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Clinical and Developmental Immunology
Volume 2012 (2012), Article ID 628293, 13 pages
http://dx.doi.org/10.1155/2012/628293
Review Article

Understanding Delayed T-Cell Priming, Lung Recruitment, and Airway Luminal T-Cell Responses in Host Defense against Pulmonary Tuberculosis

McMaster Immunology Research Centre; Department of Pathology and Molecular Medicine, McMaster University, Hamilton, ON, Canada L8S 4K1

Received 6 December 2011; Accepted 18 January 2012

Academic Editor: S. Sozzani

Copyright © 2012 Christopher R. Shaler et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. “Global tuberculosis control: key findings from the December 2009 WHO report,” The Weekly Epidemiological Record, vol. 85, pp. 69–80, 2009.
  2. D. O. Co, L. H. Hogan, S. I. Kim, and M. Sandor, “Mycobacterial Granulomas: keys to a long-lasting host-pathogen relationship,” Clinical Immunology, vol. 113, no. 2, pp. 130–136, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Ehlers, “Immunity to tuberculosis: a delicate balance between protection and pathology,” FEMS Immunology and Medical Microbiology, vol. 23, no. 2, pp. 149–158, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. S. H. Ferebee, “Controlled chemoprophylaxis trials in tuberculosis. A general review,” Bibliotheca tuberculosea, vol. 26, pp. 28–106, 1970. View at Google Scholar · View at Scopus
  5. I. Baussano, B. G. Williams, P. Nunn, M. Beggiato, U. Fedeli, and F. Scano, “Tuberculosis incidence in prisons: a systematic review,” PLoS Medicine, vol. 7, no. 12, Article ID e1000381, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Gibson, A. Cave, D. Doering, L. Ortiz, and P. Harms, “Socio-cultural factors influencing prevention and treatment of tuberculosis in immigrant and Aboriginal communities in Canada,” Social Science and Medicine, vol. 61, no. 5, pp. 931–942, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. P. A. LoBue, D. A. Enarson, and T. C. Thoen, “Tuberculosis in humans and its epidemiology, diagnosis and treatment in the United States,” International Journal of Tuberculosis and Lung Disease, vol. 14, no. 10, pp. 1226–1232, 2010. View at Google Scholar
  8. P. Andersen and T. M. Doherty, “The success and failure of BCG—Implications for a novel tuberculosis vaccine,” Nature Reviews Microbiology, vol. 3, no. 8, pp. 656–662, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. J. A. C. Sterne, L. C. Rodrigues, and I. N. Guedes, “Does the efficacy of BCG decline with time since vaccination?” International Journal of Tuberculosis and Lung Disease, vol. 2, no. 3, pp. 200–207, 1998. View at Google Scholar · View at Scopus
  10. B. M. Buddle, D. N. Wedlock, N. A. Parlane, L. A. L. Corner, G. W. De Lisle, and M. A. Skinner, “Revaccination of neonatal calves with Mycobacterium bovis BCG reduces the level of protection against bovine tuberculosis induced by a single vaccination,” Infection and Immunity, vol. 71, no. 11, pp. 6411–6419, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. V. M. Vashishtha, “WHO global tuberculosis control report 2009: tuberculosis elimination is a distant dream,” Indian Pediatrics, vol. 46, no. 5, pp. 401–402, 2009. View at Google Scholar · View at Scopus
  12. A. R. Zink, C. Sola, U. Reischl et al., “Characterization of Mycobacterium tuberculosis complex DNAs from Egyptian mummies by spoligotyping,” Journal of Clinical Microbiology, vol. 41, no. 1, pp. 359–367, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. R. Brosch, S. V. Gordon, M. Marmiesse et al., “A new evolutionary scenario for the Mycobacterium tuberculosis complex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 6, pp. 3684–3689, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. G. M Cristina, S. Brisse, R. Brosch et al., “Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis,” PLoS Pathogens, vol. 1, no. 1, article no. e5, pp. 0055–0061, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. I. Hershkovitz, H. D. Donoghue, D. E. Minnikin et al., “Detection and molecular characterization of 9000-year-old Mycobacterium tuberculosis from a neolithic settlement in the Eastern mediterranean,” PLoS One, vol. 3, no. 10, Article ID e3426, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Hershberg, M. Lipatov, P. M. Small et al., “High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography,” PLoS Biology, vol. 6, no. 12, article no. e311, pp. 2658–2671, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. K. H. Ely, L. S. Cauley, A. D. Roberts, J. W. Brennan, T. Cookenham, and D. L. Woodland, “Nonspecific recruitment of memory CD8+ T cells to the lung airways during respiratory virus infections,” Journal of Immunology, vol. 170, no. 3, pp. 1423–1429, 2003. View at Google Scholar · View at Scopus
  18. O. L. C. Wijburg, S. Dinatale, J. Vadolas, N. Van Rooijen, and R. A. Strugnell, “Alveolar macrophages regulate the induction of primary cytotoxic T- lymphocyte responses during influenza virus infection,” Journal of Virology, vol. 71, no. 12, pp. 9450–9457, 1997. View at Google Scholar · View at Scopus
  19. WHO, “Global tuberculosis control 2009,” World Health Organization WHO/HTM/TB/2009, 2009. View at Google Scholar
  20. B. K. Kang and L. S. Schlesinger, “Characterization of mannose receptor-dependent phagocytosis mediated by Mycobacterium tuberculosis lipoarabinomannan,” Infection and Immunity, vol. 66, no. 6, pp. 2769–2777, 1998. View at Google Scholar · View at Scopus
  21. J. L. Flynn and J. Chan, “Immune evasion by Mycobacterium tuberculosis: living with the enemy,” Current Opinion in Immunology, vol. 15, no. 4, pp. 450–455, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Blomgran and J. D. Ernst, “Lung neutrophils facilitate activation of naive antigen-specific CD4 + T cells during Mycobacterium tuberculosis infection,” Journal of Immunology, vol. 186, no. 12, pp. 7110–7119, 2011. View at Publisher · View at Google Scholar
  23. A. J. Wolf, B. Linas, G. J. Trevejo-Nuñez et al., “Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo,” Journal of Immunology, vol. 179, no. 4, pp. 2509–2519, 2007. View at Google Scholar · View at Scopus
  24. L. E. Bermudez and J. Goodman, “Mycobacterium tuberculosis invades and replicates within type II alveolar cells,” Infection and Immunity, vol. 64, no. 4, pp. 1400–1406, 1996. View at Google Scholar · View at Scopus
  25. K. Kudo, H. Sano, H. Takahashi et al., “Pulmonary collectins enhance phagocytosis of Mycobacterium avium through increased activity of mannose receptor,” Journal of Immunology, vol. 172, no. 12, pp. 7592–7602, 2004. View at Google Scholar · View at Scopus
  26. E. K. Jo, “Mycobacterial interaction with innate receptors: TLRs, C-type lectins, and NLRs,” Current Opinion in Infectious Diseases, vol. 21, no. 3, pp. 279–286, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Chieppa, G. Bianchi, A. Doni et al., “Cross-linking of the mannose receptor on monocyte-derived dendritic cells activates an anti-inflammatory immunosuppressive program,” Journal of Immunology, vol. 171, no. 9, pp. 4552–4560, 2003. View at Google Scholar · View at Scopus
  28. L. M. Rocha-Ramírez, I. Estrada-García, L. M. López-Marín et al., “Mycobacterium tuberculosis lipids regulate cytokines, TLR-2/4 and MHC class II expression in human macrophages,” Tuberculosis, vol. 88, no. 3, pp. 212–220, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Bafica, C. A. Scanga, C. G. Feng, C. Leifer, A. Cheever, and A. Sher, “TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis,” Journal of Experimental Medicine, vol. 202, no. 12, pp. 1715–1724, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Divangahi, S. Mostowy, F. Coulombe et al., “NOD2-deficient mice have impaired resistance to Mycobacterium tuberculosis infection through defective innate and adaptive immunity,” Journal of Immunology, vol. 181, no. 10, pp. 7157–7165, 2008. View at Google Scholar · View at Scopus
  31. R. I. Tapping and P. S. Tobias, “Mycobacterial lipoarabinomannan mediates physical interactions between TLR1 and TLR2 to induce signaling,” Journal of Endotoxin Research, vol. 9, no. 4, pp. 264–268, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. H. E. Volkman, T. C. Pozos, J. Zheng, J. M. Davis, J. F. Rawls, and L. Ramakrishnan, “Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium,” Science, vol. 327, no. 5964, pp. 466–469, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Herold, W. Von Wulffen, M. Steinmueller et al., “Alveolar epithelial cells direct monocyte transepithelial migration upon influenza virus infection: impact of chemokines and adhesion molecules,” Journal of Immunology, vol. 177, no. 3, pp. 1817–1824, 2006. View at Google Scholar · View at Scopus
  34. S. Rosseau, J. Selhorst, K. Wiechmann et al., “Monocyte migration through the alveolar epithelial barrier: adhesion molecule mechanisms and impact of chemokines,” Journal of Immunology, vol. 164, no. 1, pp. 427–435, 2000. View at Google Scholar · View at Scopus
  35. M. H. Qureshi, J. Cook-Mills, D. E. Doherty, and B. A. Garvy, “TNF-α-dependent icam-1- and vcam-1-mediated inflammatory responses are delayed in neonatal mice infected with Pneumocystis carinii,” Journal of Immunology, vol. 171, no. 9, pp. 4700–4707, 2003. View at Google Scholar · View at Scopus
  36. L. E. Bermudez, F. J. Sangari, P. Kolonoski, M. Petrofsky, and J. Goodman, “The efficiency of the translocation of Mycobacterium tuberculosis across a bilayer of epithelial and endothelial cells as a model of the alveolar wall is a consequence of transport within mononuclear phagocytes and invasion of alveolar epithelial cells,” Infection and Immunity, vol. 70, no. 1, pp. 140–146, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. A. S. McWilliam, D. Nelson, J. A. Thomas, and P. G. Holt, “Rapid dendritic cell recruitment is a hallmark of the acute inflammatory response at mucosal surfaces,” Journal of Experimental Medicine, vol. 179, no. 4, pp. 1331–1336, 1994. View at Google Scholar · View at Scopus
  38. D. N. Cook and K. Bottomly, “Innate immune control of pulmonary dendritic cell trafficking,” Proceedings of the American Thoracic Society, vol. 4, no. 3, pp. 234–239, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. S. McCormick, C. R. Shaler, and Z. Xing, “Pulmonary mucosal dendritic cells in T-cell activation: implications for TB therapy,” Expert Review of Respiratory Medicine, vol. 5, no. 1, pp. 75–85, 2011. View at Publisher · View at Google Scholar
  40. A. J. Wolf, L. Desvignes, B. Linas et al., “Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs,” Journal of Experimental Medicine, vol. 205, no. 1, pp. 105–115, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. U. Maus, J. Huwe, L. Ermert, M. Ermert, W. Seeger, and J. Lohmeyer, “Molecular pathways of monocyte emigration into the alveolar air space of intact mice,” American Journal of Respiratory and Critical Care Medicine, vol. 165, no. 1, pp. 95–100, 2002. View at Google Scholar · View at Scopus
  42. F. Blank, M. Wehrli, A. Lehmann et al., “Macrophages and dendritic cells express tight junction proteins and exchange particles in an in vitro model of the human airway wall,” Immunobiology, vol. 216, no. 1-2, pp. 86–95, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. D. V. Pechkovsky, T. Goldmann, C. Ludwig et al., “CCR2 and CXCR3 agonistic chemokines are differently expressed and regulated in human alveolar epithelial cells type II,” Respiratory Research, vol. 6, article no. 75, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. A. J. Thorley, P. A. Ford, M. A. Giembycz, P. Goldstraw, A. Young, and T. D. Tetley, “Differential regulation of cytokine release and leukocyte migration by lipopolysaccharide-stimulated primary human lung alveolar type II epithelial cells and macrophages,” Journal of Immunology, vol. 178, no. 1, pp. 463–473, 2007. View at Google Scholar · View at Scopus
  45. M. Eghtesad, H. E. Jackson, and A. C. Cunningham, “Primary human alveolar epithelial cells can elicit the transendothelial migration of CD14+ monocytes and CD3+ lymphocytes,” Immunology, vol. 102, no. 2, pp. 157–164, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Liu, M. Q. Zhao, L. Xu et al., “Requirement for tumor necrosis factor-receptor 2 in alveolar chemokine expression depends upon the form of the ligand,” American Journal of Respiratory Cell and Molecular Biology, vol. 33, no. 5, pp. 463–469, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. W. Peters, H. M. Scott, H. F. Chambers, J. L. Flynn, I. F. Charo, and J. D. Ernst, “Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 14, pp. 7958–7963, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Lagranderie, M. A. Nahori, A. M. Balazuc et al., “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, vol. 108, no. 3, pp. 352–364, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. A. C. Kirby, M. C. Coles, and P. M. Kaye, “Alveolar macrophages transport pathogens to lung draining lymph nodes,” Journal of Immunology, vol. 183, no. 3, pp. 1983–1989, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. V. Abadie, E. Badell, P. Douillard et al., “Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes,” Blood, vol. 106, no. 5, pp. 1843–1850, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. W. W. Reiley, M. D. Calayag, S. T. Wittmer et al., “ESAT-6-specific CD4 T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 31, pp. 10961–10966, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Hamilton-Easton and M. Eichelberger, “Virus-specific antigen presentation by different subsets of cells from lung and mediastinal lymph node tissues of influenza virus-infected mice,” Journal of Virology, vol. 69, no. 10, pp. 6359–6366, 1995. View at Google Scholar · View at Scopus
  53. T. W. Klein, C. Newton, Y. Yamamoto, and H. Friedman, “Immune responses to Legionella,” in Opportunistic Intracellular Bacteria and Immunity, L. J. Paradise, H. Friedman, and M. Bendinelli, Eds., pp. 149–166, Plenum Press, New York, NY, USA, 1999. View at Google Scholar
  54. M. L. Ricci, A. Torosantucci, M. Scaturro, P. Chiani, L. Baldassarri, and M. C. Pastoris, “Induction of protective immunity by Legionella pneumophila flagellum in an A/J mouse model,” Vaccine, vol. 23, no. 40, pp. 4811–4820, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. P. Hoffman, H. Friedman, and M. Bendinelli, Legionella pneumophila: Pathogenesis and Immunity, Infectious Agents and Pathogenesis, Springer, 2007.
  56. R. Teitelbaum, W. Schubert, L. Gunther et al., “The M cell as a portal of entry to the lung for the bacterial pathogen Mycobacterium tuberculosis,” Immunity, vol. 10, no. 6, pp. 641–650, 1999. View at Publisher · View at Google Scholar · View at Scopus
  57. G. S. García-Romo, A. Pedroza-González, D. Aguilar-León et al., “Airways infection with virulent Mycobacterium tuberculosis delays the influx of dendritic cells and the expression of costimulatory molecules in mediastinal lymph nodes,” Immunology, vol. 112, no. 4, pp. 661–668, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. S. A. Khader, S. Partida-Sanchez, G. Bell et al., “Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection,” Journal of Experimental Medicine, vol. 203, no. 7, pp. 1805–1815, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. R. T. Robinson, S. A. Khader, C. A. Martino et al., “Mycobacterium tuberculosis infection induces il12rb1 splicing to generate a novel IL-12Rβ1 isoform that enhances DC migration,” Journal of Experimental Medicine, vol. 207, no. 3, pp. 591–605, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. A. M. Cooper, “Cell-mediated immune responses in tuberculosis,” Annual Review of Immunology, vol. 27, pp. 393–422, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. A. A. Chackerian, J. M. Alt, T. V. Perera, C. C. Dascher, and S. M. Behar, “Dissemination of Mycobacterium tuberculosis is influenced by host factors and precedes the initiation of T-cell immunity,” Infection and Immunity, vol. 70, no. 8, pp. 4501–4509, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Kugathasan, E. K. Roediger, C. L. Small, S. McCormick, P. Yang, and Z. Xing, “CD11c+ antigen presenting cells from the alveolar space, lung parenchyma and spleen differ in their phenotype and capabilities to activate naïve and antigen-primed T cells,” BMC Immunology, vol. 9, article no. 48, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. A. N. Desch, G. J. Randolph, K. Murphy et al., “CD103+ pulmonary dendritic cells preferentially acquire and present apoptotic cell-associated antigen,” Journal of Experimental Medicine, vol. 208, no. 9, pp. 1789–1797, 2011. View at Publisher · View at Google Scholar
  64. S. O'Leary, M. P. O'Sullivan, and J. Keane, “IL-10 blocks phagosome maturation in Mycobacterium tuberculosis-infected human macrophages,” American Journal of Respiratory Cell and Molecular Biology, vol. 45, no. 1, pp. 172–180, 2011. View at Publisher · View at Google Scholar
  65. S. Nair, P. A. Ramaswamy, S. Ghosh et al., “The PPE18 of Mycobacterium tuberculosis interacts with TLR2 and activates IL-10 induction in macrophage,” Journal of Immunology, vol. 183, no. 10, pp. 6269–6281, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. A. J. Gehring, R. E. Rojas, D. H. Canaday, D. L. Lakey, C. V. Harding, and W. H. Boom, “The Mycobacterium tuberculosis 19-kilodalton lipoprotein inhibits gamma interferon-regulated HLA-DR and FcγR1 on human macrophages through toll-like receptor 2,” Infection and Immunity, vol. 71, no. 8, pp. 4487–4497, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. R. K. Pai, M. Convery, T. A. Hamilton, W. Henry Boom, and C. V. Harding, “Inhibition of IFN-γ-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion,” Journal of Immunology, vol. 171, no. 1, pp. 175–184, 2003. View at Google Scholar · View at Scopus
  68. N. D. Pecora, S. A. Fulton, S. M. Reba et al., “Mycobacterium bovis BCG decreases MHC-II expression in vivo on murine lung macrophages and dendritic cells during aerosol infection,” Cellular Immunology, vol. 254, no. 2, pp. 94–104, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. R. K. Pai, M. E. Pennini, A. A. R. Tobian, D. H. Canaday, W. H. Boom, and C. V. Harding, “Prolonged toll-like receptor signaling by Mycobacterium tuberculosis and its 19-kilodalton lipoprotein inhibits gamma interferon-induced regulation of selected genes in macrophages,” Infection and Immunity, vol. 72, no. 11, pp. 6603–6614, 2004. View at Publisher · View at Google Scholar · View at Scopus
  70. D. Wong, H. Bach, J. Sun, Z. Hmama, and Y. Av-Gay, “Mycobacterium tuberculosis protein tyrosine phosphatase (PtpA) excludes host vacuolar-H+-ATPase to inhibit phagosome acidification,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 48, pp. 19371–19376, 2011. View at Publisher · View at Google Scholar
  71. C. Kan-Sutton, C. Jagannath, and R. L. Hunter, “Trehalose 6,6′-dimycolate on the surface of Mycobacterium tuberculosis modulates surface marker expression for antigen presentation and costimulation in murine macrophages,” Microbes and Infection, vol. 11, no. 1, pp. 40–48, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Shafiani, G. Tucker-Heard, A. Kariyone, K. Takatsu, and K. B. Urdahl, “Pathogen-specific regulatory T cells delay the arrival of effector T cells in the lung during early tuberculosis,” Journal of Experimental Medicine, vol. 207, no. 7, pp. 1409–1420, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. R. S. Veazey, D. W. Horohov, J. L. Krahenbuhl, H. W. Taylor, J. L. Oliver, and T. G. Snider, “Differences in the kinetics of T cell accumulations in C3H/HeN (Bcg-resistant) and C57BL/6 (Bcg-susceptible) mice infected with Mycobacterium paratuberculosis,” Comparative Immunology, Microbiology and Infectious Diseases, vol. 19, no. 4, pp. 289–304, 1996. View at Publisher · View at Google Scholar · View at Scopus
  74. F. A. Post, C. Manca, O. Neyrolles, B. Ryffel, D. B. Young, and G. Kaplan, “Mycobacterium tuberculosis 19-kilodalton lipoprotein inhibits Mycobacterium smegmatis-induced cytokine production by human macrophages in vitro,” Infection and Immunity, vol. 69, no. 3, pp. 1433–1439, 2001. View at Publisher · View at Google Scholar · View at Scopus
  75. A. Bohsali, H. Abdalla, K. Velmurugan, and V. Briken, “The non-pathogenic mycobacteria M. smegmatis and M. fortuitum induce rapid host cell apoptosis via a caspase-3 and TNF dependent pathway,” BMC Microbiology, vol. 10, article no. 237, pp. 1–12, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. J. B. Torrelles and L. S. Schlesinger, “Diversity in Mycobacterium tuberculosis mannosylated cell wall determinants impacts adaptation to the host,” Tuberculosis, vol. 90, no. 2, pp. 84–93, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. N. Majumder, S. Bhattacharjee, R. Dey, S. Bhattacharyya (Majumdar) S., N. K. Pal, and S. Majumdar, “Arabinosylated lipoarabinomannan modulates the impaired cell mediated immune response in Mycobacterium tuberculosis H37Rv infected C57BL/6 mice,” Microbes and Infection, vol. 10, no. 4, pp. 349–357, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. A. K. Mishra, N. N. Driessen, B. J. Appelmelk, and G. S. Besra, “Lipoarabinomannan and related glycoconjugates: structure, biogenesis and role in Mycobacterium tuberculosis physiology and host-pathogen interaction,” FEMS Microbiology Reviews, vol. 35, no. 6, pp. 1126–1157, 2011. View at Publisher · View at Google Scholar
  79. D. Chatterjee, K. Lowell, B. Rivoire, M. R. McNeil, and P. J. Brennan, “Lipoarabinomannan of Mycobacterium tuberculosis. Capping with mannosyl residues in some strains,” Journal of Biological Chemistry, vol. 267, no. 9, pp. 6234–6239, 1992. View at Google Scholar · View at Scopus
  80. C. W. Wieland, S. Knapp, S. Florquin et al., “Non-mannose-capped lipoarabinomannan induces lung inflammation via toll-like receptor 2,” American Journal of Respiratory and Critical Care Medicine, vol. 170, no. 12, pp. 1367–1374, 2004. View at Publisher · View at Google Scholar · View at Scopus
  81. H. L. Birch, L. J. Alderwick, B. J. Appelmelk et al., “A truncated lipoglycan from mycobacteria with altered immunological properties,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 6, pp. 2634–2639, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. R. A. Fratti, J. Chua, I. Vergne, and V. Deretic, “Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 9, pp. 5437–5442, 2003. View at Publisher · View at Google Scholar · View at Scopus
  83. T. B. H. Geijtenbeek, S. J. Van Vliet, E. A. Koppel et al., “Mycobacteria target DC-SIGN to suppress dendritic cell function,” Journal of Experimental Medicine, vol. 197, no. 1, pp. 7–17, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. P. Dinadayala, D. Kaur, S. Berg et al., “Genetic basis for the synthesis of the immunomodulatory mannose caps of lipoarabinomannan in Mycobacterium tuberculosis,” Journal of Biological Chemistry, vol. 281, no. 29, pp. 20027–20035, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. V. Deretic, S. Singh, S. Master et al., “Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism,” Cellular Microbiology, vol. 8, no. 5, pp. 719–727, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. V. Briken, S. A. Porcelli, G. S. Besra, and L. Kremer, “Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response,” Molecular Microbiology, vol. 53, no. 2, pp. 391–403, 2004. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Ehrt and D. Schnappinger, “Mycobacterial survival strategies in the phagosome: defence against host stresses,” Cellular Microbiology, vol. 11, no. 8, pp. 1170–1178, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. H. Bruns, C. Meinken, P. Schauenberg et al., “Anti-TNF immunotherapy reduces CD8+ T cell-mediated antimicrobial activity against Mycobacterium tuberculosis in humans,” Journal of Clinical Investigation, vol. 119, no. 5, pp. 1167–1177, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. S. H. E. Kaufmann, “Protection against tuberculosis: cytokines, T cells, and macrophages,” Annals of the Rheumatic Diseases, vol. 61, no. 2, pp. ii54–ii58, 2002. View at Google Scholar · View at Scopus
  90. T. Mogues, M. E. Goodrich, L. Ryan, R. LaCourse, and R. J. North, “The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice,” Journal of Experimental Medicine, vol. 193, no. 3, pp. 271–280, 2001. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Divangahi, D. Desjardins, C. Nunes-Alves, H. G. Remold, and S. M. Behar, “Eicosanoid pathways regulate adaptive immunity to Mycobacterium tuberculosis,” Nature Immunology, vol. 11, no. 8, pp. 751–758, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. A. M. Cooper, J. E. Callahan, M. Keen, J. T. Belisle, and I. M. Orme, “Expression of memory immunity in the lung following re-exposure to Mycobacterium tuberculosis,” Tubercle and Lung Disease, vol. 78, no. 1, pp. 67–73, 1997. View at Publisher · View at Google Scholar · View at Scopus
  93. Y.-J. Jung, L. Ryan, R. LaCourse, and R. J. North, “Properties and protective value of the secondary versus primary T helper type 1 response to airborne Mycobacterium tuberculosis infection in mice,” Journal of Experimental Medicine, vol. 201, no. 12, pp. 1915–1924, 2005. View at Publisher · View at Google Scholar · View at Scopus
  94. S. A. Khader, G. K. Bell, J. E. Pearl et al., “IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge,” Nature Immunology, vol. 8, no. 4, pp. 369–377, 2007. View at Publisher · View at Google Scholar · View at Scopus
  95. C. G. Feng, A. G. D. Bean, H. Hooi, H. Briscoe, and W. J. Britton, “Increase in gamma interferon-secreting CD8+, as well as CD4+, T cells in lungs following aerosol infection with Mycobacterium tuberculosis,” Infection and Immunity, vol. 67, no. 7, pp. 3242–3247, 1999. View at Google Scholar · View at Scopus
  96. M. Jeyanathan, A. Heriazon, and Z. Xing, “Airway iuminal T cells: a newcomer on the stage of TB vaccination strategies,” Trends in Immunology, vol. 31, no. 7, pp. 247–252, 2010. View at Publisher · View at Google Scholar · View at Scopus
  97. H. M. Scott Algood and J. L. Flynn, “CCR5-deficient mice control Mycobacterium tuberculosis infection despite increased pulmonary lymphocytic infiltration,” Journal of Immunology, vol. 173, no. 5, pp. 3287–3296, 2004. View at Google Scholar · View at Scopus
  98. B. Vesosky, E. K. Rottinghaus, P. Stromberg, J. Turner, and G. Beamer, “CCL5 participates in early protection against Mycobacterium tuberculosis,” Journal of Leukocyte Biology, vol. 87, no. 6, pp. 1153–1165, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. S. A. Khader, J. Rangel-Moreno, J. J. Fountain et al., “In a murine tuberculosis model, the absence of homeostatic chemokines delays granuloma formation and protective immunity,” Journal of Immunology, vol. 183, no. 12, pp. 8004–8014, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. C. G. Feng, W. J. Britton, U. Palendira, N. L. Groat, H. Briscoe, and A. G. D. Bean, “Up-regulation of VCAM-1 and differential expansion of β integrin- expressing T lymphocytes are associated with immunity to pulmonary Mycobacterium tuberculosis infection,” Journal of Immunology, vol. 164, no. 9, pp. 4853–4860, 2000. View at Google Scholar · View at Scopus
  101. S. Ghosh, A. A. Chackerian, C. M. Parker, C. M. Ballantyne, and S. M. Behar, “The LFA-1 adhesion molecule is required for protective immunity during pulmonary Mycobacterium tuberculosis infection,” Journal of Immunology, vol. 176, no. 8, pp. 4914–4922, 2006. View at Google Scholar · View at Scopus
  102. J. G. Egen, A. G. Rothfuchs, C. G. Feng, N. Winter, A. Sher, and R. N. Germain, “Macrophage and T cell dynamics during the development and disintegration of Mycobacterial Granulomas,” Immunity, vol. 28, no. 2, pp. 271–284, 2008. View at Publisher · View at Google Scholar · View at Scopus
  103. S. Saito and M. Nakano, “Nitric oxide production by peritoneal macrophages of Mycobacterium bovis BCG-infected or non-infected mice: regulatory roles of T lymphocytes and cytokines,” Journal of Leukocyte Biology, vol. 59, no. 6, pp. 908–915, 1996. View at Google Scholar · View at Scopus
  104. B. M. Saunders and W. J. Britton, “Life and death in the granuloma: immunopathology of tuberculosis,” Immunology and Cell Biology, vol. 85, no. 2, pp. 103–111, 2007. View at Publisher · View at Google Scholar · View at Scopus
  105. J. Wang, J. Wakeham, R. Harkness, and Z. Xing, “Macrophages are a significant source of type 1 cytokines during mycobacterial infection,” Journal of Clinical Investigation, vol. 103, no. 7, pp. 1023–1029, 1999. View at Google Scholar · View at Scopus
  106. S. Ehlers, S. Kutsch, J. Benini et al., “NOS2-derived nitric oxide regulates the size, quantity and quality of granuloma formation in Mycobacterium avium-infected mice without affecting bacterial loads,” Immunology, vol. 98, no. 3, pp. 313–323, 1999. View at Publisher · View at Google Scholar · View at Scopus
  107. Y. J. Jung, R. LaCourse, L. Ryan, and R. J. North, “Virulent but not avirulent Mycobacterium tuberculosis can evade the growth inhibitory action of a T helper 1-dependent, nitric oxide synthase 2-independent defense in mice,” Journal of Experimental Medicine, vol. 196, no. 7, pp. 991–998, 2002. View at Publisher · View at Google Scholar · View at Scopus
  108. A. M. Cooper, D. K. Dalton, T. A. Stewart, J. P. Griffin, D. G. Russell, and I. M. Orme, “Disseminated tuberculosis in interferon γ gene-disrupted mice,” Journal of Experimental Medicine, vol. 178, no. 6, pp. 2243–2247, 1993. View at Publisher · View at Google Scholar · View at Scopus
  109. Z. Xing, A. Zganiacz, and M. Santosuosso, “Role of IL-12 in macrophage activation during intracellular infection: IL-12 and mycobacteria synergistically release TNF-α and nitric oxide from macrophages via IFN-γ induction,” Journal of Leukocyte Biology, vol. 68, no. 6, pp. 897–902, 2000. View at Google Scholar · View at Scopus
  110. L. H. Hogan, E. Heninger, R. A. Elsner et al., “Requirements for CD4+ T cell levels in acute Mycobacterium bovis strain bacille Calmette Guérin (BCG)-induced granulomas differ for optimal mycobacterial control versus granuloma formation,” International Immunology, vol. 19, no. 5, pp. 627–633, 2007. View at Publisher · View at Google Scholar
  111. D. R. Roach, A. G. D. Bean, C. Demangel, M. P. France, H. Briscoe, and W. J. Britton, “TNF regulates chemokine induction essential for cell recruitment, granuloma formation, and clearance of mycobacterial infection,” Journal of Immunology, vol. 168, no. 9, pp. 4620–4627, 2002. View at Google Scholar · View at Scopus
  112. M. Sandor, J. V. Weinstock, and T. A. Wynn, “Granulomas in schistosome and mycobacterial infections: a model of local immune responses,” Trends in Immunology, vol. 24, no. 1, pp. 44–52, 2003. View at Publisher · View at Google Scholar · View at Scopus
  113. J. Wakeham, J. Wang, J. Magram et al., “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,” Journal of Immunology, vol. 160, no. 12, pp. 6101–6111, 1998. View at Google Scholar · View at Scopus
  114. A. Zganiacz, M. Santosuosso, J. Wang et al., “TNF-α is a critical negative regulator of type 1 immune activation during intracellular bacterial infection,” Journal of Clinical Investigation, vol. 113, no. 3, pp. 401–413, 2004. View at Publisher · View at Google Scholar · View at Scopus
  115. J. Egen, A. Rothfuchs, C. Feng, M. Horwitz, A. Sher, and R. Germain, “Intravital imaging reveals limited antigen presentation and T cell effector function in Mycobacterial Granulomas,” Immunity, vol. 34, no. 5, pp. 807–819, 2011. View at Publisher · View at Google Scholar
  116. C. R. Shaler, K. Kugathasan, S. McCormick et al., “Pulmonary mycobacterial granuloma: increased IL-10 production contributes to establishing a symbiotic host-microbe microenvironment,” American Journal of Pathology, vol. 178, no. 4, pp. 1622–1634, 2011. View at Publisher · View at Google Scholar
  117. C. Paige and W. R. Bishai, “Penitentiary or penthouse condo: the tuberculous granuloma from the microbe's point of view,” Cellular Microbiology, vol. 12, no. 3, pp. 301–309, 2010. View at Publisher · View at Google Scholar · View at Scopus
  118. Z. Xing, “Importance of T-cell location rekindled: implication for tuberculosis vaccination strategies,” Expert Review of Vaccines, vol. 8, no. 11, pp. 1465–1468, 2009. View at Publisher · View at Google Scholar · View at Scopus
  119. C. N. Horvath, C. R. Shaler, M. Jeyanathan, A. Zganiacz, and Z. Xing, “Mechanisms of delayed anti-tuberculosis protection in the lung of parenteral-BCGvaccinated hosts: a critical role of airway luminal T cells,” Mucosal Immunology. In press.
  120. J. Wang, L. Thorson, R. W. Stokes et al., “Single mucosal, but not parenteral, immunization with recombinant adenoviral-based vaccine provides potent protection from pulmonary tuberculosis,” Journal of Immunology, vol. 173, no. 10, pp. 6357–6365, 2004. View at Google Scholar · View at Scopus
  121. N. P. Goonetilleke, H. McShane, C. M. Hannan, R. J. Anderson, R. H. Brookes, and A. V. S. Hill, “Enhanced immunogenicity and protective efficacy against Mycobacterium tuberculosis of bacille Calmette-Guérin vaccine using mucosal administration and boosting with a recombinant modified vaccinia virus Ankara,” Journal of Immunology, vol. 171, no. 3, pp. 1602–1609, 2003. View at Google Scholar · View at Scopus
  122. J. Dietrich, C. Andersen, R. Rappuoli, T. M. Doherty, C. G. Jensen, and P. Andersen, “Mucosal administration of Ag85B-ESAT-6 protects against infection with Mycobacterium tuberculosis and boosts prior bacillus Calmette-Guérin immunity,” Journal of Immunology, vol. 177, no. 9, pp. 6353–6360, 2006. View at Google Scholar · View at Scopus
  123. M. Santosuosso, X. Zhang, S. McCormick, J. Wang, M. Hitt, and Z. Xing, “Mechanisms of mucosal and parenteral tuberculosis vaccinations: adenoviral-based mucosal immunization preferentially elicits sustained accumulation of immune protective CD4 and CD8 T cells within the airway lumen,” Journal of Immunology, vol. 174, no. 12, pp. 7986–7994, 2005. View at Google Scholar · View at Scopus
  124. M. Jeyanathan, J. Mu, K. Kugathasan et al., “Airway delivery of soluble mycobacterial antigens restores protective mucosal immunity by single intramuscular plasmid DNA tuberculosis vaccination: role of proinflammatory signals in the lung,” Journal of Immunology, vol. 181, no. 8, pp. 5618–5626, 2008. View at Google Scholar · View at Scopus
  125. M. Santosuosso, S. McCormick, E. Roediger et al., “Mucosal luminal manipulation of T cell geography switches on protective efficacy by otherwise ineffective parenteral genetic immunization,” Journal of Immunology, vol. 178, no. 4, pp. 2387–2395, 2007. View at Google Scholar · View at Scopus