Attenuation of HLA-DR expression by mononuclear phagocytes infected with Mycobacterium tuberculosis is related to intracellular sequestration of immature class II heterodimers

Journal of Immunology

Volumn 161, Issue 9, 1998, Pages 4882-4893

  Hmama, Zakaria ^a,b,c   Gabathuler, Reinhard ^a   Jefferies, Wilfred A ^a   De Jong, Gary ^a   Reiner, Neil E ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b VANCOUVER HOSPITAL AND HEALTH SCIENCES CENTRE   (Canada)

^c SIDI MOHAMED BEN ABDELLAH UNIVERSITY   (Morocco)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HLA DR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MEMBRANE PROTEIN;

ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; HLA SYSTEM; HOST CELL; HUMAN; HUMAN CELL; LYSOSOME MEMBRANE; MACROPHAGE FUNCTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MYCOBACTERIOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; TUBERCULOSIS;

ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; BIOLOGICAL TRANSPORT; DIMERIZATION; ENDOSOMES; GLYCOSYLATION; GOLGI APPARATUS; HEXOSAMINIDASES; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-DR ANTIGENS; HUMANS; IMMUNOLOGIC DEFICIENCY SYNDROMES; INTERFERON-GAMMA, RECOMBINANT; LEUKEMIA, MONOCYTIC, ACUTE; LYSOSOMES; MICROSCOPY, CONFOCAL; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; NUCLEAR PROTEINS; PHAGOCYTOSIS; PROTEIN HYBRIDIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TETRADECANOYLPHORBOL ACETATE; TRANS-ACTIVATORS; TUBERCULOSIS; TUMOR CELLS, CULTURED; VACUOLES;

EID: 0032212228     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (61)

1. Raviglione, M. C., D. E. J. Snider, and A. Kochi. 1995. Global epidemiology of tuberculosis: morbidity and mortality of a worldwide epidemic. JAMA 273:220.
2. Dolin, P. J., M. C. Raviglione, and A. Kochi. 1995. Global tuberculosis incidence and mortality during 1990-2000. Bull. WHO 72:213.
3. Raviglione, M. C., J. P. Narain, and A. Kochi. 1992. HIV-associated tuberculosis in developing countries: clinical features, diagnosis, and treatment. Bull. WHO 70:515.
4. Barnes, P. F., A. B. Bloch, P. T. Davidson, and D. E. J. Snider. 1991. Tuberculosis in patients with human immunodeficiency virus infection. N. Engl. J. Med. 324:1644.
5. Hopewell, P. C. 1992. Impact of human immunodeficiency virus infection on the epidemiology, clinical features, managment, and control of tuberculosis. Clin. Infect. Dis. 15:540.
6. Bevilacqua, N., G. Marasca, A. Moscati, M. Fantoni, F. Ricci, and L. Ortona. 1993. Tuberculosis and HIV infection. Lancet 342:677.
7. Gercken, J., J. Pryjma, M. Ernst, and H.-D. Flad. 1994. Defective antigen presentation by Mycobacterium tuberculosis-infected monocytes. Infect. Immun. 62:3472.
8. Mazzaccaro, R. J., M. Gedde, E. R. Jensen, H. M. Van Santen, H. L. Ploegh, K. L. Rock, and B. R. Bloom. 1996. Major histocompatibility class I presentation of soluble antigen facilitated by Mycobacterium tuberculosis infection. Proc. Natl. Acad. Sci. USA 93:11786.
9. Kaye, P. M., M. Sims, and M. Feldmann. 1986. Regulation of macrophage accessory cell activity by mycobacteria. II. In vitro inhibition of Ia expression by Mycobacterium microti. Clin. Exp. Immunol. 64:28.
10. Mshana, R. N., R. C. Hastings, and J. L. Krahenbuhl. 1988. Infection with live mycobacteria inhibits in vitro detection of Ia antigen on macrophage. Immunobiology 177:40.
11. King, D. P. and P. P. Jones. 1983. Induction of Ia and H-2 antigens on a macrophage cell line by immune interferon. J. Immunol. 131:315.
12. Figueiredo, F., T. J. Koerner, and D. O. Adams. 1989. Molecular mechanisms regulating the expression of class II histocompatibility molecules on macrophages: effects of inductive and suppressive signals on gene transcription. J. Immunol. 143:3781.
13. Becker, S. 1984. Interferons as modulators of human monocyte-macrophage differenciation. I. Interferon-γ increases HLA-DR expression and inhibits phagocytosis of zymosan. J. Immunol. 132:1249.
14. Nandan, D., and N. E. Reiner. 1995. Attenuation of gamma interferon-induced tyrosine phosphorylation in mononuclear phagocytes infected with Leishmania donovani: selective inhibition of signaling through Janus kinases and Stat1. Infect. Immun. 63:4495.
15. Reiner, N. E. 1994. Altered cell signaling and mononuclear phagocyte deactivation during intracellular infection. Immunol. Today 15:374.
16. Steimle, V., L. A. Otten, M. Zufferey, and B. Mach. 1993. Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome). Cell 75:135.
17. Steimle, V., C.-A. Siegrist, A. Mottet, B. Lisowska-Grospierre, and B. Mach. 1994. Regulation of MHC class II expression by interferon-γ mediated by the transactivator gene CIITA. Science 265:106.
18. Reith, W., V. Steimle, and B. Mach. 1995. Molecular defects in the bare lymphocyte syndrome and regulation of MHC class II genes. Immunol. Today 16:539.
19. Greenlund, A. C., M. A. Farrar, B. L. Viviano, and R. D. Schreiber. 1994. Ligand-induced IFN-γ receptor tyrosine phosphorylation couples the receptor to its signal transduction system (p 91). EMBO J. 13:1591.
20. Greenlund, A. C., M. O. Morales, B. L. Viviano, H. Yan, J. J. Krolewski, and R. D. Schreiber. 1995. Stat recruitment by tyrosine-phosphorylated cytokine receptor: an ordered reversible affinity-driven process. Immunity 2:677.
21. Darnell, J. E., Jr., I. M. Kerr, and G. R. Stark. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415.
22. Busch, R., and E. D. Mellins. 1996. Developing and shedding inhibitions: how MHC class II molecules reach maturity. Curr. Opin. Immunol. 8:51.
23. Pieters, J. 1997. MHC class II restricted antigen presentation. Curr. Opin. Immunol. 9:89.
24. Riberdy, J. M., J. R. Newcomb, M. J. Surman, J. A. Barbosa, and P. Cresswell. 1992. HLA-DR molecules from an antigen-processing mutant cell line are associated with invariant chain peptides. Nature 360:474.
25. Sloan, V. S., P. Cameron, G. Porter, M. Gammon, and M. Amaya. 1995. Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature 375:802.
26. Denzin, L. K., N. F. Robbins, C. Carboy-Newcomb, and P. Cresswell. 1994. Assembly and intracellular transport of HLA-DM and correction of the class II antigen-processing defect in T2 cells. Immunity 1:1.
27. Stokes, R. W., I. D. Haidl, W. A. Jefferies, and D. P. Speert. 1993. Mycobacteria-macrophage interactions: macrophage phenotype determines the nonopsonic binding of Mycobacterium tuberculosis to murine macrophages. J. Immunol. 151:7067.
28. Hed, J., G. Hallden, S. G. O. Johansson, and P. Larsson. 1987. The use of fluorescence quenching in flow cytofluorometry to measure the attachment and ingestion phases in phagocytosis in peripheral blood without prior cell separation. J. Immunol. Methods 101:119.
29. Fattorossi, A., R. Nisini, J. G. Pizzolo, and R. D'Amelio. 1989. New, simple flow cytometry technique to discriminate between internalized and membrane-bound particles in phagocytosis. Cytometry 10:320.
30. Nandan, D., and N. E. Reiner. 1997. TGF-β attenuates the class II transactivator and reveals an accessory pathway of IFN-γ action. J. Immunol. 158:1095.
31. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680.
32. Germain, R. N., and L. R. Hendrix. 1991. MHC class II structure, occupancy and surface expression determined by post-endoplasmic reticulum antigen binding. Nature 353:134.
33. Neefjes, J. J., and H. L. Ploegh. 1992. Inhibition of endosomal proteolytic activity by leupeptin blocks surface expression of MHC class II molecules and their conversion to SDS resistant a,b heterodimers in endosomes. EMBO J. 11:411.
34. Bonner, W., and R. A. Laskey. 1974. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur. J. Biochem. 46:83.
35. Richter-Dahlfors, A., A. M. J. Buchan, and B. B. Finlay. 1997. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J. Exp. Med. 186:569.
36. Schlesinger, L. S., C. G. Bellinger-Kawahara, N. R. Payne, and M. A. Horwitz. 1990. Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J. Immunol. 144:2771.
37. Peterson, P. K., G. Gekker, S. Hu, W. S. Sheng, W. R. Anderson, R. J. Ulevitch, P. S. Tobias, K. V. Gustafson, T. W. Molitor, and C. C. Chao. 1995. CD14 receptor-mediated uptake of nonopsonized mycobacterium tuberculosis by human microglia. Infect. Immun. 63:1598.
38. Lian, R. H., G. J. Kotwal, S. R. Wellhausen, L. A. Hunt, and D. E. Justus. 1996. IFN-γ-induced MHC class II gene expression is suppressed in endothelial cells by dextran sulfate. J. Immunol. 157:864.
39. Chang, C. H., J. D. Fontes, M. Peterlín, and R. A. Flavell. 1994. Class II transactivator (CIITA) is sufficient for the inducible expression of major histocompatibility complex class II genes. J. Exp. Med. 180:1367.
40. Nijman, H. W., M. J. Kleijmeer, M. A. Ossevoort, V. M. J. Oorschot, M. P. M. Vierboom, M. Van de Keur, P. Kenemans, W. M. Kast, H. J. Geuze, and C. J. M. Melief. 1995. Antigen capture and major histocompatibility class II compartments of freshly isolated and cultured human blood dendritic cells. J. Exp. Med. 182:163.
41. Kleijmeer, M. J., M. A. Ossevoon, C. J. H. Van Veen, J. J. Van Hellemond, J. J. Neefjes, W. M. Kast, C. J. M. Melief, and H. J. Geuze. 1995. MHC class II compartments and the kinetics of antigen presentation in activated mouse spleen dendritic cells. J. Immunol. 154:5715.
42. Tsuchiya, S., M. Yamabe, Y. Yamagushi, Y. Kobayashi, T. Konno, and K. Tada. 1980. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Internal. J. Cancer 26:171.
43. -x Salmonella typhimurium with that of live virus. J. Immunol. 150:2869.
44. Nadler, S. G., B. M. Rankin, P. Moran-Davis, J. S. Cleaveland, and P. A. Kiener. 1994. Effect of interferon-γ on antigen processing in human monocytes. Eur. J. Immunol. 24:3124.
45. Lee, B. Y., and M. A. Horwitz. 1995. Identification of macrophage and stress-induced proteins of Mycobacterium tuberculosis. J. Clin. Invest. 96:245.
46. Chang, C.-H. and R. A. Flavell. 1995. Class II transactivator regulates the expression of multiple genes involved in antigen presentation. J. Exp. Med. 181:765.
47. Kropshofer, H., G. J. Hammerling, and A. B. Vogt. 1997. How HLA-DM edits the MHC class II peptide repertoire: survival of the fittest? Immunol. Today 18:77.
48. 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.
49. Neefjes, J. J., V. Stollorz, P. J. Peters, H. J. Geuze, and H. L. Ploegh. 1990. The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell 61:171.
50. Gordon, A. H., P. D. Hart, and M. R. Young. 1980. Ammonia inhibits phagosome-lysosome fusion in macrophages. Nature 286:78.
51. Harth, G., D. L. Clemens, and M. A. Horwitz. 1994. Glutamine synthetase of Mycobacterium tuberculosis: extracellular release and characterization of its enzymatic activity. Proc. Natl. Acad. Sci. USA 91:9342.
52. Clemens, D. L., B.-Y. Lee, and M. A. Horwitz. 1995. Purification, characterization, and genetic analysis of Mycobacterium tuberculosis urease, a potentially critical determinant of host-pathogen interaction. J. Bacteriol. 177:5644.
53. Xu, S., A. Cooper, S. Sturgill-Koszycki, T. Van Heyningen, D. Chatterjee, I. Orme, P. Allen, and D. G. Russell. 1994. Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J. Immunol. 153:2568.
54. Khoo, K. H., A. Dell, H. R. Morris, P. J. Brennan, and D. Chatterjee. 1995. Inositol phosphate capping of the nonreducing termini of lipoarabinomannan from rapidly growing strains of Mycobacterium. J. Biol Chem. 270:12380.
55. Goren, M. B., P. D'Arcy Hart, M. R. Young, and J. A. Armstrong. 1976. Prevention of phagosome-lysosome fusion in cultured macrophages by sulfatides of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 73:2510.
56. Hunter, S. W., R. C. Murphy, K. Clay, and M. B. Goren. 1983. Trehalose-containing lipooligosaccharides: a new class of species-specific antigens from Mycobacterium. J. Biol. Chem. 258:10481.
57. Chan, J., and S. H. E. Kaufmann. 1994. Immune mechanisms of protection. In Tuberculosis, Pathogenesis, Protection, and Control. B. R. Bloom, ed. American Society for Microbiology, Washington, DC, p. 389.
58. D'Arcy Hart, P., M. R. Young, A. H. Gordon, and K. H. Sullivan. 1987. Inhibition of phagosome-lysosome fusion in macrophages by certain mycobacteria can be explained by inhibition of lysosomal movements observed after phagocytosis. J. Exp. Med. 166:933.
59. + T cells of mycobacteria growing in human macrophages. Science 260:984.
60. lyn and phosphatidylinositol 3-kinase in human monocytes. J. Immunol. 156:1157.
61. Peters, P. J., G. Raposo, J. J. Neefjes, V. Oorschot, R. L. Leijendekker, and H. J. Geuze. 1995. Major histocompatibility complex class II compartments in human B lymphoblastoid cells are distinct from early endosomes. J. Exp. Med. 182:325.