Within the enemy's camp: Contribution of the granuloma to the dissemination, persistence and transmission of Mycobacterium tuberculosis

Frontiers in Immunology

Volumn 4, Issue FRB, 2013, Pages

  Shaler, Christopher R ^a   Horvath, Carly N ^a   Jeyanathan, Mangalakumari ^a   Xing, Zhou ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Bacterial persistence; Granuloma; Immune regulation; Immunopathology; Mycobacteria; Tuberculosis

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CORD FACTOR; EARLY SECRETORY ANTIGENIC TARGET 6; GAMMA INTERFERON; GELATINASE B; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; NITRIC OXIDE; TUMOR NECROSIS FACTOR;

ANTIGEN PRESENTING CELL; DISEASE TRANSMISSION; GENE EXPRESSION; GRANULOMA; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; LUNG TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; NECROSIS; NONHUMAN; REVIEW; T LYMPHOCYTE; UPREGULATION;

EID: 84883714353     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00030     Document Type: Review

References (82)

1. Algood, H. M., Lin, P. L., and Flynn, J. L. (2005). Tumor necrosis factor and chemokine interactions in the formation and maintenance of granulomas in tuberculosis. Clin. Infect. Dis. 41, S189-S193.
2. Anis, M. M., Fulton, S. A., Reba, S. M., Liu, Y., Harding, C. V., and Boom, W. H. (2008). Modulation of pulmonary dendritic cell function during mycobacterial infection. Infect. Immun. 76, 671-677.
3. Aston, C., Rom, W. N., Talbot, A. T., and Reibman, J. (1998). Early inhibition of mycobacterial growth by human alveolar macrophages is not due to nitric oxide. Am. J. Respir. Crit. Care Med. 157, 1943-1950.
4. Barry, C. E. III, Boshoff, H. I., Dartois, V., Dick, T., Ehrt, S., Flynn, J., et al. (2009). The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat. Rev. Microbiol. 7, 845-855.
5. Beham, A. W., Puellmann, K., Laird, R., Fuchs, T., Streich, R., Breysach, C., et al. (2011). A TNF-regulated recombinatorial macrophage immune receptor implicated in granuloma formation in tuberculosis. PLoS Pathog. 7:e1002375. doi: 10.1371/journal.ppat.1002375
6. Behler, F, Steinwede, K., Balboa, L., Ueberberg, B., Maus, R., Kirchhof, G., et al. (2012). Role of Mincle in alveolar macrophage-dependent innate immunity against mycobacterial infections in mice. J. Immunol. 189, 3121-3129.
7. Birkness, K. A., Guarner, J., Sable, S. B., Tripp, R. A., Kellar, K. L., Bartlett, J., et al. (2007). An in vitro model of the leukocyte interactions associated with granuloma formation in Mycobacterium tuberculosis infection. Immunol. Cell Biol. 85, 160-168.
8. Capuano, S. V. III, Croix, D. A., Pawar, S., Zinovik, A., Myers, A., Lin, P. L., et al. (2003). Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection. Infect. Immun. 71, 5831-5844.
9. Cardona, P. J. (2009). A dynamic reinfection hypothesis of latent tuberculosis infection. Infection 37, 80-86.
10. Cardona, P. J. (2010). Revisiting the natural history of tuberculosis. The inclusion of constant reinfection, host tolerance, and damage-response frameworks leads to a better understanding of latent infection and its evolution towards active disease. Arch. Immunol. Ther. Exp. 58, 7-14.
11. Cardona, P. J., and Ivanyi, J. (2011). The secret trumps, impelling the pathogenicity of tubercle bacilli. Enferm. Infecc. Microbiol. Clin. 29(Suppl. 1), 14-19.
12. Castano, D., Barrera, L. F., and Rojas, M. (2011). Mycobacterium tuberculosis alters the differentiation of monocytes into macrophages in vitro. Cell. Immunol. 268, 60-67.
13. Chiu, B. C., Freeman, C. M., Stolberg, V. R., Hu, J. S., Komuniecki, E., and Chensue, S. W. (2004). The innate pulmonary granuloma: characterization and demonstration of dendritic cell recruitment and function. Am. J. Pathol. 164, 1021-1030.
14. Chiu, B. C., Stolberg, V. R., and Chensue, S. W. (2008). Mononuclear phagocyte-derived IL-10 suppresses the innate IL-12/IFN-gamma axis in lung-challenged aged mice. J. Immunol. 181, 3156-3166.
15. Chiu, B. C., Stolberg, V. R., Freeman, C. M., and Chensue, S. W. (2007). Mononuclear phagocyte-derived interleukin-10 suppresses the innate pulmonary granuloma cytokine response in aged mice. Am. J. Pathol. 171, 829-837.
16. Corbett, E. L., Watt, C. J., Walker, N., Maher, D., Williams, B. G., Raviglione, M. C., et al. (2003). The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch. Intern. Med. 163, 1009-1021.
17. Davis, J. M., and Ramakrishnan, L. (2009). The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136, 37-49.
18. Dejerine, J. (1884). Recherche du bacilli de koch dans la tuberculose calcifee. Compt. Rend. Soc. Biol. 36, 500-505.
19. de le Boe, F. (1679). Opera medica, Vol. 934. Amstelodami: Apud Danielem Elsevirium, et Abrahamum Wolfgang, 150-200.
20. de Waal Malefyt, R., Yssel, H., and De Vries, J. E. (1993). Direct effects of IL-10 on subsets of human CD4+ T cell clones and resting T cells. Specific inhibition of IL-2 production and proliferation. J. Immunol. 150, 4754-4765.
21. Dlugovitzky, D., Bay, M. L., Rateni, L., Fiorenza, G., Vietti, L., Farroni, M. A., et al. (2000). Influence of disease severity on nitrite and cytokine production by peripheral blood mononuclear cells (PBMC) from patients with pulmonary tuberculosis (TB). Clin. Exp. Immunol. 122, 343-349.
22. Doenhoff, M. J. (1997). A role for granulomatous inflammation in the transmission of infectious disease: schistosomiasis and tuberculosis. Parasitology 115(Suppl.), S113-S125.
23. Egen, J. G., Rothfuchs, A. G., Feng, C. G., Horwitz, M. A., Sher, A., and Germain, R. N. (2011). Intravital imaging reveals limited antigen presentation and T cell effector function in mycobacterial granulomas. Immunity 34, 807-819.
24. Egen, J. G., Rothfuchs, A. G., Feng, C. G., Winter, N., Sher, A., and Germain, R. N. (2008). Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity 28, 271-284.
25. Ehlers, S., Benini, J., Held, H. D., Roeck, C., Alber, G., and Uhlig, S. (2001). Alphabeta T cell receptor-positive cells and interferon-gamma, but not inducible nitric oxide synthase, are critical for granuloma necrosis in a mouse model of mycobacteria-induced pulmonary immunopathology. J. Exp. Med. 194, 1847-1859.
26. Feldman, W., and Baggenstoss, A. (1938). The residual infectivity of the primary complex of tuberculosis. Am. J. Pathol. 14, 473-490.
27. Feldman, W., and Baggenstoss, A. (1939). The occurence of virulent tubercle bacilli in presumably non-tuberculous lung tissue. Am. J. Pathol. 15, 501-515.
28. Ferrer, N. L., Gomez, A. B., Neyrolles, O., Gicquel, B., and Martin, C. (2010). Interactions of attenuated Mycobacterium tuberculosis phoP mutant with human macrophages. PLoS ONE 5:e12978. doi: 10.1371/journal.pone.0012978
29. Flynn, J. L., Capuano, S. V., Croix, D., Pawar, S., Myers, A., Zinovik, A., et al. (2003). Non-human primates: a model for tuberculosis research. Tuberculosis 83, 116-118.
30. Flynn, J. L., Scanga, C. A., Tanaka, K. E., and Chan, J. (1998). Effects of aminoguanidine on latent murine tuberculosis. J. Immunol. 160, 1796-1803.
31. Gallegos, A. M., Van Heijst, J. W., Samstein, M., Su, X., Pamer, E. G., and Glickman, M. S. (2011). A gamma interferon independent mechanism of CD4 T cell mediated control of M. tuberculosis infection in vivo. PLoS Pathog. 7:e1002052. doi: 10.1371/journal.ppat.1002052
32. Geldmacher, C., Zumla, A., and Hoelscher, M. (2012). Interaction between HIV and Mycobacterium tuberculosis: HIV-1-induced CD4 T-cell depletion and the development of active tuberculosis. Curr. Opin. HIV AIDS 7, 268-275.
33. Glynn, J. R., Murray, J., Bester, A., Nelson, G., Shearer, S., and Sonnenberg, P. (2008). Effects of duration of HIV infection and secondary tuberculosis transmission on tuberculosis incidence in the South African gold mines. AIDS 22, 1859-1867.
34. Higgins, D. M., Sanchez-Campillo, J., Rosas-Taraco, A. G., Lee, E. J., Orme, I. M., and Gonzalez-Juarrero, M. (2009). Lack of IL-10 alters inflammatory and immune responses during pulmonary Mycobacterium tuberculosis infection. Tuberculosis (Edinb) 89, 149-157.
35. Hunter, R. L. (2011). Pathology of post primary tuberculosis of the lung: an illustrated critical review. Tuberculosis 91, 497-509.
36. Hunter, R. L., Jagannath, C., and Actor, J. K. (2007). Pathology of postprimary tuberculosis in humans and mice: contradiction of long-held beliefs. Tuberculosis 87, 267-278.
37. Hunter, R. L., Olsen, M., Jagannath, C., and Actor, J. K. (2006). Trehalose 6,6'-dimycolate and lipid in the pathogenesis of caseating granulomas of tuberculosis in mice. Am. J.Pathol. 168, 1249-1261.
38. Jacobs, M., Fick, L., Allie, N., Brown, N., and Ryffel, B. (2002). Enhanced immune response in Mycobacterium bovis bacille calmette guerin (BCG)-infected IL-10-deficient mice. Clin. Chem. Lab. Med. 40, 893-902.
39. Jagannath, C., Actor, J. K., and Hunter, R. L. Jr. (1998). Induction of nitric oxide in human monocytes and monocyte cell lines by Mycobacterium tuberculosis. Nitric Oxide 2, 174-186.
40. Johnson, C. M., Cooper, A. M., Frank, A. A., and Orme, I. M. (1998). Adequate expression of protective immunity in the absence of granuloma formation in Mycobacterium tuberculosis-infected mice with a disruption in the intracellular adhesion molecule 1 gene. Infect. Immun. 66, 1666-1670.
41. Kaneko, H., Yamada, H., Mizuno, S., Udagawa, T., Kazumi, Y., Sekikawa, K., et al. (1999). Role of tumor necrosis factor-alpha in Mycobacterium-induced granuloma formation in tumor necrosis factor-alpha-deficient mice. Lab. Invest. 79, 379-386.
42. Karakousis, P. C., Yoshimatsu, T., Lamichhane, G., Woolwine, S. C., Nuermberger, E. L., Grosset, J., et al. (2004). Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J. Exp. Med. 200, 647-657.
43. Kim, M. J., Wainwright, H. C., Locketz, M., Bekker, L. G., Walther, G. B., Dittrich, C., et al. (2010). Caseation of human tuberculosis granulomas correlates with elevated host lipid metabolism. EMBO Mol. Med. 2, 258-274.
44. Ledru, E., Ledru, S., and Zoubga, A. (1999). Granuloma formation and tuberculosis transmission in HIV-infected patients. Immunol. Today 20, 336-337.
45. Lee, W. B., Kang, J. S., Yan, J. J., Lee, M. S., Jeon, B. Y., Cho, S. N., et al. (2012). Neutrophils promote Mycobacterial trehalose dimycolate-induced lung inflammation via the mincle pathway. PLoS Pathog. 8:e1002614. doi: 10.1371/journal.ppat.1002614
46. Ly, L. H., Russell, M. I., and Mcmurray, D. N. (2007). Microdissection of the cytokine milieu of pulmonary granulomas from tuberculous guinea pigs. Cell. Microbiol. 9, 1127-1136.
47. Marino, S., Myers, A., Flynn, J. L., and Kirschner, D. E. (2010). TNF and IL-10 are major factors in modulation of the phagocytic cell environment in lung and lymph node in tuberculosis: a next-generation two-compartmental model. J. Theor. Biol. 265, 586-598.
48. Mehra, S., Pahar, B., Dutta, N. K., Conerly, C. N., Philippi-Falkenstein, K., Alvarez, X., et al. (2010). Transcriptional reprogramming in nonhuman primate (rhesus macaque) tuberculosis granulomas. PLoS ONE 5:e12266. doi: 10.1371/journal.pone.0012266
49. Mogues, T., Goodrich, M. E., Ryan, L., Lacourse, R., and North, R. J. (2001). The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. J. Exp. Med. 193, 271-280.
50. O'leary, S., O'Sullivan, M. P., and Keane, J. (2011). IL-10 blocks phagosome maturation in mycobacterium tuberculosis-infected human macrophages. Am. J. Respir. Cell Mol. Biol. 45 172-180.
51. Opie, E., and Aronson, J. (1927). Tubercle bacilli in latent tuberculosis lesions and in lung tissue without tuberculous lesions. Arch. Pathol. Lab. Med. 4, 1-21.
52. Opie, E. L. (1917). The relation of apical tuberculosis of adults to the focal tuberculosis of children. J. Exp. Med. 26, 263-277.
53. Pearl, J. E., Khader, S. A., Solache, A., Gilmartin, L., Ghilardi, N., Desauvage, F., et al. (2004). IL-27 signaling compromises control of bacterial growth in mycobacteria-infected mice. J. Immunol. 173, 7490-7496.
54. Peyron, P., Vaubourgeix, J., Poquet, Y., Levillain, F., Botanch, C., Bardou, F., et al. (2008). Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog. 4:e1000204. doi: 10.1371/journal.ppat.1000204
55. Rahman, S. (2009). Compartmentalization of immune responses in human tuberculosis: few CD8+ effector T cells but elevated levels of FoxP3+ regulatory t cells in the granulomatous lesions. Am. J. Pathol. 174, 2211-2224.
56. Ramakrishnan, L. (2012). Revisiting the role of the granuloma in tuberculosis. Nat. Rev. Immunol. 12, 352-366.
57. Redente, E. F., Higgins, D. M., Dwyer-Nield, L. D., Orme, I. M., Gonzalez-Juarrero, M., and Malkinson, A. M. (2010). Differential polarization of alveolar macrophages and bone marrow-derived monocytes following chemically and pathogen-induced chronic lung inflammation. J. Leukoc. Biol. 88, 159-168.
58. Redford, P. S., Boonstra, A., Read, S., Pitt, J., Graham, C., Stavropoulos, E., et al. (2010). Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. Eur. J. Immunol. 40, 2200-2210.
59. Rhoades, E. R., Frank, A. A., and Orme, I. M. (1997). Progression of chronic pulmonary tuberculosis in mice aerogenically infected with virulent Mycobacterium tuberculosis. Tuber. Lung Dis. 78, 57-66.
60. Rich, E. A., Torres, M., Sada, E., Finegan, C. K., Hamilton, B. D., and Toossi, Z. (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.
61. Robertson, H. (1933). The persistence of tuberculous infections. Am. J. Pathol. 9, 711-718.
62. Rohde, K. H., Veiga, D. F., Caldwell, S., Balazsi, G., and Russell, D. G. (2012). Linking the transcriptional profiles and the physiological states of Mycobacterium tuberculosis during an extended intracellular infection. PLoS Pathog. 8:e1002769. doi: 10.1371/journal.ppat.1002769
63. Saunders, B. M., Frank, A. A., Orme, I. M., and Cooper, A. M. (2002). CD4 is required for the development of a protective granulomatous response to pulmonary tuberculosis. Cell. Immunol. 216, 65-72.
64. Schreiber, H. A., Harding, J. S., Hunt, O., Altamirano, C. J., Hulseberg, P. D., Stewart, D., et al. (2011). Inflammatory dendritic cells migrate in and out of transplanted chronic mycobacterial granulomas in mice. J. Clin. Invest. 121, 3902-3913.
65. Schreiber, H. A., Hulseberg, P. D., Lee, J., Prechl, J., Barta, P., Szlavik, N., et al. (2010). Dendritic cells in chronic mycobacterial granulomas restrict local anti-bacterial T cell response in a murine model. PLoS ONE 5:e11453. doi: 10.1371/journal.pone.0011453
66. Scott, H. M., and Flynn, J. L. (2002). Mycobacterium tuberculosis in chemokine receptor 2-deficient mice: influence of dose on disease progression. Infect. Immun. 70, 5946-5954.
67. Scott-Browne, J. P., Shafiani, S., Tucker-Heard, G., Ishida-Tsubota, K., Fontenot, J. D., Rudensky, A. Y., et al. (2007). Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J. Exp. Med. 204, 2159-2169.
68. Segovia-Juarez, J. L., Ganguli, S., and Kirschner, D. (2004). Identifying control mechanisms of granuloma formation during M. tuberculosis infection using an agent-based model. J. Theor. Biol. 231, 357-376.
69. Shaler, C. R., Horvath, C., Lai, R., and Xing, Z. (2012). Understanding delayed T-cell priming, lung recruitment, and airway luminal T-cell responses in host defense against pulmonary tuberculosis. Clin. Dev. Immunol. 2012, 1-13.
70. Shaler, C. R., Kugathasan, K., Mccormick, S., Damjanovic, D., Horvath, C., Small, C. L., et al. (2011). Pulmonary mycobacterial granuloma increased IL-10 production contributes to establishing a symbiotic host-microbe microenvironment. Am. J. Pathol. 178, 1622-1634.
71. Taylor, J. L., Hattle, J. M., Dreitz, S. A., Troudt, J. M., Izzo, L. S., Basaraba, R. J., et al. (2006). Role for matrix metalloproteinase 9 in granuloma formation during pulmonary Mycobacterium tuberculosis infection. Infect. Immun. 74, 6135-6144.
72. Tsai, M. C., Chakravarty, S., Zhu, G., Xu, J., Tanaka, K., Koch, C., et al. (2006). Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cell. Microbiol. 8, 218-232.
73. Turner, O. C., Basaraba, R. J., and Orme, I. M. (2003). Immunopathogenesis of pulmonary granulomas in the guinea pig after infection with Mycobacterium tuberculosis. Infect. Immun. 71, 864-871.
74. Via, L. E., Lin, P. L., Ray, S. M., Carrillo, J., Allen, S. S., Eum, S. Y., et al. (2008). Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect. Immun. 76, 2333-2340.
75. Volkman, H. E., Clay, H., Beery, D., Chang, J. C. W., Sherman, D. R., and Ramakrishnan, L. (2004). Tuberculous granuloma formation is enhanced by a Mycobacterium virulence determinant. PLoS Biol. 2:e367. doi: 10.1371/journal.pbio.0020367
76. Volkman, H. E., Pozos, T. C., Zheng, J., Davis, J. M., Rawls, J. F., and Ramakrishnan, L. (2010). Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 327, 466-469.
77. Wang, C. (1916). An experimentalstudy of latent tuberculosis. Lancet 2, 417-419.
78. Welin, A., Raffetseder, J., Eklund, D., Stendahl, O., and Lerm, M. (2011). Importance of phagosomal functionality for growth restriction of Mycobacterium tuberculosis in primary human macrophages. J. Innate Immun. 3, 508-518.
79. WHO. (2012). Global Tuberculosis Report 2012. Geneva: WHO.
80. Winau, F., Weber, S., Sad, S., De Diego, J., Hoops, S. L., Breiden, B., et al. (2006). Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity 24, 105-117.
81. Yahagi, A., Umemura, M., Tamura, T., Kariyone, A., Begum, M. D., Kawakami, K., et al. (2010). Suppressed induction of mycobacterial antigen-specific Th1-type CD4+ T cells in the lung after pulmonary mycobacterial infection. Int. Immunol. 22, 307-318.
82. Yamasaki, S., Ishikawa, E., Sakuma, M., Hara, H., Ogata, K., and Saito, T. (2008). Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat. Immunol. 9, 1179-1188.