Increased susceptibility of mice lacking T-bet to infection with Mycobacterium tuberculosis correlates with increased IL-10 and decreased IFN-γ production

Journal of Immunology

Volumn 175, Issue 7, 2005, Pages 4593-4602

  Sullivan, Brandon M ^a   Jobe, Ousman ^a   Lazarevic, Vanja ^a   Vasquez, Kristine ^a   Bronson, Roderick ^b   Glimcher, Laurie H ^a,b   Kramnik, Igor ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL POLARITY; CELL TYPE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; DISEASE ACTIVITY; DISEASE COURSE; DISEASE PREDISPOSITION; EOSINOPHIL; GIANT CELL; IMMUNE RESPONSE; INFECTION SENSITIVITY; LUNG TUBERCULOSIS; MACROPHAGE; MOUSE; MULTINUCLEAR CELL; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

EID: 25444482624     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.7.4593     Document Type: Article

References (58)

1. Kochi, A. 1991. The global tuberculosis situation and the new control strategy of the World Health Organization. Tubercle 72: 1-6.
2. Corbett, E. L., C. J. Watt, N. Walker, D. Maher, B. G. Williams, M. C. Raviglione, and C. Dye. 2003. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch. Intern. Med. 163: 1009-1021.
3. Saunders, B. M., and A. M. Cooper. 2000. Restraining mycobacteria: role of granulomas in mycobacterial infections. Immunol. Cell Biol. 78: 334-341.
4. Casanova, J. L., and L. Abel. 2002. Genetic dissection of immunity to mycobacteria: the human model. Annu. Rev. Immunol. 20: 581-620.
5. Caruso, A. M., N. Serbina, E. Klein, K. Triebold, B. R. Bloom, and J. L. Flynn. 1999. Mice deficient in CD4 T cells have only transiently diminished levels of IFN-γ, yet succumb to tuberculosis. J. Immunol. 162: 5407-5416.
6. + T cells causes reactivation of murine persistent tuberculosis despite continued expression of Interferon y and nitric oxide synthase 2. J. Exp. Med. 192: 347-358.
7. Saunders, B. M., A. A. Frank, I. M. Orme, and A. M. Cooper. 2002. CD4 is required for the development of a protective granulomatous response to pulmonary tuberculosis. Cell. Immunol. 216: 65-72.
8. + T cells during Mycobacterium tuberculosis infection. J. Immunol. 167: 6991-7000.
9. Cooper, A., 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.
10. + T lymphocytes in the lung correlate with resistance to infection with Mycobacterium tuberculosis. Infect. Immun. 69: 2666-2674.
11. Eruslanov, E. B., K. B. Majorov, M. O. Orlova, V. V. Mischenko, T. K. Kondratieva, A. S. Apt, and I. V. Lyadova. 2004. Lung cell responses to M. tuberculosis in genetically susceptible and resistant mice following intratracheal challenge. Clin. Exp. Immunol. 135: 19-28.
12. Lyadova, I. V., E. B. Eruslanov, S. V. Khaidukov, V. V. Yeremeev, K. B. Majorov, A. V. Pichugin, B. V. Nikonenko, T. K. Kondratieva, and A. S. Apt. 2000. Comparative analysis of T lymphocytes recovered from the lungs of mice genetically susceptible, resistant, and hyperresistant to Mycobacterium tuberculosis-triggered disease. J. Immunol. 165: 5921-5931.
13. Nathan, C., and M. U. Shiloh. 2000. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 97: 8841-8848.
14. MacMicking, J. D., R. J. North, R. LaCourse, J. S. Mudgett, S. K. Shah, and C. F. Nathan. 1997. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA 94: 5243-5248.
15. MacMicking, J. D., G. A. Taylor, and J. D. McKinney. 2003. Immune control of tuberculosis by IFN-γ-inducible LRG-47. Science 302: 654-659.
16. Feng, C. G., C. M. Collazo-Custodio, M. Eckhaus, S. Hieny, Y. Belkaid, K. Elkins, D. Jankovic, G. A. Taylor, and A. Sher. 2004. Mice deficient in LRG-47 display increased susceptibility to mycobacterial infection associated with the induction of lymphopenia. J. Immunol. 172: 1163-1168.
17. Szabo, S. J., S. T. Kim, G. L. Costa, X. Zhang, G. C. Fathman, and L. H. Glimcher. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669.
18. Lugo, G., R. Maldonado-Lopez, R. Possemato, C. Penaranda, and L. H. Glimcher. 2003. T-bet is required for optimal production of IFN-γ and antigen-specific T cell activation by dendritic cells. Proc. Natl. Acad. Sci. USA 100: 7749-7754.
19. Townsend, M., A. S. Weinmann, J. Matsuda, R. Saloman, P. Farnham, C. A. Biron, L. Gapin, and L. H. Glimcher. 2004. T-bet regulates the terminal maturation and homeostasis of NK and Val4iNKT cells. Immunity 20: 477-494.
20. Szabo, S. J., B. M. Sullivan, C. Stemmann, A. R. Satoskar, B. P. Sleckman, and L. H. Glimcher. 2002. Distinct effects of T-bet in TH1 lineage commitment and IFN-γ production in CD4 and CD8 T cells. Science 295: 338-342.
21. Sullivan, B. M., A. Juedes, S. J. Szabo, M. von Herrath, and L. H. Glimcher. 2003. Antigen-driven effector CD8 T cell function regulated by T-bet. Proc. Natl. Acad. Sci. USA 100: 15818-15823.
22. Hultgren, O. H., M. Verdrengh, and A. Tarkowski. 2004. T-box transcription-factor-deficient mice display increased joint pathology and failure of infection control during staphylococcal arthritis. Microbes Infect. 6: 529-535.
23. Medina, E., and R. J. North. 1998. Resistance ranking of some common inbred mouse strains to Mycobacterium tuberculosis and relationship to major histocompatibility complex haplotype and Nramp1 genotype. Immunology 93: 270-274.
24. Mitsos, L. M., L. R. Cardon, A. Fortin, L. Ryan, R. LaCourse, R. J. North, and P. Gros. 2000. Genetic control of susceptibility to infection with Mycobacterium tuberculosis in mice. Genes Immun. 1: 467-477.
25. Kramnik, I., W. F. Dietrich, P. Demant, and B. R. Bloom. 2000. Genetic control of resistance to experimental infection with virulent Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 97: 8560-8565.
26. Bettelli, E., B. M. Sullivan, S. I. Szabo, R. A. Sobel, L. H. Glimcher, and V. K. Kuchroo. 2004. Loss of T-bet, but not STAT1, prevents the development of experimental autoimmune encephalomyelitis. J. Exp. Med. 200: 79-87.
27. Kramnik, I. B., A. S. Apt, and A. M. Moroz. 1990. [Suppression of immune response by lung cells in experimental tuberculosis.] Biull. Eksp. Biol. Med. 110: 77-80.
28. Ulrichs, T., R. Anding, S. H. Kaufmann, and M. E. Munk. 2000. Numbers of IFN-γ-producing cells against ESAT-6 increase in tuberculosis patients during chemotherapy. Int. J. Tuberc. Lung Dis. 4: 1181-1183.
29. Pathan, A. A., K. A. Wilkinson, P. Klenerman, H. McShane, R. N. Davidson, G. Pasvol, A. V. Hill, and A. Lalvani. 2001. Direct ex vivo analysis of antigen-specific IFN-γ-secreting CD4 T cells in Mycobacterium tuberculosis-infected individuals: associations with clinical disease state and effect of treatment. J. Immunol. 167: 5217-5225.
30. Rook, G. A., R. Hernandez-Pando, K. Dheda, and G. Teng Seah. 2004. IL-4 in tuberculosis: implications for vaccine design. Trends Immunol. 25: 483-488.
31. Ordway, D. J., L. Costa, M. Martins, H. Silveira, L. Amaral, M. J. Arroz, F. A. Ventura, and H. M. Dockrell. 2004. Increased interleukin-4 production by CD8 and γδ T cells in health-care workers is associated with the subsequent development of active tuberculosis. J. Infect. Dis. 190: 756-766.
32. Sharma, S. K., D. K. Mitra, A. Balamurugan, R. M. Pandey, and N. K. Mehra. 2002. Cytokine polarization in miliary and pleural tuberculosis. J. Clin. Immunol. 22: 345-352.
33. Jung, Y. J., R. LaCourse, L. Ryan, and R. J. North. 2002. Evidence inconsistent with a negative influence of T helper 2 cells on protection afforded by a dominant T helper 1 response against Mycobacterium tuberculosis lung infection in mice. Infect. Immun. 70: 6436-6443.
34. North, R. J. 1998. Mice incapable of making IL-4 or IL-10 display normal resistance to infection with Mycobacterium tuberculosis. Clin. Exp. Immunol. 113: 55-58.
35. Kramnik, I., D. Radzioch, and E. Skamene. 1994. T-helper 1-like subset selection in Mycobacterium bovis bacillus Calmette-Guerin-infected resistant and susceptible mice. Immunology 81: 618-625.
36. + T cells that are cytotoxic and display Th1-like cytokine secretion profile: heterogeneity in cytotoxic activity and cytokine secretion levels. Eur. J. Immunol. 23: 2189-2195.
37. 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.
38. Cooper, A. M., J. Magram, J. Ferrante, and I. M. Orme. 1997. Interleukin 12 (IL-12) is crucial to the development of protective immunity in mice intravenously infected with Mycobacterium tuberculosis. J. Exp. Med. 186: 39-45.
39. Data, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-γ genes. Science 259: 1739-1742.
40. Wakeham, J., J. Wang, J. Magram, K. Croitoru, R. Harkness, P. Dunn, A. Zganiacz, and Z. Xing. 1998. Lack of both types 1 and 2 cytokines, tissue inflammatory responses, and immune protection during pulmonary infection by Mycobacterium bovis bacille Calmette-Guerin in IL-12-deficient mice. J. Immunol. 160: 6101-6111.
41. Demangel, C., P. Bertolino, and W. J. Britton. 2002. Autocrine IL-10 impairs dendritic cell (DC)-derived immune responses to mycobacterial infection by suppressing DC trafficking to draining lymph nodes and local IL-12 production. Eur. J. Immunol. 32: 994-1002.
42. Turner, J., M. Gonzalez-Juarrero, D. L. Ellis, R. J. Basaraba, A. Kipnis, I. M. Orme, and A. M. Cooper. 2002. In vivo IL-10 production reactivates chronic pulmonary tuberculosis in C57BL/6 mice. J. Immunol. 169: 6343-6351.
43. + T-cell responses to Mycobacterium tuberculosis by interleukin-10 and transforming growth factor β. Infect. Immun. 67: 6461-6472.
44. Murray, P. J., and R. A. Young. 1999. Increased antimycobacterial immunity in interleukin-10-deficient mice. Infect. Immun. 67: 3087-3095.
45. Lang, R., R. L. Rutschman, D. R. Greaves, and P. J. Murray. 2002. Autocrine deactivation of macrophages in transgenic mice constitutively overexpressing IL-10 under control of the human CD68 promoter. J. Immunol. 168: 3402-3411.
46. Jacobs, M., N. Brown, N. Allie, R. Gulert, and B. Ryffel. 2000. Increased resistance to mycobacterial infection in the absence of interleukin-10. Immunology 100:494-501.
47. Jacobs, M., L. Fick, N. Allie, N. Brown, and B. Ryffel. 2002. Enhanced immune response in Mycobacterium bovis bacille Calmette Guerin (BCG)-infected IL-10-deficient mice. Clin. Chem. Lab. Med. 40: 893-902.
48. Gerard, C., C. Bruyns, A. Marchant, D. Abramowicz, P. Vandenabeele, A. Delvaux, W. Fiers, M. Goldman, and T. Velu. 1993. Interleukin 10 reduces the release of tumor necrosis factor and prevents lethality in experimental endotoxemia. J. Exp. Med. 177: 547-550.
49. Ito, S., P. Ansari, M. Sakatsume, H. Dickensheets, N. Vazquez, R. P. Donnelly, A. C. Larner, and D. S. Finbloom. 1999. Interleukin-10 inhibits expression of both interferon α- and interferon γ-induced genes by suppressing tyrosine phosphorylation of STAT1. Blood 93: 1456-1463.
50. Florentino, D. F., A. Zlotnik, P. Vieira, T. Mosmann, M. Howard, D. W. Moore, and A. O'Garra. 1991. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J. Immunol. 146: 3444-3451.
51. Balcewicz-Sablinska, M. K., J. Keane, H. Kornfeld, and H. G. Remold. 1998. Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-α. J. Immunol. 161: 2636-2641.
52. Lazarevic, V., A. J. Myers, C. A. Scanga, and J. L. Flynn. 2003. CD40, but not CD40L, is required for the optimal priming of T cells and control of aerosol M. tuberculosis infection. Immunity 19: 823-835.
53. Dranoff, G., A. D. Crawford, M. Sadelain, B. Ream, A. Rashid, R. T. Bronson, G. R. Dickersin, C. J. Bachurski, E. L. Mark, J. A. Whitsett, et al. 1994. Involvement of granulocyte-macrophage colony-stimulating factor in pulmonary homeostasis. Science 264: 713-716.
54. + suppressor T cells. Immunol. Rev. 182: 58-67.
55. Roncarolo, M. G., R. Bacchetta, C. Bordignon, S. Narula, and M. K. Levings. 2001. Type 1 T regulatory cells. Immunol. Rev. 182: 68-79.
56. Weiner, H. L. 2001. Induction and mechanism of action of transforming growth factor-β-secreting Th3 regulatory cells. Immunol. Rev. 182: 207-214.
57. + regulatory T cells control Leishmania major persistence and immunity. Nature 420: 502-507.
58. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389: 737-742.