Mannose receptor expression and function define a new population of murine dendritic cells

Journal of Immunology

Volumn 178, Issue 8, 2007, Pages 4975-4983

  McKenzie, Emma J ^a,b   Taylor, Philip R ^a   Stillion, Richard J ^a   Lucas, Andrew D ^a,c   Harris, James ^a,d   Gordon, Siamon ^a   Martinez Pomares, Luisa ^a,e  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c MURDOCH UNIVERSITY   (Australia)

^d ST JAMES S HOSPITAL   (Ireland)

^e UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MANNOSE RECEPTOR;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CELL POPULATION; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; HUMORAL IMMUNITY; IMMUNOGENICITY; INNATE IMMUNITY; LYMPH NODE; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN; T LYMPHOCYTE;

EID: 34247174971     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.8.4975     Document Type: Article

References (54)

1. Pugh, C. W., G. G. MacPherson, and H. W. Steer. 1983. Characterization of nonlymphoid cells derived from rat peripheral lymph. J. Exp. Med. 157: 1758-1779.
2. Huang, F.-P., N. Platt, M. Wykes, J. R. Major, T. J. Powell, C. D. Jenkins, and G. G. MacPherson. 2000. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J. Exp. Med. 191: 435-444.
3. Lee, S. J., S. Evers, D. Roeder, A. F. Parlow, J. Risteli, L. Risteli, Y. C. Lee, T. Feizi, H. Langen, and M. C. Nussenzweig. 2002. Mannose receptor-mediated regulation of serum glycoprotein homeostasis. Science 295: 1898-1901.
4. Leteux, C., W. Chai, R. W. Loveless, C. T. Yuen, L. Uhlin-Hansen, Y. Combarnous, M. Jankovic, S. C. Marie, Z. Misulovin, M. C. Nussenzweig, and T. Feizi. 2000. The cysteine-rich domain of the macrophage mannose receptor is a multispecific lectin that recognizes chondroitin sulfates A and B and sulfated oligosaccharides of blood group Lewis(a) and Lewis(s) types in addition to the sulfated N-glycans of lutropin. J. Exp. Med. 191: 1117-1126.
5. Liu, Y., A. J. Chirino, Z. Misulovin, C. Leteux, T. Feizi, M. C. Nussenzweig, and P. J. Bjorkman. 2000. Crystal structure of the cysteine-rich domain of mannose receptor complexed with a sulfated carbohydrate ligand. J. Exp. Med. 191: 1105-1116.
6. Martinez-Pomares, L., D. Wienke, R. Stillion, E. J. McKenzie, J. N. Arnold, J. Harris, E. McGreal, R. B. Sim, C. M. Isacke, and S. Gordon. 2006. Carbohydrate-independent recognition of collagens by the macrophage mannose receptor. Eur. J. Immunol. 36: 1074-1082.
7. Taylor, P. R., L. Martinez-Pomares, M. Stacey, H. H. Lin, G. D. Brown, and S. Gordon. 2005. Macrophage receptors and immune recognition. Annu. Rev. Immunol. 23: 901-944.
8. Linehan, S. A., L. Martinez-Pomares, P. D. Stahl, and S. Gordon. 1999. Mannose receptor and its putative ligands in normal murine lymphoid and nonlymphoid organs: in situ expression of mannose receptor by selected macrophages, endothelial cells, perivascular microglia, and mesangial cells, but not dendritic cells. J. Exp. Med. 189: 1961-1972.
9. Engering, A., T. B. Geijtenbeek, S. J. van Vliet, M. Wijers, E. van Liempt, N. Demaurex, A. Lanzavecchia, J. Fransen, C. G. Figdor, V. Piguet, and Y. van Kooyk. 2002. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J. Immunol. 168: 2118-2126.
10. Wollenberg, A., M. Mommaas, T. Oppel, E. M. Schottdorf, S. Gunther, and M. Moderer. 2002. Expression and function of the mannose receptor CD206 on epidermal dendritic cells in inflammatory skin diseases. J. Invest. Dermatol. 118: 327-334.
11. Martinez-Pomares, L., L. G. Hanitsch, R. Stillion, S. Keshav, and S. Gordon. 2005. Expression of mannose receptor and ligands for its cysteine-rich domain in venous sinuses of human spleen. Lab. Invest. 85: 1238-1249.
12. 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.
13. Prigozy, T. I., P. A. Sieling, D. Clemens, P. L. Stewart, S. M. Behar, S. A. Porcelli, M. B. Brenner, R. L. Modlin, and M. Kronenberg. 1997. The mannose receptor delivers lipoglycan antigens to endosomes for presentation to T cells by CD1b molecules. Immunity 6: 187-197.
14. Engering, A. J., M. Cella, D. Fluitsma, M. Brockhaus, E. C. Hoefsmit, A. Lanzavecchia, and J. Pieters. 1997. The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells. Eur. J. Immunol. 27: 2417-2425.
15. Tan, M. C., A. M. Mommaas, J. W. Drijfhout, R. Jordens, J. J. Underwater, D. Verwoerd, A. A. Mulder, A. N. van der Heiden, D. Scheidegger, L. C. Oomen, et al. 1997. Mannose receptor-mediated uptake of antigens strongly enhances HLA class II-restricted antigen presentation by cultured dendritic cells. Eur. J. Immunol. 27: 2426-2435.
16. Mommaas, A. M., A. A. Mulder, R. Jordens, C. Out, M. C. Tan, P. Cresswell, P. M. Kluin, and F. Koning. 1999. Human epidermal Langerhans cells lack functional mannose receptors and a fully developed endosomal/lysosomal compartment for loading of HLA class II molecules. Eur. J. Immunol. 29: 571-580.
17. Ramakrishna, V., J. F. Treml, L. Vitale, J. E. Connolly, T. O'Neill, P. A. Smith, C. L. Jones, L. Z. He, J. Goldstein, P. K. Wallace, et al. 2004. Mannose receptor targeting of tumor antigen pmel17 to human dendritic cells directs anti-melanoma T cell responses via multiple HLA molecules. J. Immunol. 172: 2845-2852.
18. Mahnke, K., M. Guo, S. Lee, H. Sepulveda, S. L. Swain, M. Nussenzweig, and R. M. Steinman. 2000. The dendritic cell receptor for endocytosis, DEC-205, can recycle and enhance antigen presentation via major histocompatibility complex class II-positive lysosomal compartments. J. Cell Biol. 151; 673-684.
19. Burgdorf, S., V. Lukacs-Kornek, and C. Kurts. 2006. The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J. Immunol. 176: 6770-6776.
20. Napper, C. E., and M. E. Taylor. 2004 The mannose receptor fails to enhance processing and presentation of a glycoprotein antigen in transfected fibroblasts. Glycobiology 14: 7C-12C.
21. Lam, J. S., M. K. Mansour, C. A. Specht, and S. M. Levitz. 2005. A model vaccine exploiting fungal mannosylation to increase antigen immunogenicity. J. Immunol. 175: 7496-7503.
22. Linehan, S. A., L. Martinez-Pomares, R. P. da Silva, and S. Gordon. 2001. Endogenous ligands of carbohydrate recognition domains of the mannose receptor in murine macrophages, endothelial cells and secretory cells; potential relevance to inflammation and immunity. Eur. J. Immunol. 31: 1857-1866.
23. Roitt, I., D. Doniach, R. Campbell, and R. Hudson. 1956. Autoantibodies in Hashimoto's disease (lymphadenoid goitre). Lancet 2: 820-821.
24. Savige, J., M. Gallicchio, T. Georgiou, and D. Davies. 1990. Diverse target antigens recognized by circulating antibodies in anti-neutrophil cytoplasm antibody-associated renal vasculitides. Clin. Exp. Immunol. 82: 238-243.
25. Corrigall, V. M., and G. S. Panayi. 2002. Autoantigens and immune pathways in rheumatoid arthritis. Crit. Rev. Immunol. 22: 281-293.
26. Wang, X.-P., A. B. Fogo, S. Colon, G. Giannico, S. R. Abul-Ezz, J. H. Miner, and D.-B. Borza. 2005. Distinct epitopes for anti-glomerular basement membrane Alport alloantibodies and Goodpasture autoantibodies within the noncollagenous domain of α3(IV) collagen: a Janus-faced antigen. J. Am. Soc. Nephrol. 16: 3563-3571.
27. Henri, S., D. Vremec, A. Kamath, J. Waithman, S. Williams, C. Benoist, K. Burnham, S. Saeland, E. Handman, and K. Shortman. 2001. The dendritic cell populations of mouse lymph nodes. J. Immunol. 167: 741-748.
28. Berney, C., S. Herren, C. A. Power, S. Gordon, L. Martinez-Pomares, and M. H. Kosco-Vilbois. 1999. A member of the dendritic cell family that enters B cell follicles and stimulates primary antibody responses identified by a mannose receptor fusion protein. J. Exp. Med. 190: 851-860.
29. Mueller, C. G., I. Cremer, P. E. Paulet, S. Niida, N. Maeda, S. Lebeque, W. H. Fridman, and C. Sautes-Fridman. 2001. Mannose receptor ligand-positive cells express the metalloprotease decysin in the B cell follicle. J. Immunol. 167: 5052-5060.
30. Yu, P., Y. Wang, R. K. Chin, L. Martinez-Pomares, S. Gordon, M. H. Kosco-Vibois, J. Cyster, and Y. X. Fu. 2002. B cells control the migration of a subset of dendritic cells into B cell follicles via CXC chemokine ligand 13 in a lymphotoxin-dependent fashion. J. Immunol. 168: 5117-5123.
31. Martinez-Pomares, L., J. A. Mahoney, R. Kaposzta, S. A. Linehan, P. D. Stahl, and S. Gordon. 1998. A functional soluble form of the murine mannose receptor is produced by macrophages in vitro and is present in mouse serum. J. Biol. Chem. 273: 23376-23380.
32. MacPherson, G. G., C. D. Jenkins, M. J. Stein, and C. Edwards. 1995. Endotoxin-mediated dendritic cell release from the intestine. Characterization of released dendritic cells and TNF dependence. J. Immunol. 154; 1317-1322.
33. Roake, J. A., A. S. Rao, P. J. Morris, C. P. Larsen, D. F. Hankins, and J. M. Austyn. 1995. Dendritic cell loss from nonlymphoid tissues after systemic administration of lipopolysaccharide, tumor necrosis factor, and interleukin 1. J. Exp. Med. 181: 2237-2247.
34. De Smedt, T., B. Pajak, E. Muraille, L. Lespagnard, E. Meinen, P. De Baetselier, J. Urbain, O. Leo, and M. Moser. 1996. Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. J. Exp. Med. 184: 1413-1424.
35. Reis e Sousa, C., S. Hieny, T. Scharton-Kersten, D. Jankovic, H. Charest, R. N. Germain, and A. Sher. 1997. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med. 186: 1819-1829.
36. Suzuki, H., B. Wang, G. M. Shivji, P. Toto, P. Amerio, M. A. Tomai, R. L. Miller, and D. N. Sauder, 2000. Imiquimod, a topical immune response modifier, induces migration of Langerhans cells. J. Invest. Dermatol. 114: 135-141.
37. - dendritic cells. J. Immunol. 171: 1156-1163.
38. Turnbull, E. L., U. Yrlid, C. D. Jenkins, and G. G. Macpherson. 2005. Intestinal dendritic cell subsets: differential effects of systemic TLR4 stimulation on migratory fate and activation in vivo. J. Immunol. 174: 1374-1384.
39. Martinez-Pomares, L., D. M. Reid, G. D. Brown, P. R. Taylor, R. J. Stillion, S. A. Linehan, S. Zamze, S. Gordon, and S. Y. Wong. 2003. Analysis of mannose receptor regulation by IL-4, IL-10, and proteolytic processing using novel monoclonal antibodies. J. Leukocyte Biol. 73: 604-613.
40. Finkelman, F. D., A. Lees, R. Birnbaum, W. C. Gause, and S. C. Morris. 1996. Dendritic cells can present antigen in vivo in a tolerogenic or immunogenic fashion. J. Immunol. 157: 1406-1414.
41. Carayanniotis, G., and B. H. Barber. 1987. Adjuvant-free IgG responses induced with antigen coupled to antibodies against class II MHC. Nature 327: 59-61.
42. Lunde, E., K. H. Western, I. B. Rasmussen, I. Sandlie, and B. Bogen. 2002. Efficient delivery of T cell epitopes to APC by use of MHC class II-specific Troybodies. J. Immunol. 168: 2154-2162.
43. Hawiger, D., K. Inaba, Y. Dorse«, M. Guo, K. Mahnke, M. Rivera, J. V. Ravetch, R. M. Steinman, and M. C. Nussenzweig. 2001. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194: 769-779.
44. + T cell tolerance. J. Exp. Med. 196: 1627-1638.
45. Tacken, P. J., I. J. de Vries, K. Gijzen, B. Joosten, D. Wu, R. P. Rother, S. J. Faas, C. J. Punt, R. Torensma, G. J. Adema, and C. G. Figdor. 2005. Effective induction of naive and recall T-cell responses by targeting antigen to human dendritic cells via a humanized anti-DC-SIGN antibody. Blood 106: 1278-1285.
46. - dendritic cell subset induces humoral immunity in the absence of conventional "danger". Eur. J. Immunol. 35: 2815-2825.
47. + dendritic cells and antigen-specific CD4 T cells after subcutaneous injection of antigen. J. Immunol. 169: 2247-2252.
48. Gretz, J. E., C. C. Norbury, A. O. Anderson, A. E. Proudfoot, and S. Shaw. 2000. Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venuies via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J. Exp. Med. 192: 1425-1440.
49. Bonifaz, L. C., D. P. Bonnyay, A. Charalambous, D. I. Darguste, S.-I. Fujii, H. Soares, M. K. Brimnes, B. Moltedo, T. M. Moran, and R. M. Steinman. 2004. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J. Exp. Med. 199: 815-824.
50. Swain, S. D., S. J. Lee, M. C. Nussenzweig, and A. G. Harmsen. 2003. Absence of the macrophage mannose receptor in mice does not increase susceptibility to Pneumocystis carinii infection in vivo. Infect. Immun. 71: 6213-6221.
51. Lee, S. J., N. Y. Zheng, M. Clavijo, and M. C. Nussenzweig. 2003. Normal host defense during systemic candidiasis in mannose receptor-deficient mice. Infect. Immun. 71: 437-445.
52. Chieppa, M., G. Bianchi, A. Doni, A. Del Prete, M. Sironi, G. Laskarin, P. Monti, L. Piemonti, A. Biondi, A. Mantovani, et al. 2003. Cross-linking of the mannose receptor on monocyte-derived dendritic cells activates an anti-inflammatory immunosuppressive program. J. Immunol. 171: 4552-4560.
53. Taylor, P. R., S. Zamze, R. J. Stillion, S. Y. Wong, S. Gordon, and L. Martinez-Pomares. 2004. Development of a specific system for targeting protein to metallophilic macrophages. Proc. Natl. Acad. Sci. USA 101: 1963-1968.
54. Taylor, P. R., S. Gordon, and L. Martinez-Pomares. 2005. The mannose receptor: linking homeostasis and immunity through sugar recognition. Trends Immunol. 26: 104-110.