Mechanisms of Host Protection and Pathogen Evasion of Immune Response During Tuberculosis

Chapter

Abstract

An integrated response of the host is essential in health and disease. Upon microbial exposure, infected hosts strictly regulate immune responses to both contain pathogen dissemination and modulate immunopathology-associated effects, thus preventing mortality. In addition to a variety of molecules, such potent responses are kept under tight control by a class of anti-inflammatory eicosanoids, the lipoxins. Lipoxins are induced following exposure to several infectious agents and can function as immuno-modulatory molecules. A number of observations made in animal models of infection and human studies indicate that such lipid mediators play a critical role in controlling early as well as chronic immune responses. This chapter summarizes the role of cytokines and lipoxins in regulating innate immune responses to a major human pathogen, Mycobaterium tuberculosis.

Keywords

Tuberculosis Bacillus Glucocorticoid Smoke Microbe 

References

  1. Aguirre-Blanco, A. M., P. T. Lukey, et al. (2007). “Strain-dependent variation in Mycobacterium bovis BCG-induced human T-cell activation and gamma interferon production in vitro.” Infect Immun 75(6): 3197–201.PubMedCrossRefGoogle Scholar
  2. Aleman, M., S. de la Barrera, et al. (2007). “Spontaneous or Mycobacterium tuberculosis-induced apoptotic neutrophils exert opposite effects on the dendritic cell-mediated immune response.” Eur J Immunol 37(6): 1524–37.PubMedCrossRefGoogle Scholar
  3. Aleman, M., S. S. de la Barrera, et al. (2005). “In tuberculous pleural effusions, activated neutrophils undergo apoptosis and acquire a dendritic cell-like phenotype.” J Infect Dis 192(3): 399–409.PubMedCrossRefGoogle Scholar
  4. Aleman, M., A. Garcia, et al. (2002). “Mycobacterium tuberculosis-induced activation accelerates apoptosis in peripheral blood neutrophils from patients with active tuberculosis.” Am J Respir Cell Mol Biol 27(5): 583–92.PubMedGoogle Scholar
  5. Algood, H. M., P. L. Lin, et al. (2005). “Tumor necrosis factor and chemokine interactions in the formation and maintenance of granulomas in tuberculosis.” Clin Infect Dis 41 Suppl 3: S189–93.PubMedCrossRefGoogle Scholar
  6. Algood, H. M., P. L. Lin, et al. (2004). “TNF influences chemokine expression of macrophages in vitro and that of CD11b  +  cells in vivo during Mycobacterium tuberculosis infection.” J Immunol 172(11): 6846–57.PubMedGoogle Scholar
  7. Appelberg, R. (1992). “Mycobacterial infection primes T cells and macrophages for enhanced recruitment of neutrophils.” J Leukoc Biol 51(5): 472–7.PubMedGoogle Scholar
  8. Appelberg, R. (2007). “Neutrophils and intracellular pathogens: beyond phagocytosis and killing.” Trends Microbiol 15(2): 87–92.PubMedCrossRefGoogle Scholar
  9. Awomoyi, A. A., A. Marchant, et al. (2002). “Interleukin-10, polymorphism in SLC11A1 (­formerly NRAMP1), and susceptibility to tuberculosis.” J Infect Dis 186(12): 1808–14.PubMedCrossRefGoogle Scholar
  10. Badri, M., D. Wilson, et al. (2002). “Effect of highly active antiretroviral therapy on incidence of tuberculosis in South Africa: a cohort study.” Lancet 359(9323): 2059–64.PubMedCrossRefGoogle Scholar
  11. Bafica, A., C. A. Scanga, et al. (2005). “Host control of Mycobacterium tuberculosis is regulated by 5-lipoxygenase-dependent lipoxin production.” J Clin Invest 115(6): 1601–6.PubMedCrossRefGoogle Scholar
  12. Barber, S. L., M. Smid, et al. (2009). “Multidrug-resistant tuberculosis and quality-assured medicines.” Lancet 374(9686): 292.PubMedCrossRefGoogle Scholar
  13. Beamer, G. L., D. K. Flaherty, et al. (2008). “Interleukin-10 promotes Mycobacterium tuberculosis disease progression in CBA/J mice.” J Immunol 181(8): 5545–50.PubMedGoogle Scholar
  14. Belisle, J. T., V. D. Vissa, et al. (1997). “Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis.” Science 276(5317): 1420–2.PubMedCrossRefGoogle Scholar
  15. Beveridge, N. E., D. A. Price, et al. (2007). “Immunisation with BCG and recombinant MVA85A induces long-lasting, polyfunctional Mycobacterium tuberculosis-specific CD4+ memory T lymphocyte populations.” Eur J Immunol 37(11): 3089–100.PubMedCrossRefGoogle Scholar
  16. Bhatt, K., S. P. Hickman, et al. (2004). “Cutting edge: a new approach to modeling early lung immunity in murine tuberculosis.” J Immunol 172(5): 2748–51.PubMedGoogle Scholar
  17. Billeskov, R., C. Vingsbo-Lundberg, et al. (2007). “Induction of CD8 T cells against a novel epitope in TB10.4: correlation with mycobacterial virulence and the presence of a functional region of difference-1.” J Immunol 179(6): 3973–81.PubMedGoogle Scholar
  18. Brill, K. J., Q. Li, et al. (2001). “Human natural killer cells mediate killing of intracellular Mycobacterium tuberculosis H37Rv via granule-independent mechanisms.” Infect Immun 69(3): 1755–65.PubMedCrossRefGoogle Scholar
  19. Chackerian, A. A., T. V. Perera, et al. (2001). “Gamma interferon-producing CD4+ T lymphocytes in the lung correlate with resistance to infection with Mycobacterium tuberculosis.” Infect Immun 69(4): 2666–74.PubMedCrossRefGoogle Scholar
  20. Chan, J., X. D. Fan, et al. (1991). “Lipoarabinomannan, a possible virulence factor involved in persistence of Mycobacterium tuberculosis within macrophages.” Infect Immun 59(5): 1755–61.PubMedGoogle Scholar
  21. Chatterjee, D., S. W. Hunter, et al. (1992). “Lipoarabinomannan. Multiglycosylated form of the mycobacterial mannosylphosphatidylinositols.” J Biol Chem 267(9): 6228–33.PubMedGoogle Scholar
  22. Chow, K., D. Ng, et al. (1994). “Protein tyrosine phosphorylation in Mycobacterium tuberculosis.” FEMS Microbiol Lett 124(2): 203–7.PubMedCrossRefGoogle Scholar
  23. Clay, H., H. E. Volkman, et al. (2008). “Tumor necrosis factor signaling mediates resistance to mycobacteria by inhibiting bacterial growth and macrophage death.” Immunity 29(2): 283–94.PubMedCrossRefGoogle Scholar
  24. Cohn, M. A., I. Hjelmso, et al. (2001). “Characterization of Sp1, AP-1, CBF and KRC binding sites and minisatellite DNA as functional elements of the metastasis-associated mts1/S100A4 gene intronic enhancer.” Nucleic Acids Res 29(16): 3335–46.PubMedCrossRefGoogle Scholar
  25. Condos, R., W. N. Rom, et al. (1998). “Local immune responses correlate with presentation and outcome in tuberculosis.” Am J Respir Crit Care Med 157(3 Pt 1): 729–35.PubMedGoogle Scholar
  26. Cooper, A. M. (2009). “Cell-mediated immune responses in tuberculosis.” Annu Rev Immunol 27: 393–422.PubMedCrossRefGoogle Scholar
  27. Cooper, A. M., L. B. Adams, et al. (2002). “IFN-gamma and NO in mycobacterial disease: new jobs for old hands.” Trends Microbiol 10(5): 221–6.PubMedCrossRefGoogle Scholar
  28. Cooper, A. M., D. K. Dalton, et al. (1993). “Disseminated tuberculosis in interferon gamma gene-disrupted mice.” J Exp Med 178(6): 2243–7.PubMedCrossRefGoogle Scholar
  29. Daffe, M. and P. Draper (1998). “The envelope layers of mycobacteria with reference to their pathogenicity.” Adv Microb Physiol 39: 131–203.PubMedCrossRefGoogle Scholar
  30. Demangel, C., P. Bertolino, et al. (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(4): 994–1002.PubMedCrossRefGoogle Scholar
  31. Denis, M. (1994). “Interleukin-12 (IL-12) augments cytolytic activity of natural killer cells toward Mycobacterium tuberculosis-infected human monocytes.” Cell Immunol 156(2): 529–36.PubMedCrossRefGoogle Scholar
  32. Diedrich, C. R., J. T. Mattila, et al. (2010). “Reactivation of latent tuberculosis in cynomolgus macaques infected with SIV is associated with early peripheral T cell depletion and not virus load.” PLoS One 5(3): e9611.Google Scholar
  33. Djoba Siawaya, J. F., M. Ruhwald, et al. (2007). “Correlates for disease progression and prognosis during concurrent HIV/TB infection.” Int J Infect Dis 11(4): 289–99.PubMedCrossRefGoogle Scholar
  34. 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(9): 3428–37.PubMedGoogle Scholar
  35. Eruslanov, E. B., I. V. Lyadova, et al. (2005). “Neutrophil responses to Mycobacterium tuberculosis infection in genetically susceptible and resistant mice.” Infect Immun 73(3): 1744–53.PubMedCrossRefGoogle Scholar
  36. Feng, C. G., M. Kaviratne, et al. (2006). “NK cell-derived IFN-gamma differentially regulates innate resistance and neutrophil response in T cell-deficient hosts infected with Mycobacterium tuberculosis.” J Immunol 177(10): 7086–93.PubMedGoogle Scholar
  37. Fine, P. E. (1995). “Variation in protection by BCG: implications of and for heterologous immunity.” Lancet 346(8986): 1339–45.PubMedCrossRefGoogle Scholar
  38. Flynn, J. L., M. M. Goldstein, et al. (1995). “Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice.” Immunity 2(6): 561–72.PubMedCrossRefGoogle Scholar
  39. Garg, A., P. F. Barnes, et al. (2006). “Vimentin expressed on Mycobacterium tuberculosis-infected human monocytes is involved in binding to the NKp46 receptor.” J Immunol 177(9): 6192–8.PubMedGoogle Scholar
  40. Garg, A., P. F. Barnes, et al. (2008). “Mannose-capped lipoarabinomannan- and prostaglandin E2-dependent expansion of regulatory T cells in human Mycobacterium tuberculosis infection.” Eur J Immunol 38(2): 459–69.PubMedCrossRefGoogle Scholar
  41. Glickman, M. S., J. S. Cox, et al. (2000). “A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis.” Mol Cell 5(4): 717–27.PubMedCrossRefGoogle Scholar
  42. Glickman, M. S. and W. R. Jacobs, Jr. (2001). “Microbial pathogenesis of Mycobacterium tuberculosis: dawn of a discipline.” Cell 104(4): 477–85.PubMedCrossRefGoogle Scholar
  43. Gordon, A. H., P. D. Hart, et al. (1980). “Ammonia inhibits phagosome-lysosome fusion in macrophages.” Nature 286(5768): 79–80.PubMedCrossRefGoogle Scholar
  44. Goren, M. B. (1977). “Phagocyte lysosomes: interactions with infectious agents, phagosomes, and experimental perturbations in function.” Annu Rev Microbiol 31: 507–33.PubMedCrossRefGoogle Scholar
  45. Hart, P. D., M. R. Young, et al. (1983). “Chemical inhibitors of phagosome-lysosome fusion in cultured macrophages also inhibit saltatory lysosomal movements. A combined microscopic and computer study.” J Exp Med 158(2): 477–92.PubMedCrossRefGoogle Scholar
  46. Herb, F., T. Thye, et al. (2008). “ALOX5 variants associated with susceptibility to human pulmonary tuberculosis.” Hum Mol Genet 17(7): 1052–60.PubMedCrossRefGoogle Scholar
  47. Hinchey, J., S. Lee, et al. (2007). “Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis.” J Clin Invest 117(8): 2279–88.PubMedCrossRefGoogle Scholar
  48. Hirsch, C. S., J. J. Ellner, et al. (1997). “In vitro restoration of T cell responses in tuberculosis and augmentation of monocyte effector function against Mycobacterium tuberculosis by natural inhibitors of transforming growth factor beta.” Proc Natl Acad Sci USA 94(8): 3926–31.PubMedCrossRefGoogle Scholar
  49. Hirsch, C. S., T. Yoneda, et al. (1994). “Enhancement of intracellular growth of Mycobacterium tuberculosis in human monocytes by transforming growth factor-beta 1.” J Infect Dis 170(5): 1229–37.PubMedCrossRefGoogle Scholar
  50. Horsburgh, C. R., Jr. (2004). “Priorities for the treatment of latent tuberculosis infection in the United States.” N Engl J Med 350(20): 2060–7.PubMedCrossRefGoogle Scholar
  51. Jick, S. S., E. S. Lieberman, et al. (2006). “Glucocorticoid use, other associated factors, and the risk of tuberculosis.” Arthritis Rheum 55(1): 19–26.PubMedCrossRefGoogle Scholar
  52. Junqueira-Kipnis, A. P., A. Kipnis, et al. (2003). “NK cells respond to pulmonary infection with Mycobacterium tuberculosis, but play a minimal role in protection.” J Immunol 171(11): 6039–45.PubMedGoogle Scholar
  53. Keane, J. (2004). “Tumor necrosis factor blockers and reactivation of latent tuberculosis.” Clin Infect Dis 39(3): 300–2.PubMedCrossRefGoogle Scholar
  54. Keane, J., M. K. Balcewicz-Sablinska, et al. (1997). “Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis.” Infect Immun 65(1): 298–304.PubMedGoogle Scholar
  55. Khader, S. A., S. Partida-Sanchez, et al. (2006). “Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection.” J Exp Med 203(7): 1805–15.PubMedCrossRefGoogle Scholar
  56. Koch, R. (1891). “A Further Communication on a Remedy for Tuberculosis.” Br Med J 1(1568): 125–127.PubMedCrossRefGoogle Scholar
  57. Koul, A., A. Choidas, et al. (2000). “Cloning and characterization of secretory tyrosine phosphatases of Mycobacterium tuberculosis.” J Bacteriol 182(19): 5425–32.PubMedCrossRefGoogle Scholar
  58. Kusner, D. J., C. F. Hall, et al. (1996). “Activation of phospholipase D is tightly coupled to the phagocytosis of Mycobacterium tuberculosis or opsonized zymosan by human macrophages.” J Exp Med 184(2): 585–95.PubMedCrossRefGoogle Scholar
  59. Lasco, T. M., O. C. Turner, et al. (2004). “Rapid accumulation of eosinophils in lung lesions in guinea pigs infected with Mycobacterium tuberculosis.” Infect Immun 72(2): 1147–9.PubMedCrossRefGoogle Scholar
  60. Lawn, S. D., L. G. Bekker, et al. (2005). “How effectively does HAART restore immune responses to Mycobacterium tuberculosis? Implications for tuberculosis control.” AIDS 19(11): 1113–24.PubMedCrossRefGoogle Scholar
  61. Lawn, S. D., L. Myer, et al. (2009). “Short-term and long-term risk of tuberculosis associated with CD4 cell recovery during antiretroviral therapy in South Africa.” AIDS 23(13): 1717–25.PubMedCrossRefGoogle Scholar
  62. Lin, P. L., A. Myers, et al. (2010). “Tumor necrosis factor neutralization results in disseminated disease in acute and latent Mycobacterium tuberculosis infection with normal granuloma structure in a cynomolgus macaque model.” Arthritis Rheum 62(2): 340–50.Google Scholar
  63. Lodoen, M. B. and L. L. Lanier (2006). “Natural killer cells as an initial defense against pathogens.” Curr Opin Immunol 18(4): 391–8.PubMedCrossRefGoogle Scholar
  64. Lonnroth, K. and M. Raviglione (2008). “Global epidemiology of tuberculosis: prospects for control.” Semin Respir Crit Care Med 29(5): 481–91.PubMedCrossRefGoogle Scholar
  65. Maiti, D., A. Bhattacharyya, et al. (2001). “Lipoarabinomannan from Mycobacterium tuberculosis promotes macrophage survival by phosphorylating Bad through a phosphatidylinositol 3-kinase/Akt pathway.” J Biol Chem 276(1): 329–33.PubMedCrossRefGoogle Scholar
  66. McDonough, K. A., Y. Kress, et al. (1993). “Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages.” Infect Immun 61(7): 2763–73.PubMedGoogle Scholar
  67. McKinney, J. D., K. Honer zu Bentrup, et al. (2000). “Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase.” Nature 406(6797): 735–8.PubMedCrossRefGoogle Scholar
  68. Meintjes, G., S. D. Lawn, et al. (2008). “Tuberculosis-associated immune reconstitution inflammatory syndrome: case definitions for use in resource-limited settings.” Lancet Infect Dis 8(8): 516–23.PubMedCrossRefGoogle Scholar
  69. Millman, A. C., M. Salman, et al. (2008). “Natural killer cells, glutathione, cytokines, and innate immunity against Mycobacterium tuberculosis.” J Interferon Cytokine Res 28(3): 153–65.PubMedCrossRefGoogle Scholar
  70. Mittrucker, H. W., U. Steinhoff, et al. (2007). “Poor correlation between BCG vaccination-induced T cell responses and protection against tuberculosis.” Proc Natl Acad Sci USA 104(30): 12434–9.PubMedCrossRefGoogle Scholar
  71. Mohan, V. P., C. A. Scanga, et al. (2001). “Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: possible role for limiting pathology.” Infect Immun 69(3): 1847–55.PubMedCrossRefGoogle Scholar
  72. Moller, M., F. Flachsbart, et al. “A functional haplotype in the 3’untranslated region of TNFRSF1B is associated with tuberculosis in two African populations.” Am J Respir Crit Care Med 181(4): 388–93.Google Scholar
  73. Moretta, A., E. Marcenaro, et al. (2008). “NK cells at the interface between innate and adaptive immunity.” Cell Death Differ 15(2): 226–33.PubMedCrossRefGoogle Scholar
  74. Moulder, J. W. (1985). “Comparative biology of intracellular parasitism.” Microbiol Rev 49(3): 298–337.PubMedGoogle Scholar
  75. Newman, K. C. and E. M. Riley (2007). “Whatever turns you on: accessory-cell-dependent activation of NK cells by pathogens.” Nat Rev Immunol 7(4): 279–91.PubMedCrossRefGoogle Scholar
  76. Pedrosa, J., B. M. Saunders, et al. (2000). “Neutrophils play a protective nonphagocytic role in systemic Mycobacterium tuberculosis infection of mice.” Infect Immun 68(2): 577–83.PubMedCrossRefGoogle Scholar
  77. Peters, W., H. M. Scott, et al. (2001). “Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis.” Proc Natl Acad Sci USA 98(14): 7958–63.PubMedCrossRefGoogle Scholar
  78. Quinn, K. M., F. J. Rich, et al. (2008). “Accelerating the secondary immune response by inactivating CD4(+)CD25(+) T regulatory cells prior to BCG vaccination does not enhance protection against tuberculosis.” Eur J Immunol 38(3): 695–705.PubMedCrossRefGoogle Scholar
  79. Reiley, W. W., M. D. Calayag, et al. (2008). “ESAT-6-specific CD4 T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes.” Proc Natl Acad Sci USA 105(31): 10961–6.PubMedCrossRefGoogle Scholar
  80. Schluger, N. W. and W. N. Rom (1998). “The host immune response to tuberculosis.” Am J Respir Crit Care Med 157(3 Pt 1): 679–91.PubMedGoogle Scholar
  81. 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(11): 5946–54.PubMedCrossRefGoogle Scholar
  82. Scott-Browne, J. P., S. Shafiani, et al. (2007). “Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis.” J Exp Med 204(9): 2159–69.PubMedCrossRefGoogle Scholar
  83. Seddiki, N., S. C. Sasson, et al. (2009). “Proliferation of weakly suppressive regulatory CD4+ T cells is associated with over-active CD4+ T-cell responses in HIV-positive patients with mycobacterial immune restoration disease.” Eur J Immunol 39(2): 391–403.PubMedCrossRefGoogle Scholar
  84. Segal, A. W. (2005). “How neutrophils kill microbes.” Annu Rev Immunol 23: 197–223.PubMedCrossRefGoogle Scholar
  85. Seiler, P., P. Aichele, et al. (2000). “Rapid neutrophil response controls fast-replicating intracellular bacteria but not slow-replicating Mycobacterium tuberculosis.” J Infect Dis 181(2): 671–80.PubMedCrossRefGoogle Scholar
  86. Small, P. M., P. C. Hopewell, et al. (1994). “The epidemiology of tuberculosis in San Francisco. A population-based study using conventional and molecular methods.” N Engl J Med 330(24): 1703–9.PubMedCrossRefGoogle Scholar
  87. Stenger, S., J. P. Rosat, et al. (1999). “Granulysin: a lethal weapon of cytolytic T cells.” Immunol Today 20(9): 390–4.PubMedCrossRefGoogle Scholar
  88. Sugawara, I., T. Udagawa, et al. (2004). “Rat neutrophils prevent the development of tuberculosis.” Infect Immun 72(3): 1804–6.PubMedCrossRefGoogle Scholar
  89. Tan, B. H., C. Meinken, et al. (2006). “Macrophages acquire neutrophil granules for antimicrobial activity against intracellular pathogens.” J Immunol 177(3): 1864–71.PubMedGoogle Scholar
  90. Triccas, J. A., E. Shklovskaya, et al. (2007). “Effects of DNA- and Mycobacterium bovis BCG-based delivery of the Flt3 ligand on protective immunity to Mycobacterium tuberculosis.” Infect Immun 75(11): 5368–75.PubMedCrossRefGoogle Scholar
  91. Turner, J., M. Gonzalez-Juarrero, et al. (2002). “In vivo IL-10 production reactivates chronic ­pulmonary tuberculosis in C57BL/6 mice.” J Immunol 169(11): 6343–51.PubMedGoogle Scholar
  92. Ulrichs, T. and S. H. Kaufmann (2006). “New insights into the function of granulomas in human tuberculosis.” J Pathol 208(2): 261–9.PubMedCrossRefGoogle Scholar
  93. Vankayalapati, R., A. Garg, et al. (2005). “Role of NK cell-activating receptors and their ligands in the lysis of mononuclear phagocytes infected with an intracellular bacterium.” J Immunol 175(7): 4611–7.PubMedGoogle Scholar
  94. Vankayalapati, R., B. Wizel, et al. (2002). “The NKp46 receptor contributes to NK cell lysis of mononuclear phagocytes infected with an intracellular bacterium.” J Immunol 168(7): 3451–7.PubMedGoogle Scholar
  95. Wallis, R. S. (2009). “Infectious complications of tumor necrosis factor blockade.” Curr Opin Infect Dis 22(4): 403–9.PubMedCrossRefGoogle Scholar
  96. Wang, S., M. Wang, et al. (2008). “A novel variable number of tandem repeats (VNTR) polymorphism containing Sp1 binding elements in the promoter of XRCC5 is a risk factor for human bladder cancer.” Mutat Res 638(1–2): 26–36.PubMedGoogle Scholar
  97. Wayne, L. G. and C. D. Sohaskey (2001). “Nonreplicating persistence of mycobacterium tuberculosis.” Annu Rev Microbiol 55: 139–63.PubMedCrossRefGoogle Scholar
  98. Windish, H. P., P. L. Lin, et al. (2009). “Aberrant TGF-beta signaling reduces T regulatory cells in ICAM-1-deficient mice, increasing the inflammatory response to Mycobacterium tuberculosis.” J Leukoc Biol 86(3): 713–25.PubMedCrossRefGoogle Scholar
  99. Wolf, A. J., L. Desvignes, et al. (2008). “Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs.” J Exp Med 205(1): 105–15.PubMedCrossRefGoogle Scholar
  100. Wolf, A. J., B. Linas, et al. (2007). “Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo.” J Immunol 179(4): 2509–19.PubMedGoogle Scholar
  101. Woodworth, J. S., S. M. Fortune, et al. (2008). “Bacterial protein secretion is required for priming of CD8+ T cells specific for the Mycobacterium tuberculosis antigen CFP10.” Infect Immun 76(9): 4199–205.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media LLC 2012

Authors and Affiliations

  1. 1.Department of Microbiology, Immunology and ParasitologyFederal University of Santa CatarinaFlorianopolisBrazil
  2. 2.Divisions of Molecular Immunology and Pulmonary Medicine, Cincinnati Children’s Hospital Medical Center and School of MedicineUniversity of CincinnatiCincinnatiUSA

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