Mycobacterium tuberculosis antigens specifically modulate CCR2 and MCP-1/CCL2 on lymphoid cells from human pulmonary hilar lymph nodes

Journal of Immunology

Volumn 179, Issue 12, 2007, Pages 8381-8391

  Arias, Mauricio A ^a,b   Jaramillo, Gabriela ^a   López, Yúrika P ^a   Mejía, Natalia ^a   Mejía, Camila ^a   Pantoja, Adelis E ^a   Shattock, Robin J ^b   García, Luis F ^a   Griffin, George E ^b  

^a UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^b ST GEORGE S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENALIN; B7 ANTIGEN; CD14 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR7; CYTOKINE; DESMOPRESSIN; DOPAMINE; HLA DR ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; LIPOARABINOMANNAN; MONOCYTE CHEMOTACTIC PROTEIN 1; MYCOBACTERIUM ANTIGEN; TUBERCULIN; BACTERIAL ANTIGEN; CCL2 PROTEIN, HUMAN; CCR2 PROTEIN, HUMAN; CHEMOKINE; CHEMOKINE RECEPTOR; LIPOPOLYSACCHARIDE; MYCOBACTERIUM TUBERCULOSIS ANTIGENS; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ANTIGEN EXPRESSION; ARTICLE; CELL POPULATION; CELL STIMULATION; CHILD; CONTROLLED STUDY; DENDRITIC CELL; DOWN REGULATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; IMMUNOMODULATION; IMMUNOPATHOGENESIS; LUNG HILUS; LYMPH NODE; LYMPHOID TISSUE; MALE; MYCOBACTERIUM TUBERCULOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SCHOOL CHILD; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; DRUG EFFECT; IMMUNOLOGY; LUNG; LYMPHOCYTE; MACROPHAGE; METABOLISM; MONOCYTE;

ADULT; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; ANTIGENS, BACTERIAL; CHEMOKINE CCL2; CHEMOKINES; CHILD; DENDRITIC CELLS; FLOW CYTOMETRY; HUMANS; LIPOPOLYSACCHARIDES; LUNG; LYMPH NODES; LYMPHOCYTES; MACROPHAGES; MALE; MONOCYTES; RECEPTORS, CCR2; RECEPTORS, CHEMOKINE; TUBERCULIN;

EID: 40049089972     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.12.8381     Document Type: Article

References (63)

1. Ottenhoff, T. H., F. A. Verreck, M. A. Hoeve, and E. van de Vosse. 2005. Control of human host immunity to mycobacteria. Tuberculosis (Edinb.) 85: 53-64.
2. Flynn, J. L., and J. Chan. 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19: 93-129.
3. Lin, Y., J. Gong, M. Zhang, W. Xue, and P. F. Barnes. 1998. Production of monocyte chemoattractant protein 1 in tuberculosis patients. Infect. Immun. 66: 2319-2322.
4. Peters, W., and J. D. Ernst. 2003. Mechanisms of cell recruitment in the immune response to Mycobacterium tuberculosis. Microbes. Infect. 5: 151-158.
5. Gerszten, R. E., E. A. Garcia-Zepeda, Y. C. Lim, M. Yoshida, H. A. Ding, M. A. Gimbrone, Jr., A. D. Luster, F. W. Luscinskas, and A. Rosenzweig. 1999. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature 398: 718-723.
6. Holt, P. G., and M. A. Schon-Hegrad. 1987. Localization of T cells, macrophages and dendritic cells in rat respiratory tract tissue: implications for immune function studies. Immunology 62: 349-356.
7. Sertl, K., T. Takemura, E. Tschachler, V. J. Ferrans, M. A. Kaliner, and E. M. Shevach. 1986. Dendritic cells with antigen-presenting capability reside in airway epithelium, lung parenchyma, and visceral pleura. J. Exp. Med. 163: 436-451.
8. Devergne, O., A. Marfaing-Koka, T. J. Schall, M. B. Leger-Ravet, M. Sadick, M. Peuchmaur, M. C. Crevon, K. J. Kim, T. T. Schall, T. Kim, et al. 1994. Production of the RANTES chemokine in delayed-type hypersensitivity reactions: involvement of macrophages and endothelial cells. J. Exp. Med. 179: 1689-1694.
9. Kurashima, K., N. Mukaida, M. Fujimura, M. Yasui, Y. Nakazumi, T. Matsuda, and K. Matsushima. 1997. Elevated chemokine levels in bronchoalveolar lavage fluid of tuberculosis patients. Am. J. Respir. Crit Care Med. 155: 1474-1477.
10. Schall, T. J., K. Bacon, K. J. Toy, and D. V. Goeddel. 1990. Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 347: 669 - 671.
11. Schall, T. J., K. Bacon, R. D. Camp, J. W. Kaspari, and D. V. Goeddel. 1993. Human macrophage inflammatory protein α (MIP-1 α) and MIP-1 β chemokines attract distinct populations of lymphocytes. J. Exp. Med. 177: 1821-1826.
12. Juffermans, N. P., A. Verbon, S. J. van Deventer, H. van Deutekom, J. T. Belisle, M. E. Ellis, P. Speelman, and T. van der Poll. 1999. Elevated chemokine concentrations in sera of human immunodeficiency virus (HIV)-seropositive and HIV-seronegative patients with tuberculosis: a possible role for mycobacterial lipoarabinomannan. Infect. Immun. 67: 4295-4297.
13. Mohammed, K. A., N. Nasreen, M. J. Ward, K. K. Mubarak, F. Rodriguez-Panadero, and V. B. Antony. 1998. Mycobacterium-mediated chemokine expression in pleural mesothelial cells: role of C-C chemokines in tuberculous pleurisy. J. Infect. Dis. 178: 1450-1456.
14. Marino, S., S. Pawar, C. L. Fuller, T. A. Reinhart, J. L. Flynn, and D. E. Kirschner. 2004. Dendritic cell trafficking and antigen presentation in the human immune response to Mycobacterium tuberculosis. J. Immunol. 173: 494-506.
15. Sallusto, F., C. R. Mackay, and A. Lanzavecchia. 2000. The role of chemokine receptors in primary, effector, and memory immune responses. Annu. Rev. Immunol. 18: 593-620.
16. Cyster, J. G. 1999. Chemokines and the homing of dendritic cells to the T cell areas of lymphoid organs. J. Exp. Med. 189: 447-450.
17. Peters, W., H. M. Scott, H. F. Chambers, J. L. Flynn, I. F. Charo, and J. D. Ernst. 2001. Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 98: 7958-7963.
18. Peters, W., J. G. Cyster, M. Mack, D. Schlondorff, A. J. Wolf, J. D. Ernst, and I. F. Charo. 2004. CCR2-dependent trafficking of F4/80dim macrophages and CD11cdim/intermediate dendritic cells is crucial for T cell recruitment to lungs infected with Mycobacterium tuberculosis. J. Immunol. 172: 7647-7653.
19. Boring, L., J. Gosling, S. W. Chensue, S. L. Kunkel, R. V. Farese, Jr., H. E. Broxmeyer, and I. F. Charo. 1997. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J. Clin. Invest. 100: 2552-2561.
20. Sato, N., S. K. Ahuja, M. Quinones, V. Kostecki, R. L. Reddick, P. C. Melby, W. A. Kuziel, and S. S. Ahuja. 2000. CC chemokine receptor (CCR)2 is required for Langerhans cell migration and localization of T helper cell type 1 (Th1)-inducing dendritic cells: absence of CCR2 shifts the Leishmania major-resistant phenotype to a susceptible state dominated by Th2 cytokines, B cell outgrowth, and sustained neutrophilic inflammation. J. Exp. Med. 192: 205-218.
21. Bhatt, K., S. P. Hickman, and P. Salgame. 2004. Cutting edge: a new approach to modeling early lung immunity in murine tuberculosis. J. Immunol. 172: 2748-2751.
22. Wang, Y., C. G. Kelly, M. Singh, E. G. McGowan, A. S. Carrara, L. A. Bergmeier, and T. Lehner. 2002. Stimulation of Th1-polarizing cytokines, C-C chemokines, maturation of dendritic cells, and adjuvant function by the peptide binding fragment of heat shock protein 70. J. Immunol. 169: 2422-2429.
23. Gunn, M. D., K. Tangemann, C. Tam, J. G. Cyster, S. D. Rosen, and L. T. Williams. 1998. A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. Proc. Natl. Acad. Sci. USA 95: 258-263.
24. Ngo, V. N., H. L. Tang, and J. G. Cyster. 1998. Epstein-Barr virus-induced molecule 1 ligand chemokine is expressed by dendritic cells in lymphoid tissues and strongly attracts naive T cells and activated B cells. J. Exp. Med. 188: 181-191.
25. Gunn, M. D., S. Kyuwa, C. Tam, T. Kakiuchi, A. Matsuzawa, L. T. Williams, and H. Nakano. 1999. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J. Exp. Med. 189: 451-460.
26. Hickman, S. P., J. Chan, and P. Salgame. 2002. Mycobacterium tuberculosis induces differential cytokine production from dendritic cells and macrophages with divergent effects on naive T cell polarization. J. Immunol. 168: 4636-4642.
27. Rossi, M., and J. W. Young. 2005. Human dendritic cells: potent antigen-presenting cells at the crossroads of innate and adaptive immunity. J. Immunol. 175: 1373-1381.
28. Henderson, R. A., S. C. Watkins, and J. L. Flynn. 1997. Activation of human dendritic cells following infection with Mycobacterium tuberculosis. J. Immunol. 159: 635-643.
29. Jiao, X., R. Lo-Man, P. Guermonprez, L. Fiette, E. Deriaud, S. Burgaud, B. Gicquel, N. Winter, and C. Leclerc. 2002. Dendritic cells are host cells for mycobacteria in vivo that trigger innate and acquired immunity. J. Immunol. 168: 1294-1301.
30. Kaufmann, S. H. 2001. How can immunology contribute to the control of tuberculosis? Nat. Rev. Immunol. 1: 20-30.
31. Giacomini, E., E. Iona, L. Ferroni, M. Miettinen, L. Fattorini, G. Orefici, I. Julkunen, and E. M. Coccia. 2001. Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J. Immunol. 166: 7033-7041.
32. Choi, Y. K., B. A. Fallert, M. A. Murphey-Corb, and T. A. Reinhart. 2003. Simian immunodeficiency virus dramatically alters expression of homeostatic chemokines and dendritic cell markers during infection in vivo. Blood 101: 1684-1691.
33. Wilson, N. S., D. El-Sukkari, G. T. Belz, C. M. Smith, R. J. Steptoe, W. R. Heath, K. Shortman, and J. A. Villadangos. 2003. Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood 102: 2187-2194.
34. Campbell, J. J., C. E. Brightling, F. A. Symon, S. Qin, K. E. Murphy, M. Hodge, D. P. Andrew, L. Wu, E. C. Butcher, and A. J. Wardlaw. 2001. Expression of chemokine receptors by lung T cells from normal and asthmatic subjects. J. Immunol. 166: 2842-2848.
35. Wang, S. Y., M. L. Hsu, C. H. Tzeng, H. C. Hsu, and C. K. Ho. 1998. The influence of cryopreservation on cytokine production by human T lymphocytes. Cryobiology 37: 22-29.
36. Randolph, G. J., S. Beaulieu, S. Lebecque, R. M. Steinman, and W. A. Muller. 1998. Differentiation of monocytes into dendritic cells in a model of transendothelial trafficking. Science 282: 480-483.
37. Bonecchi, R., G. Bianchi, P. P. Bordignon, D. D'Ambrosio, R. Lang, A. Borsatti, S. Sozzani, P. Allavena, P. A. Gray, A. Mantovani, and F. Sinigaglia. 1998. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J. Exp. Med. 187: 129-134.
38. Sallusto, F., D. Lenig, C. R. Mackay, and A. Lanzavecchia. 1998. Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J. Exp. Med. 187: 875-883.
39. Chensue, S. W., K. S. Warmington, J. H. Ruth, P. S. Sanghi, P. Lincoln, and S. L. Kunkel. 1996. Role of monocyte chemoattractant protein-1 (MCP-1) in Th1 (mycobacterial) and Th2 (schistosomal) antigen-induced granuloma formation: relationship to local inflammation, Th cell expression, and IL-12 production. J. Immunol. 157: 4602-4608.
40. Gordon, S., and P. R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5: 953-964.
41. Randolph, G. J., K. Inaba, D. F. Robbiani, R. M. Steinman, and W. A. Muller. 1999. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 11: 753-761.
42. Fantuzzi, L., P. Borghi, V. Ciolli, G. Pavlakis, F. Belardelli, and S. Gessani. 1999. Loss of CCR2 expression and functional response to monocyte chemotactic protein (MCP-1) during the differentiation of human monocytes: role of secreted MCP-1 in the regulation of the chemotactic response. Blood 94: 875-883.
43. Arias, M. A., A. E. Pantoja, G. Jaramillo, S. C. Paris, R. J. Shattock, L. F. Garcia, and G. E. Griffin. 2006. Chemokine receptor expression and modulation by Mycobacterium tuberculosis antigens on mononuclear cells from human lymphoid tissues. Immunology 118: 171-184.
44. Arias, M. A., A. E. Pantoja, G. Jaramillo, Y. P. Lopez, N. Mejia, C. Mejia, S. C. Paris, R. J. Shattock, G. E. Griffin, and L. F. Garcia. 2007. Chemokine/ cytokine production by mononuclear cells from human lymphoid tissues and their modulation by Mycobacterium tuberculosis antigens. FEMS Immunol. Med. Microbiol. 49: 272-279.
45. Scott, H. M., and J. L. Flynn. 2002. Mycobacterium tuberculosis in chemokine receptor 2-deficient mice: influence of dose on disease progression. Infect. Immun. 70: 5946-5954.
46. Sica, A., A. Saccani, A. Borsatti, C. A. Power, T. N. Wells, W. Luini, N. Polentarutti, S. Sozzani, and A. Mantovani. 1997. Bacterial lipopolysaccharide rapidly inhibits expression of C-C chemokine receptors in human monocytes. J. Exp. Med. 185: 969-974.
47. Xu, L., R. Rahimpour, L. Ran, C. Kong, A. Biragyn, J. Andrews, M. Devries, J. M. Wang, and D. J. Kelvin. 1997. Regulation of CCR2 chemokine receptor mRNA stability. J. Leukocyte Biol. 62: 653-660.
48. Sozzani, S., P. Allavena, G. D'Amico, W. Luini, G. Bianchi, M. Kataura, T. Imai, O. Yoshie, R. Bonecchi, and A. Mantovani. 1998. Differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties. J. Immunol. 161: 1083-1086.
49. Kasahara, K., T. Tobe, M. Tomita, N. Mukaida, S. Shao-Bo, K. Matsushima, T. Yoshida, S. Sugihara, and K. Kobayashi. 1994. Selective expression of monocyte chemotactic and activating factor/monocyte chemoattractant protein 1 in human blood monocytes by Mycobacterium tuberculosis. J. Infect. Dis. 170: 1238-1247.
50. Rhoades, E. R., A. M. Cooper, and I. M. Orme. 1995. Chemokine response in mice infected with Mycobacterium tuberculosis. Infect. Immun. 63: 3871-3877.
51. Fietta, A., F. Meloni, C. Francioli, M. Morosini, A. Bulgheroni, L. Casali, and G. G. Gialdroni. 2001. Virulence of Mycobacterium tuberculosis affects interleukin-8, monocyte chemoattractant protein-1 and interleukin-10 production by human mononuclear phagocytes. Int. J. Tissue React. 23: 113-125.
52. Berman, J. S., R. L. Blumenthal, H. Kornfeld, J. A. Cook, W. W. Cruikshank, M. W. Vermeulen, D. Chatterjee, J. T. Belisle, and M. J. Fenton. 1996. Chemotactic activity of mycobacterial lipoarabinomannans for human blood T lymphocytes in vitro. J. Immunol. 156: 3828-3835.
53. Nigou, J., C. Zelle-Rieser, M. Gilleron, M. Thurnher, and G. Puzo. 2001. Mannosylated lipoarabinomannans inhibit IL-12 production by human dendritic cells: evidence for a negative signal delivered through the mannose receptor. J. Immunol. 166: 7477-7485.
54. Wang, J., E. Guan, G. Roderiquez, and M. A. Norcross. 1999. Inhibition of CCR5 expression by IL-12 through induction of β-chemokines in human T lymphocytes. J. Immunol. 163: 5763-5769.
55. Dahl, K. E., H. Shiratsuchi, B. D. Hamilton, J. J. Ellner, and Z. Toossi. 1996. Selective induction of transforming growth factor β in human monocytes by lipoarabinomannan of Mycobacterium tuberculosis. Infect. Immun. 64: 399-405.
56. Colotta, F., A. Borre, J. M. Wang, M. Tattanelli, F. Maddalena, N. Polentarutti, G. Peri, and A. Mantovani. 1992. Expression of a monocyte chemotactic cytokine by human mononuclear phagocytes. J. Immunol. 148: 760-765.
57. Kopydlowski, K. M., C. A. Salkowski, M. J. Cody, N. van Rooijen, J. Major, T. A. Hamilton, and S. N. Vogel. 1999. Regulation of macrophage chemokine expression by lipopolysaccharide in vitro and in vivo. J. Immunol. 163: 1537-1544.
58. Zisman, D. A., S. L. Kunkel, R. M. Strieter, W. C. Tsai, K. Bucknell, J. Wilkowski, and T. J. Standiford. 1997. MCP-1 protects mice in lethal endotoxemia. J. Clin. Invest. 99: 2832-2836.
59. Re, F., and J. L. Strominger. 2001. Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells. J. Biol. Chem. 276: 37692-37699.
60. Serbina, N. V., W. Kuziel, R. Flavell, S. Akira, B. Rollins, and E. G. Pamer. 2003. Sequential MyD88-independent and -dependent activation of innate immune responses to intracellular bacterial infection. Immunity 19: 891-901.
61. Kawakami, K., M. H. Qureshi, T. Zhang, Y. Koguchi, K. Shibuya, S. Naoe, and A. Saito. 1999. Interferon-γ (IFN-γ)-dependent protection and synthesis of chemoattractants for mononuclear leucocytes caused by IL-12 in the lungs of mice infected with Cryptococcus neoformans. Clin. Exp. Immunol. 117: 113-122.
62. Losana, G., C. Bovolenta, L. Rigamonti, I. Borghi, F. Altare, E. Jouanguy, G. Forni, J. L. Casanova, B. Sherry, M. Mengozzi, et al. 2002. IFN-γ and IL-12 differentially regulate CC chemokine secretion and CCR5 expression in human T lymphocytes. J. Leukocyte Biol. 72: 735-742.
63. Schrum, S., P. Probst, B. Fleischer, and P. F. Zipfel. 1996. Synthesis of the CC-chemokines MIP-1α, MIP-1β, and RANTES is associated with a type 1 immune response. J. Immunol. 157: 3598-3604.