Sieling, D. Alland, J. Convit, X. D. Fan, S. W. Hunter, and P. J. Brennan. 1992. A major T cell antigen of Mycobacterium leprae is a 10-kD heat-shock cognate protein. J. Exp. Med. 175: 275-284.
22. Sieling, P. A., D. Jullien, M. Dahlem, T. F. Tedder, T. H. Rea, R. L. Modlin, and S. A. Porcelli. 1999. CD1 expression by dendritic cells in human leprosy lesions: correlation with effective host immunity. J. Immunol. 162: 1851-1858.
23. Burshtyn, D. N., A. M. Scharenberg, N. Wagtmann, S. Rajagopalan, K. Berrada, T. Yi, J. P. Kinet, and E. O. Long. 1996. Recruitment of tyrosine phosphatase HCP by the killer cell inhibitor receptor. Immunity 4: 77-85.
24. Fanger, N. A., D. Cosman, L. Peterson, S. C. Braddy, C. R. Maliszewski, and L. Borges. 1998. The MHC class I binding proteins LIR-1 and LIR-2 inhibit Fc receptor-mediated signaling in monocytes. Eur. J. Immunol. 28: 3423-3434.
25. Nakajima, H., J. Samaridis, L. Angman, and M. Colonna. 1999. Human myeloid cells express an activating ILT receptor (ILT1) that associates with Fc receptor γ-chain. J. Immunol. 162: 5-8.
26. Werlen, G., B. Hausmann, and E. Palmer. 2000. A motif in the αβ T-cell receptor controls positive selection by modulating ERK activity. Nature 406: 422-426.
27. Hesslein, D. G., R. Takaki, M. L. Hermiston, A. Weiss, and L. L. Lanier. 2006. Dysregulation of signaling pathways in CD45-deficient NK cells leads to differentially regulated cytotoxicity and cytokine production. Proc. Natl. Acad. Sci. USA 103: 7012-7017.
28. Young, D. A., L. D. Lowe, and S. C. Clark. 1990. Comparison of the effects of IL-3, granulocyte-macrophage colony-stimulating factor, and macrophage colony-stimulating factor in supporting monocyte differentiation in culture: analysis of macrophage antibody-dependent cellular cytotoxicity. J. Immunol. 145: 607-615.
29. Markowicz, S., and E. G. Engleman. 1990. Granulocyte-macrophage colony-stimulating factor promotes differentiation and survival of human peripheral blood dendritic cells in vitro. J. Clin. Invest. 85: 955-961.
30. Krutzik, S. R., B. Tan, H. Li, M. T. Ochoa, P. T. Liu, S. E. Sharfstein, T. G. Graeber, P. A. Sieling, Y. J. Liu, T. H. Rea, et al. 2005. TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells. Nat. Med. 11: 653-660.
31. Granelli-Piperno, A., A. Pritsker, M. Pack, I. Shimeliovich, J. F. Arrighi, C. G. Park, C. Trumpfheller, V. Piguet, T. M. Moran, and R. M. Steinman. 2005. Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin/CD209 is abundant on macrophages in the normal human lymph node and is not required for dendritic cell stimulation of the mixed leukocyte reaction. J. Immunol. 175: 4265-4273.
32. van Lent, P. L., C. G. Figdor, P. Barrera, K. van Ginkel, A. Sloetjes, W. B. van den Berg, and R. Torensma. 2003. Expression of the dendritic cell-associated C-type lectin DC-SIGN by inflammatory matrix metalloproteinaseproducing macrophages in rheumatoid arthritis synovium and interaction with intercellular adhesion molecule 3-positive T cells. Arthritis Rheum. 48: 360-369.
33. Goyert, S. M., E. Ferrero, W. J. Rettig, A. K. Yenamandra, F. Obata, and M. M. Le Beau. 1988. The CD14 monocyte differentiation antigen maps to a region encoding growth factors and receptors. Science 239: 497-500.
34. Lee, S. H., P. R. Crocker, S. Westaby, N. Key, D. Y. Mason, S. Gordon, and D. J. Weatherall. 1988. Isolation and immunocytochemical characterization of human bone marrow stromal macrophages in hemopoietic clusters. J. Exp. Med. 168: 1193-1198.
35. Baumgartner, I., O. Scheiner, C. Holzinger, G. Boltz-Nitulescu, H. Klech, H. Lassmann, H. Rumpold, O. Forster, and D. Kraft. 1988. Expression of the VEP13 antigen (CD16) on native human alveolar macrophages and cultured blood monocytes. Immunobiology 177: 317-326.
36. Becker, S., and E. G. Daniel. 1990. Antagonistic and additive effects of IL-4 and interferon-γ on human monocytes and macrophages: effects on Fc receptors, HLA-D antigens, and superoxide production. Cell. Immunol. 129: 351-362.
37. + T cells during Mycobacterium tuberculosis infection. J. Immunol. 167: 6991-7000.
38. Caruso, A. M., N. Serbina, E. Klein, K. Triebold, B. R. Bloom, and J. L. Flynn. 1999. Mice deficient in CD4 T cells have only transiently diminished levels of IFN-γ, yet succumb to tuberculosis. J. Immunol. 162: 5407-5416.
39. Salgame, P. 2005. Host innate and Th1 responses and the bacterial factors that control Mycobacterium tuberculosis infection. Curr. Opin. Immunol. 17: 374-380.
40. Sallusto, F., M. Cella, C. Danieli, and A. Lanzavecchia. 1995. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J. Exp. Med. 182: 389-400.
41. Reddy, A., M. Sapp, M. Feldman, M. Subklewe, and N. Bhardwaj. 1997. A monocyte conditioned medium is more effective than defined cytokines in mediating the terminal maturation of human dendritic cells. Blood 90: 3640-3646.
42. Romani, N., D. Reider, M. Heuer, S. Ebner, E. Kampgen, B. Eibl, D. Niederwieser, and G. Schuler. 1996. Generation of mature dendritic cells from human blood: an improved method with special regard to clinical applicability. J. Immunol. Methods 196: 137-151.
43. Matzinger, P. 2002. The danger model: a renewed sense of self. Science 296: 301-305.
44. Samelson, L. E. 2002. Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu. Rev. Immunol. 20: 371-394.
45. McVicar, D. W., and D. N. Burshtyn. 2001. Intracellular signaling by the killer immunoglobulin-like receptors and Ly49. Sci. STKE 2001: RE1.
46. Isakov, N. 1998. ITAMs: immunoregulatory scaffolds that link immunoreceptors to their intracellular signaling pathways. Recept. Channels 5: 243-253.
47. Humphrey, M. B., L. L. Lanier, and M. C. Nakamura. 2005. Role of ITAM-containing adapter proteins and their receptors in the immune system and bone. Immunol. Rev. 208: 50-65.
48. Hamerman, J. A., and L. L. Lanier. 2006. Inhibition of immune responses by ITAM-bearing receptors. Sci. STKE 2006: RE1.
49. -/- mice. Nat. Immunol. 3: 542-548.
50. Hamerman, J. A., J. R. Jarjoura, M. B. Humphrey, M. C. Nakamura, W. E. Seaman, and L. L. Lanier. 2006. Cutting edge: inhibition of TLR and FcR responses in macrophages by triggering receptor expressed on myeloid cells TREM-2 and DAP12. J. Immunol. 177: 2051-2055.
51. Bakker, A. B., E. Baker, G. R. Sutherland, J. H. Phillips, and L. L. Lanier. 1999. Myeloid DAP12-associating lectin (MDL)-1 is a cell surface receptor involved in the activation of myeloid cells. Proc. Natl. Acad. Sci. USA 96: 9792-9796.
52. Bakker, A. B., R. M. Hoek, A. Cerwenka, B. Blom, L. Lucian, T. McNeil, R. Murray, L. H. Phillips, J. D. Sedgwick, and L. L. Lanier. 2000. DAP12-deficient mice fail to develop autoimmunity due to impaired antigen priming. Immunity 13: 345-353.
53. Krutzik, S. R., M. T. Ochoa, P. A. Sieling, S. Uematsu, Y. W. Ng, A. Legaspi, P. T. Liu, S. T. Cole, P. J. Godowski, Y. Maeda, et al. 2003. Activation and regulation of toll-like receptors 2 and 1 in human leprosy. Nat. Med. 9: 525-532.
54. Modlin, R. L., J. Melancon-Kaplan, S. M. Young, C. Pirmez, H. Kino, J. Convit, T. H. Rea, and B. R. Bloom. 1988. Learning from lesions: patterns of tissue inflammation in leprosy. Proc. Natl. Acad. Sci. USA 85: 1213-1217.
55. Allan, D. S., M. Colonna, L. L. Lanier, T. D. Churakova, J. S. Abrams, S. A. Ellis, A. J. McMichael, and V. M. Braud. 1999. Tetrameric complexes of human histocompatibility leukocyte antigen (HLA)-G bind to peripheral blood myelomonocytic cells. J. Exp. Med. 189: 1149-1156.
56. Chapman, T. L., A. P. Heikeman, and P. J. Bjorkman. 1999. The inhibitory receptor LIR-1 uses a common binding interaction to recognize class I MHC molecules and the viral homolog UL18. Immunity 11: 603-613.
57. Colonna, M., J. Samaridis, M. Cella, L. Angman, R. L. Allen, C. A. O'Callaghan, R. Dunbar, G. S. Ogg, V. Cerundolo, and A. Rolink. 1998. Human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules. J. Immunol. 160: 3096-3100.
58. Cosman, D., N. Fanger, L. Borges, M. Kubin, W. Chin, L. Peterson, and M. L. Hsu. 1997. A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7: 273-282.
59. Allen, R. L., T. Raine, A. Haude, J. Trowsdale, and M. J. Wilson. 2001. Leukocyte receptor complex-encoded immunomodulatory receptors show differing specificity for alternative HLA-B27 structures. J. Immunol. 167: 5543-5547.