Mycobacterium tuberculosis impairs dendritic cell response by altering CD1b, DC-SIGN and MR profile

Immunology and Cell Biology

Volumn 88, Issue 7, 2010, Pages 716-726

  Balboa, Luciana ^a   Romero, María Mercedes ^a   Yokobori, Noemí ^a   Schierloh, Pablo ^a   Geffner, Laura ^a   Basile, Juan I ^a   Musella, Rosa M ^b   Abbate, Eduardo ^a   De La Barrera, Silvia ^a   Sasiain, María C ^a   Alemán, Mercedes ^a  

^a INST DE INVEST HEMATOLOGICAS   (Argentina)

^b HOSPITAL F J MUÑIZ   (Argentina)

Author keywords

antigen presentation; immune evasion; monocyte differentiation; Mycobacteriatuberculosis

Indexed keywords

CD1B ANTIGEN; CD209 ANTIGEN; CD86 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE P38; TOLL LIKE RECEPTOR 2;

ADULT; ANTIGEN PRESENTATION; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL POPULATION; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; GAMMA IRRADIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MONOCYTE; MYCOBACTERIUM TUBERCULOSIS;

ADULT; ANTIGENS, CD1; ANTIGENS, CD86; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DENDRITIC CELLS; HUMANS; INTERLEUKIN-10; LECTINS, C-TYPE; LYMPHOCYTE CULTURE TEST, MIXED; MACROPHAGES; MANNOSE-BINDING LECTINS; MIDDLE AGED; MYCOBACTERIUM TUBERCULOSIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, CELL SURFACE; TOLL-LIKE RECEPTOR 2; TUBERCULOSIS;

MYCOBACTERIUM TUBERCULOSIS;

EID: 77957842399     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2010.22     Document Type: Article

References (46)

1. Fenton MJ, Vermeulen MW. Immunopathology of tuberculosis: roles of macrophages and monocytes. Infect Immun 1996; 64: 683-690.
2. Holt PG. Pulmonary dendritic cells in local immunity to inert and pathogenic antigens in the respiratory tract. Proc Am Thorac Soc 2005; 2: 116-120.
3. Muller WA, Randolph GJ. Migration of leukocytes across endothelium and beyond: molecules involved in the transmigration and fate of monocytes. J Leukoc Biol 1999; 66: 698-704.
4. Gordon S. Macrophage-restricted molecules: role in differentiation and activation. Immunol Lett 1999; 65: 5-8.
5. Mariotti S, Teloni R, Iona E, Fattorini L, Romagnoli G, Gagliardi MC et al. Mycobacter-ium tuberculosis diverts alpha interferon-induced monocyte differentiation from den-dritic cells into immunoprivileged macrophage-like host cells. Infect Immun 2004; 72: 4385-4392.
6. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ et al. Immunobiology of dendritic cells. Annu Rev Immunol 2000; 18: 767-811.
7. Sallusto F, Lanzavecchia A. 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 necrosisfactor alpha. J Exp Med 1994; 179: 1109-1118.
8. Cutler CW, Jotwani R, Pulendran B. Dendritic cells: immune saviors or Achilles' heel? Infect Immun 2001; 69: 4703-4708.
9. Stenger S, Niazi KR, Modlin RL. Down-regulation of CD1 on antigen-presentingcells by infection with Mycobacterium tuberculosis. J Immunol 1998; 161: 3582-3588.
10. Flynn JL, Chan J. Immune evasion by Mycobacterium tuberculosis: living with the enemy. Curr Opin Immunol 2003; 15: 450-455.
11. Trajkovic V, Natarajan K, Sharma P. Immunomodulatory action of mycobacterial secretoryproteins. Microbes Infect 2004; 6: 513-519.
12. Gagliardi MC, Teloni R, Giannoni F, Pardini M, Sargentini V, Brunori L et al. Myco-bacterium bovis Bacillus Calmette-Guerin infects DC-SIGN-dendritic cell and causes the inhibition ofIL-12 and theenhancement of IL-10 production. J Leukoc Biol 2005; 78: 106-113.
13. Mariotti S, Teloni R, Iona E, Fattorini L, Giannoni F, Romagnoli G et al. Mycobacterium tuberculosis subverts the differentiation of human monocytes into dendritic cells. Eur J Immunol 2002; 32: 3050-3058.
14. Ernst JD. Macrophagereceptors for Mycobacteriumtuberculosis. Infect Immun 1998; 66: 1277-1281.
15. Tailleux L, Schwartz O, Herrmann JL, Pivert E, Jackson M, Amara A et al. DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 2003; 197: 121-127.
16. Berrington WR, Hawn TR. Mycobacterium tuberculosis, macrophages, and the innate immune response: does common variation matter? Immunol Rev 2007; 219: 167-186.
17. Geijtenbeek TB, van Vliet SJ, Engering A, t Hart BA, van Kooyk Y. Self-and nonself-recognition byC-type lectins on dendritic cells. Annu Rev Immunol 2004; 22: 33-54.
18. Moody DB. TLR gateways to CD1 function. Nat Immunol 2006; 7: 811-817.
19. Aleman M, de la Barrera S, Schierloh P, Yokobori N, Baldini M, Musella R et al. Spontaneous or Mycobacterium tuberculosis-induced apoptotic neutrophils exert opposite effects on the dendritic cell-mediated immune response. Eur J Immunol 2007; 37: 1524-1537.
20. Skold M, Behar SM. Tuberculosistriggersatissue-dependent program of differentiation and acquisition of effector functions bycirculating monocytes. J Immunol 2008; 181: 6349-6360.
21. Giacomini E, Iona E, Ferroni L, Miettinen M, Fattorini L, Orefici G et al. Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokinegene expression that modulates Tcell response. J Immunol 2001; 166:7033-7041.
22. Beckman EM, Porcelli SA, Morita CT, Behar SM, Furlong ST, Brenner MB. Recognition of a lipid antigen by CD1-restricted alpha beta+ Tcells. Nature 1994; 372: 691-694.
23. Moody DB, Reinhold BB, Guy MR, Beckman EM, Frederique DE, Furlong ST et al. Structural requirements for glycolipid antigen recognition by CD1b-restricted T cells. Science 1997; 278: 283-286.
24. Sieling PA, Chatterjee D, Porcelli SA, Prigozy TI, Mazzaccaro RJ, Soriano T et al. CD1-restricted Tcell recognition of microbial lipoglycanantigens. Science 1995; 269: 227-230.
25. de la Barrera S, Aleman M, Musella R, Schierloh P, Pasquinelli V, Garcia V et al. IL-10 down-regulates costimulatory molecules on Mycobacterium tuberculosis-pulsed macro-phages and impairs the lytic activity of CD4 and CD8 CTL in tuberculosis patients. Clin Exp Immunol 2004; 138: 128-138.
26. Allavena P, Piemonti L, Longoni D, Bernasconi S, Stoppacciaro A, Ruco L et al. IL-10 prevents the differentiation of monocytes to dendritic cells but promotes their matura-tion to macrophages. Eur J Immunol 1998; 28: 359-369.
27. Stenger S, Modlin RL. Control of Mycobacterium tuberculosisthrough mammalian Toll-like receptors. Curr Opin Immunol 2002; 14: 452-457.
28. Thoma-Uszynski S, Kiertscher SM, Ochoa MT, Bouis DA, Norgard MV, Miyake K et al. Activation of toll-like receptor 2 on human dendritic cells triggers induction of IL-12, but not IL-10. J Immunol 2000; 165: 3804-3810.
29. Tsuji S, Matsumoto M, Takeuchi O, Akira S, Azuma I, Hayashi A et al. Maturation of human dendritic cells by cell wall skeleton of Mycobacterium bovis bacillus Calmette-Guerin: involvement of toll-like receptors. Infect Immun 2000; 68: 6883-6890.
30. Martino A, Sacchi A, Colizzi V, Vendetti S. Mycobacteria and dendritic cell differentia-tion: escape or control of immunity. Immunol Lett 2006; 102: 115-117.
31. Gagliardi MC, Teloni R, Mariotti S, Iona E, Pardini M, Fattorini L et al. Bacillus Calmette-Guerin shares with virulent Mycobacterium tuberculosis the capacity to subvert monocyte differentiation into dendritic cell: implication for its efficacy as a vaccinepreventingtuberculosis. Vaccine 2004; 22:3848-3857.
32. Gagliardi MC, Lemassu A, Teloni R, Mariotti S, Sargentini V, Pardini M et al. Cell wall-associated alpha-glucan is instrumental for Mycobacterium tuberculosis to block CD1molecule expression and disable the function of dendritic cell derived from infected monocyte. Cell Microbiol 2007; 9: 2081-2092.
33. Ulrichs T, Moody DB, Grant E, Kaufmann SH, Porcelli SA. T-cell responses to CD1-presented lipid antigens in humans with Mycobacterium tuberculosis infection. Infect Immun 2003; 71: 3076-3087.
34. Gredmark S, Soderberg-Naucler C. Human cytomegalovirus inhibits differentiation of monocytes into dendritic cells with the consequence of depressed immunological functions. J Virol 2003; 77: 10943-10956.
35. Li L, Choi YS. Follicular dendritic cell-signaling molecules required for proliferation and differentiation of GC-B cells. Semin Immunol 2002; 14: 259-266.
36. McRae BL, Nagai T, Semnani RT, van Seventer JM, van Seventer GA. Interferon-alpha and-beta inhibitthe in vitrodifferentiation of immunocompetent human dendriticcells from CD14(+) precursors. Blood 2000; 96: 210-217.
37. Fortsch D, Rollinghoff M, Stenger S. IL-10 converts human dendritic cells into macrophage-likecellswith increased antibacterial activityagainstvirulent Mycobacter-iumtuberculosis. J Immunol 2000; 165: 978-987.
38. Baliko Z, Szereday L, Szekeres-Bartho J. Th2 biased immune response in cases with active Mycobacterium tuberculosis infection and tuberculin anergy. FEMS Immunol Med Microbiol 1998; 22: 199-204.
39. Caux C, Massacrier C, Vanbervliet B, Barthelemy C, Liu YJ, Banchereau J. Interleukin 10 inhibits Tcell alloreaction induced by human dendritic cells. Int Immunol 1994; 6: 1177-1185.
40. Geijtenbeek TB, Van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CM, Appelmelk B et al. Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 2003; 197: 7-17.
41. Underhill DM, Ozinsky A, Smith KD, Aderem A. Toll-like receptor-2 mediates myco-bacteria-induced proinflammatorysignaling in macrophages. Proc Natl Acad Sci USA 1999; 96: 14459-14463.
42. Vasselon T, Hanlon WA, Wright SD, Detmers PA. Toll-like receptor 2 (TLR2) mediates activation of stress-activated MAP kinase p38. J Leukoc Biol 2002; 71: 503-510.
43. Guo Y, Feinberg H, Conroy E, Mitchell DA, Alvarez R, Blixt O et al. Structural basis for distinct ligand-binding and targeting properties of the receptors DC-SIGN and DC-SIGNR. Nat Struct Mol Biol 2004; 11: 591-598.
44. Zhang P, Skurnik M, Zhang SS, Schwartz O, Kalyanasundaram R, Bulgheresi S et al. Human dendritic cell-specific intercellular adhesion molecule-grabbing nonintegrin (CD209) is a receptor for Yersinia pestis that promotes phagocytosis by dendritic cells. Infect Immun 2008; 76: 2070-2079.
45. Klena J, Zhang P, Schwartz O, Hull S, Chen T. The core lipopolysaccharide of Escherichia coli is a ligand for the dendritic-cell-specific intercellular adhesion molecule nonintegrin CD209 receptor. J Bacteriol 2005; 187: 1710-1715.
46. Maeda N, Nigou J, Herrmann JL, Jackson M, Amara A, Lagrange PH et al. The cell surface receptor DC-SIGN discriminates between Mycobacterium species through selective recognition of the mannose caps on lipoarabinomannan. J Biol Chem 2003; 278: 5513-5516.