Inhibition of Major Histocompatibility Complex II Expression and Antigen Processing in Murine Alveolar Macrophages by Mycobacterium bovis BCG and the 19-Kilodalton Mycobacterial Lipoprotein

Infection and Immunity

Volumn 72, Issue 4, 2004, Pages 2101-2110

  Fulton, Scott A ^a   Reba, Scott M ^a   Pai, Rish K ^b   Pennini, Meghan ^b   Torres, Martha ^a,d   Harding, Clifford V ^b   Boom, W Henry ^a,c  

^a UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

^d INSTITUTO NACIONAL DE ENFERMEDADES RESPIRATORIAS   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD11B ANTIGEN; CD40 ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; LIPOPROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; INFECTION CONTROL; LUNG ALVEOLUS MACROPHAGE; MOUSE; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD11C; ANTIGENS, CD80; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTERFERON TYPE II; LIPOPROTEINS; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; MYCOBACTERIUM BOVIS; TUBERCULOSIS;

EID: 1842484130     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.4.2101-2110.2004     Document Type: Article

References (53)

1. Beatty, W. L., E. R. Rhoades, H. J. Ullrich, D. Chatterjee, J. E. Heuser, and D. G. Russell. 2000. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 1:235-247.
2. Brightbill, H. D., D. H. Libraty, S. R. Krutzik, R. B. Yang, J. T. Belisle, J. R. Bleharski, M. Maitland, M. V. Norgard, S. E. Plevy, S. T. Smale, P. J. Brennan, B. R. Bloom, P. J. Godowski, and R. L. Modlin. 1999. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 285:732-736.
3. Chensue, S. W., K. Warmington, J. Ruth, P. Lincoln, M. C. Kuo, and S. L. Kunkel. 1994. Cytokine responses during mycobacterial and schistosomal antigen-induced pulmonary granuloma formation. Production of Th1 and Th2 cytokines and relative contribution of tumor necrosis factor. Am. J. Pathol. 145:1105-1113.
4. Constant, S. L., K. S. Lee, and K. Bottomly. 2000. Site of antigen delivery can influence T cell priming: pulmonary environment promotes preferential Th2-type differentiation. Eur. J. Immunol. 30:840-847.
5. Cooper, A. M., J. E. Callahan, M. Keen, J. T. Belisle, and I. M. Orme. 1997. Expression of memory immunity in the lung following re-exposure to Mycobacterium tuberculosis. Tuber. Lung Dis. 78:67-73.
6. Cooper, A. M., D. K. Dalton, T. A. Stewart, J. P. Griffin, D. G. Russell, and I. M. Orme. 1993. Disseminated tuberculosis in interferon-γ gene-disrupted mice. J. Exp. Med. 178:2243-2247.
7. Crouch, E., K. Hartshorn, and I. Ofek. 2000. Collectins and pulmonary innate immunity. Immunol. Rev. 173:52-65.
8. Crouch, E. C. 2000. Surfactant protein-D and pulmonary host defense. Respir. Res. 1:93-108.
9. Dunn, P. L., and R. J. North. 1995. Virulence ranking of some Mycobacterium tuberculosis and Mycobacterium bovis strains according to their ability to multiply in the lungs, induce lung pathology, and cause mortality in mice. Infect. Immun. 63:3428-3437.
10. Ferguson, J. S., and L. S. Schlesinger. 2000. Pulmonary surfactant in innate immunity and the pathogenesis of tuberculosis. Tuber. Lung Dis. 80:173-184.
11. Flynn, J. L., and J. Chan. 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19:93-129.
12. Flynn, J. L., J. Chan, K. J. Triebold, D. K. Dalton, T. A. Stewart, and B. R. Bloom. 1993. An essential role for interferon γ in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178:2249-2254.
13. Fulton, S. A., T. D. Martin, R. W. Redline, and W. Henry Boom. 2000. Pulmonary immune responses during primary Mycobacterium bovis-Calmette-Guerin bacillus infection in C57Bl/6 mice. Am. J. Respir. Cell Mol. Biol. 22:333-343.
14. Fulton, S. A., S. M. Reba, T. D. Martin, and W. H. Boom. 2002. Neutrophil-mediated mycobacteriocidal immunity in the lung during Mycobacterium bovis BCG infection in C57BL/6 mice. Infect. Immun. 70:5322-5327.
15. Gonzalez-Juarrero, M., and I. M. Orme. 2001. Characterization of murine lung dendritic cells infected with Mycobacterium tuberculosis. Infect. Immun. 69:1127-1133.
16. Gonzalez-Juarrero, M., T. S. Shim, A. Kipnis, A. P. Junqueira-Kipnis, and I. M. Orme. 2003. Dynamics of macrophage cell populations during murine pulmonary tuberculosis. J. Immunol. 171:3128-3135.
17. Hanekom, W. A., M. Mendillo, C. Manca, P. A. Haslett, M. R. Siddiqui, C. Barry III, and G. Kaplan. 2003. Mycobacterium tuberculosis inhibits maturation of human monocyte-derived dendritic cells in vitro. J. Infect. Dis. 188:257-266.
18. Harding, C. V., D. S. Collins, O. Kanagawa, and E. R. Unanue. 1991. Liposome-encapsulated antigens engender lysosomal processing for class II MHC presentation and cytosolic processing for class I presentation. J. Immunol. 147:2860-2863.
19. Hertz, C. J., S. M. Kiertscher, P. J. Godowski, D. A. Bouis, M. V. Norgard, M. D. Roth, and R. L. Modlin. 2001. Microbial lipopeptides stimulate dendritic cell maturation via Toll-like receptor 2. J. Immunol. 166:2444-2450.
20. Hirsch, C. S., T. Yoneda, L. Averill, J. J. Ellner, and Z. Toossi. 1994. Enhancement of intracellular growth of Mycobacterium tuberculosis in human monocytes by transforming growth factor-β1. J. Infect. Dis. 170:1229-1237.
21. Kamijo, R., J. Le, D. Shapiro, E. A. Havell, S. Huang, M. Aguet, M. Bosland, and J. Vilcek. 1993. Mice that lack the interferon-gamma receptor have profoundly altered responses to infection with Bacillus Calmette-Guerin and subsequent challenge with lipopolysaccharide. J. Exp. Med. 178:1435-1440.
22. Kelsall, B. L., C. A. Biron, O. Sharma, and P. M. Kaye. 2002. Dendritic cells at the host-pathogen interface. Nat. Immunol. 3:699-702.
23. Kincaid, E. Z., and J. D. Ernst. 2003. Mycobacterium tuberculosis exerts gene-selective inhibition of transcriptional responses to IFN-γ without inhibiting STAT1 function. J. Immunol. 171:2042-2049.
24. Lagranderie, M., M. A. Nahori, A. M. Balazuc, H. Kiefer-Biasizzo, J. R. Lapa e Silva, G. Milon, G. Marchal, and B. B. Vargaftig. 2003. Dendritic cells recruited to the lung shortly after intranasal delivery of Mycobacterium bovis BCG drive the primary immune response towards a type 1 cytokine production. Immunology 108:352-364.
25. Leemans, J. C., N. P. Juffermans, S. Florquin, N. van Rooijen, M. J. Vervoordeldonk, A. Verbon, S. J. van Deventer, and T. van der Poll. 2001. Depletion of alveolar macrophages exerts protective effects in pulmonary tuberculosis in mice. J. Immunol. 166:4604-4611.
26. Legge, K. L., and T. J. Braciale. 2003. Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 18:265-277.
27. LeVine, A. M., K. E. Kurak, M. D. Bruno, J. M. Stark, J. A. Whitsett, and T. R. Korfhagen. 1998. Surfactant protein-A-deficient mice are susceptible to Pseudomonas aeruginosa infection. Am. J. Respir. Cell Mol. Biol. 19:700-708.
28. LeVine, A. M., J. A. Reed, K. E. Kurak, E. Cianciolo, and J. A. Whitsett. 1999. GM-CSF deficient mice are susceptible to pulmonary group B streptococcal infection. J. Clin. Investig. 103:563-569.
29. Maus, U., S. Herold, H. Muth, R. Maus, L. Ermert, M. Ermert, N. Weissmann, S. Rosseau, W. Seeger, F. Grimminger, and J. Lohmeyer. 2001. Monocytes recruited into the alveolar air space of mice show a monocytic phenotype but upregulate CD14. Am. J. Physiol. Lung Cell. Mol. Physiol. 280:L58-L68.
30. Means, T. K., S. Wang, E. Lien, A. Yoshimura, D. T. Golenbock, and M. J. Fenton. 1999. Human toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J. Immunol. 163:3920-3927.
31. Noss, E. H., C. V. Harding, and W. H. Boom. 2000. Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell. Immunol. 201:63-74.
32. Noss, E. H., R. K. Pai, T. J. Sellati, J. D. Radolf, J. Belisle, D. T. Golenbock, W. H. Boom, and C. V. Harding. 2001. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J. Immunol. 167:910-918.
33. Orme, I. M., P. Andersen, and W. H. Boom. 1993. T cell response to Mycobacterium tuberculosis. J. Infect. Dis. 167:1481-1497.
34. Pal, R. K., M. Convery, T. A. Hamilton, W. H. Boom, and C. V. Harding. 2003. Inhibition of IFN-γ-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J. Immunol. 171:175-184.
35. Paine, R., III, S. B. Morris, H. Jin, S. E. Wilcoxen, S. M. Phare, B. B. Moore, M. J. Coffey, and G. B. Toews. 2001. Impaired functional activity of alveolar macrophages from GM-CSF-deficient mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 281:L1210-L1218.
36. Pasula, R., J. R. Wright, D. L. Kachel, and W. J. Martin II. 1999. Surfactant protein A suppresses reactive nitrogen intermediates by alveolar macrophages in response to Mycobacterium tuberculosis. J. Clin. Investig. 103:483-490.
37. Pearl, J. E., B. Saunders, S. Ehlers, I. M. Orme, and A. M. Cooper. 2001. Inflammation and lymphocyte activation during mycobacterial infection in the interferon-gamma-deficient mouse. Cell. Immunol. 211:43-50.
38. Rich, E. A., M. Torres, E. Sada, C. K. Finegan, B. D. Hamilton, and Z. Toossi. 1997. Mycobacterium tuberculosis (MTB)-stimulated production of nitric oxide by human alveolar macrophages and relationship of nitric oxide production to growth inhibition of MTB. Tuber. Lung Dis. 78:247-255.
39. Sadek, M. I., E. Sada, Z. Toossi, S. K. Schwander, and E. A. Rich. 1998. Chemokines induced by infection of mononuclear phagocytes with mycobacteria and present in lung alveoli during active pulmonary tuberculosis. Am. J. Respir. Cell Mol. Biol. 19:513-521.
40. Schauble, T. L., W. H. Boom, C. K. Finegan, and E. A. Rich. 1993. Characterization of suppressor function of human alveolar macrophages for T lymphocyte responses to phytohemagglutinin: cellular selectivity, reversibility and early events in T cell activation. Am. J. Respir. Cell Mol. Biol. 8:89-97.
41. Schneeberger, E. E., M. DeFerrari, M. J. Skoskiewicz, P. S. Russell, and R. B. Colvin. 1986. Induction of MHC-determined antigens in the lung by interferon-γ. Lab. Investig. 55:138-144.
42. Schwander, S. K., M. Torres, E. Sada, C. Carranza, E. Ramos, M. Tary-Lehmann, R. S. Wallis, J. Sierra, and E. A. Rich. 1998. Enhanced responses to Mycobacterium tuberculosis antigens by human alveolar lymphocytes during active pulmonary tuberculosis. J. Infect. Dis. 178:1434-1445.
43. -/-) and IL-10 knockout mice causes increased expression and function of B7 costimulatory molecules on alveolar macrophages. J. Immunol. 168:1903-1910.
44. Stokes, R. W., L. M. Thorson, and D. P. Speert. 1998. Nonopsonic and opsonic association of Mycobacterium tuberculosis with resident alveolar macrophages is inefficient. J. Immunol. 160:5514-5521.
45. Strieter, R. M., S. W. Chensue, M. A. Basha, T. J. Standiford, J. P. Lynch, M. Baggiolini, and S. L. Kunkel. 1990. Human alveolar macrophage gene expression of interleukin-8 by tumor necrosis factor-α, lipopolysaccharide, and interleukin-1-β. Am. J. Respir. Cell Mol. Biol. 2:321-326.
46. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll-like receptors. Annu. Rev. Immunol. 21:335-376.
47. Ting, L. M., A. C. Kim, A. Cattamanchi, and J. D. Ernst. 1999. Mycobacterium tuberculosis inhibits IFN-γ transcriptional responses without inhibiting activation of STAT1. J. Immunol. 163:3898-3906.
48. Toews, G. B., W. C. Vial, M. M. Dunn, P. Guzzetta, G. Nunez, P. Stastny, and M. F. Lipscomb. 1984. The accessory cell function of human alveolar macrophages in specific T cell proliferation. J. Immunol. 132:181-186.
49. Toossi, Z., P. Gogate, H. Shiratsuchi, T. Young, and J. J. Ellner. 1995. Enhanced production of TGF-β by blood monocytes from patients with active tuberculosis and presence of TGF-β in tuberculous granulomatous lung lesions. J. Immunol. 154:465-473.
50. Tsao, T. C., J. Hong, C. Huang, P. Yang, S. L. Liao, and K. S. Chang. 1999. Increased TNF-alpha, IL-1 beta and IL-6 levels in the bronchoalveolar lavage fluid with the upregulation of their mRNA in macrophages lavaged from patients with active pulmonary tuberculosis. Tuber. Lung Dis. 79:279-285.
51. Underhill, D. M., A. Ozinsky, K. D. Smith, and A. Aderem. 1999. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl. Acad. Sci. USA 96:14459-14463.
52. van Crevel, R., T. H. M. Ottenhoff, and J. W. M. van der Meer. 2002. Innate immunity to Mycobacterium tuberculosis. Clin. Microbiol. Rev. 15:294-309.
53. Zhang, P., W. R. Summer, G. J. Bagby, and S. Nelson. 2000. Innate immunity and pulmonary host defense. Immunol. Rev. 173:39-51.