The onset of adaptive immunity in the mouse model of tuberculosis and the factors that compromise its expression

Immunological Reviews

Volumn 264, Issue 1, 2015, Pages 46-59

  Robinson, Richard T ^a   Orme, Ian M ^b   Cooper, Andrea M ^c  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c TRUDEAU INSTITUTE   (United States)

Author keywords

Infectious disease; Inflammation; Lung; T cells; Vaccination

Indexed keywords

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; LUNG; LYMPHOCYTE FUNCTION; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; REGULATORY MECHANISM; T LYMPHOCYTE; TUBERCULOSIS; ANIMAL; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; LUNG TUBERCULOSIS; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHIL CHEMOTAXIS; T LYMPHOCYTE SUBPOPULATION;

BACTERIAL ANTIGEN;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, BACTERIAL; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHIL INFILTRATION; T-LYMPHOCYTE SUBSETS; TUBERCULOSIS; TUBERCULOSIS, PULMONARY;

EID: 84923118321     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12259     Document Type: Article

References (122)

1. Dye C, Glaziou P, Floyd K, Raviglione M. Prospects for tuberculosis elimination. Ann Rev Pub Health 2013;34:271-286.
2. Tameris MD, et al. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet 2013;381:1021-1028.
3. Gagneux S. Host-pathogen coevolution in human tuberculosis. Philos Trans R Soc Lond B Biol Sci 2012;367:850-859.
4. Ernst JD. The immunological life cycle of tuberculosis. Nat Rev Immunol 2012;12:581-591.
5. Blaser MJ, Kirschner D. The equilibria that allow bacterial persistence in human hosts. Nature 2007;449:843-849.
6. Hardy MA, Schmidek HH. Epidemiology of tuberculosis aboard a ship. JAMA 1968;203:175-179.
7. Comas I, et al. Human T cell epitopes of Mycobacterium tuberculosis are evolutionarily hyperconserved. Nat Gene 2010;42:498-503.
8. Cambier CJ, et al. Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids. Nature 2014;505:218-222.
9. Rao V, Fujiwara N, Porcelli S, Glickman M. Mycobacterium tuberculosis controls host innate immune activation through cyclopropane modification of a glycolipid effector molecule. J Exp Med 2005;201:535-543.
10. de Noronha A, Báfica A, Nogueira L, Barral A, Barral-Netto M. Lung granulomas from Mycobacterium tuberculosis/HIV-1 co-infected patients display decreased in situ TNF production. Pathol Res Pract 2008;204:155-161.
11. Lawn SD, Butera ST, Shinnick TM. Tuberculosis unleashed: the impact of human immunodeficiency virus infection on the host granulomatous response to Mycobacterium tuberculosis. Microbes Infect 2002;4:635-646.
12. Law KF, Jagirdar J, Weiden MD, Bodkin M, Rom WN. Tuberculosis in HIV-positive patients: cellular response and immune activation in the lung. Am J Respir Crit Care Med 1996;153:1377-1384.
13. Mayer-Barber KD, et al. Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk. Nature 2014;511:99-103.
14. Behar SM, Sassetti CM. Immunology: fixing the odds against tuberculosis. Nature 2014;511:39-40.
15. Cooper AM. Cell mediated immune responses in tuberculosis. Annu Rev Immunol 2009;27:393-422.
16. lo T cells in mycobacterial infection. Eur J Immunol 2012;42:3267-3279.
17. Geldmacher C, Zumla A, Hoelscher M. Interaction between HIV and Mycobacterium tuberculosis: HIV-1-induced CD4 T-cell depletion and the development of active tuberculosis. Curr Opin HIV AIDS 2012;7:268-274.
18. Leemans JC, et al. Depletion of alveolar macrophages exerts protective effects in pulmonary tuberculosis in Mice. J Immunol 2001;166:4604-4611.
19. Leemans JC, et al. Macrophages play a dual role during pulmonary tuberculosis in mice. J Infect Dis 2005;191:65-74.
20. Davis J, Ramakrishnan L. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 2009;136:37-49.
21. Volkman H, Pozos T, Zheng J, Davis J, Rawls J, Ramakrishnan L. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 2010;327:466-469.
22. Turner O, Basaraba R, Frank A, Orme IM. Granuloma formation in mouse and guinea pig models of experimental tuberculosis. In: Boros D ed. Granulomatous Infections and Inflammation: Cellular and Molecular Mechanisms. Washington, DC: ASM Press, 2003:65-84.
23. Appelberg R. Neutrophils and intracellular pathogens: beyond phagocytosis and killing. Trends Microbiol 2007;15:87-92.
24. Wolf AJ, et al. Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J Immunol 2007;179:2509-2519.
25. + inflammatory monocytes during Mycobacterium tuberculosis-specific T cell priming. eLife 2013;2:e01086.
26. Bhatt K, Salgame P. Host innate immune response to Mycobacterium tuberculosis. J Clin Immunol 2007;27:347-362.
27. Chen M, Gan H, Remold HG. A mechanism of virulence: virulent Mycobacterium tuberculosis strain H37Rv, but not attenuated H37Ra, causes significant mitochondrial inner membrane disruption in macrophages leading to necrosis. J Immunol 2006;176:3707-3716.
28. Flynn J, Chan J. Immunology of tuberculosis. Annu Rev Immunol 2001;19:93-129.
29. Chen M, et al. Lipid mediators in innate immunity against tuberculosis: opposing roles of PGE2 and LXA4 in the induction of macrophage death. J Exp Med 2008;205:2791-2801.
30. Divangahi M, et al. Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat Immunol 2009;10:899-906.
31. Behar SM, Divangahi M, Remold HG. Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy? Nat Rev Microbiol 2010;8:668-674.
32. Divangahi M, Desjardins D, Nunes-Alves C, Remold HG, Behar SM. Eicosanoid pathways regulate adaptive immunity to Mycobacterium tuberculosis. Nat Immunol 2010;11:751-758.
33. + T cells during Mycobacterium tuberculosis infection. J Immunol 2011;186:7110-7119.
34. Blomgran R, Desvignes L, Briken V, Ernst JD. Mycobacterium tuberculosis inhibits neutrophil apoptosis, leading to delayed activation of naive CD4 T cells. Cell Host Microbe 2012;11:81-90.
35. Khader S, et al. Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection. J Exp Med 2006;203:1805-1815.
36. Robinson R, et al. Mycobacterium tuberculosis infection induces il12rb1 splicing to generate a novel IL-12Rβ1 isoform that enhances DC migration. J Exp Med 2010;207:591-605.
37. Keeton R, et al. Soluble TNFRp75 regulates host protective immunity against Mycobacterium tuberculosis. J Clin Invest 2014;124:1537-1551.
38. Flores-Villanueva P, et al. A functional promoter polymorphism in monocyte chemoattractant protein-1 is associated with increased susceptibility to pulmonary tuberculosis. J Exp Med 2005;202:1649-1658.
39. Khader S, et al. In a murine tuberculosis model, the absence of homeostatic chemokines delays granuloma formation and protective immunity. J Immunol 2009;183:8004-8014.
40. Day TA, et al. Secondary lymphoid organs are dispensable for the development of T-cell-mediated immunity during tuberculosis. Eur J Immunol 2010;40:1663-1673.
41. Reiley W, et al. ESAT-6-specific CD4 T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in mediastinal lymph nodes. Proc Natl Acad Sci USA 2008;105:10961-10966.
42. Chackerian A, Alt J, Perera T, Dascher C, Behar S. Dissemination of Mycobacterium tuberculosis is influenced by host factors and precedes the initiation of T-cell immunity. Infect Immun 2002;70:4501-4509.
43. Wolf A, et al. Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J Exp Med 2008;205:105-115.
44. + T cells after airborne M. tuberculosis infection. J Exp Med 2008;205:2359-2368.
45. Madan-Lala R, et al. Mycobacterium tuberculosis impairs dendritic cell functions through the serine hydrolase Hip1. J Immunol 2014;192:4263-4272.
46. Naffin-Olivos JL, et al. Mycobacterium tuberculosis Hip1 modulates macrophage responses through proteolysis of GroEL2. PLoS Pathog 2014;10:e1004132.
47. Scott-Browne J, et al. Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J Exp Med 2007;204:2159-2169.
48. Shafiani S, Tucker-Heard G, Kariyone A, Takatsu K, Urdahl KB. Pathogen-specific regulatory T cells delay the arrival of effector T cells in the lung during early tuberculosis. J Exp Med 2010;207:1409-1420.
49. Brandt L, Oettinger T, Holm A, Andersen A, Andersen P. Key epitopes on the ESAT-6 antigen recognized in mice during the recall of protective immunity to Mycobacterium tuberculosis. J Immunol 1996;157:3527-3533.
50. Winslow GM, Roberts AD, Blackman MA, Woodland DL. Persistence and turnover of antigen-specific CD4 T cells during chronic tuberculosis infection in the mouse. J Immunol 2003;170:2046-2052.
51. + T cells in human tuberculosis. J Immunol 2011;186:1068-1080.
52. Commandeur S, et al. An unbiased genome-wide Mycobacterium tuberculosis gene expression approach to discover antigens targeted by human T cells expressed during pulmonary infection. J Immunol 2013;190:1659-1671.
53. Lindestam Arlehamn CS, et al. Memory T cells in latent Mycobacterium tuberculosis infection are directed against three antigenic islands and largely contained in a CXCR+CCR+ Th1 Subset. PLoS Pathog 2013;9:e1003130.
54. Gomes MS, Florido M, Pais TF, Appelberg R. Improved clearance of Mycobacterium avium upon disruption of the inducible nitric oxide synthase gene. J Immunol 1999;162:6734-6739.
55. Tsiganov EN, et al. Gr-1dimCD11b+ immature myeloid-derived suppressor cells but not neutrophils are markers of lethal tuberculosis infection in mice. J Immunol 2014;192:4718-4727.
56. Reiley WW, et al. Distinct functions of antigen-specific CD4 T cells during murine Mycobacterium tuberculosis infection. Proc Natl Acad Sci USA 2010;107:19408-19413.
57. + memory T-cell phenotype at the site of disease in extrapulmonary tuberculosis. Eur J Immunol 2012;42:147-157.
58. Geldmacher C, et al. Preferential infection and depletion of Mycobacterium tuberculosis-specific CD4 T cells after HIV-1 infection. J Exp Med 2010;207:2869-2881.
59. Barber DL, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006;439:682-687.
60. Couzin-Frankel J. Cancer Immunotherapy. Science 2013;342:1432-1433.
61. Lazar-Molnar E, et al. Programmed death-1 (PD-1)-deficient mice are extraordinarily sensitive to tuberculosis. Proc Natl Acad Sci USA 2010;107:13402-13407.
62. Barber DL, Mayer-Barber KD, Feng CG, Sharpe AH, Sher A. CD4 T cells promote rather than control tuberculosis in the absence of PD-1-mediated inhibition. J Immunol 2011;186:1598-1607.
63. Kamphorst AO, Ahmed R. Manipulating the PD-1 pathway to improve immunity. Curr Opin Immunol 2013;25:381-388.
64. Cyktor JC, Carruthers B, Stromberg P, Flaño E, Pircher H, Turner J. Killer cell lectin-like receptor G1 deficiency significantly enhances survival after Mycobacterium tuberculosis Infection. Infect Immun 2013;81:1090-1099.
65. Anderson KG, et al. Intravascular staining for discrimination of vascular and tissue leukocytes. Nat Protoc 2014;9:209-222.
66. Sakai S, et al. Cutting edge: control of Mycobacterium tuberculosis infection by a subset of lung parenchyma-homing CD4 T cells. J Immunol 2014;192:2965-2969.
67. Ulrichs T, et al. Human tuberculous granulomas induce peripheral lymphoid follicle-like structures to orchestrate local host defence in the lung. J Pathol 2004;204:217-228.
68. Kahnert A, Höpken U, Stein M, Bandermann S, Lipp M, Kaufmann S. Mycobacterium tuberculosis triggers formation of lymphoid structure in murine lungs. J Infect Dis 2007;195:46-54.
69. Khader SA, et al. IL-23 is required for long-term control of Mycobacterium tuberculosis and B cell follicle formation in the infected lung. J Immunol 2011;187:5402-5407.
70. + T helper cells mediate protective immunity against tuberculosis. J Clin Invest 2013;123:712-726.
71. Srivastava S, Ernst JD. Cutting edge: direct recognition of infected cells by CD4 T cells is required for control of intracellular Mycobacterium tuberculosis in vivo. J Immunol 2013;191:1016-1020.
72. Green AM, Difazio R, Flynn JL. IFN-gamma from CD4 T cells is essential for host survival and enhances CD8 T cell function during Mycobacterium tuberculosis infection. J Immunol 2013;190:270-277.
73. Desvignes L, Ernst JD. Interferon-γ-responsive nonhematopoietic cells regulate the immune response to Mycobacterium tuberculosis. Immunity 2009;31:974-985.
74. Nandi B, Behar SM. Regulation of neutrophils by interferon-γ limits lung inflammation during tuberculosis infection. J Exp Med 2011;208:2251-2262.
75. + T-cell function. Eur J Immunol 2013;43:2409-2420.
76. Arlehamn CL, et al. Transcriptional profile of tuberculosis antigen-specific T cells reveals novel multifunctional features. J Immunol 2014;193:2931-2940.
77. Ordway D, et al. The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J Immunol 2007;179:522-531.
78. Koch M, Tucker-Heard G, Perdue N, Killebrew J, Urdahl K, Campbell D. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat Immunol 2009;10:595-602.
79. Shafiani S, et al. Pathogen-specific Treg cells expand early during Mycobacterium tuberculosis infection but are later eliminated in response to Interleukin-12. Immunity 2013;38:1261-1270.
80. Ordway DJ, et al. Mycobacterium bovis BCG-mediated protection against W-Beijing strains of Mycobacterium tuberculosis is diminished concomitant with the emergence of regulatory T cells. Clin Vaccine Immunol 2011;18:1527-1535.
81. Egen JG, Rothfuchs AG, Feng CG, Horwitz MA, Sher A, Germain RN. Intravital imaging reveals limited antigen presentation and T cell effector function in mycobacterial granulomas. Immunity 2011;34:807-819.
82. Egen J, Rothfuchs A, Feng C, Winter N, Sher A, Germain R. Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity 2008;28:271-284.
83. + effector cells enables persistence of M. tuberculosis in vivo. PLoS Pathog 2011;7:e1002063.
84. Shi L, Jung Y, Tyagi S, Gennaro M, North R. Expression of Th1-mediated immunity in mouse lungs induces a Mycobacterium tuberculosis transcription pattern characteristic of nonreplicating persistence. Proc Natl Acad Sci USA 2003;100:241-246.
85. Pai R, Convery M, Hamilton T, Boom W, Harding C. Inhibition of IFN-gamma-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J Immunol 2003;171:175-184.
86. Fulton S, et al. Inhibition of major histocompatibility complex II expression and antigen processing in murine alveolar macrophages by Mycobacterium bovis BCG and the 19-kilodalton mycobacterial lipoprotein. Infect Immun 2004;72:2101-2110.
87. + T cell dynamic behavior and effector function in the lung. J Immunol 2014;192:1651-1660.
88. Woodworth JS, Aagaard CS, Hansen PR, Cassidy JP, Agger EM, Andersen P. Protective CD4 T cells targeting cryptic epitopes of Mycobacterium tuberculosis resist infection-driven terminal differentiation. J Immunol 2014;192:3247-3258.
89. Lindenstrom T, Knudsen NP, Agger EM, Andersen P. Control of chronic Mycobacterium tuberculosis infection by CD4 KLRG1-IL-2-secreting central memory cells. J Immunol 2013;190:6311-6319.
90. Peters W, Scott H, Chambers H, Flynn J, Charo I, Ernst J. Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis. Proc Natl Acad Sci USA 2001;98:7958-7963.
91. Scott H, Flynn J. Mycobacterium tuberculosis in chemokine receptor 2-deficient mice: influence of dose on disease progression. Infect Immun 2002;70:5946-5954.
92. Kipnis A, Basaraba R, Orme I, Cooper A. Role of chemokine CCL2 in the protective response to early murine pulmonary tuberculosis. Immunology 2003;109:547-551.
93. Peters W, et al. CCR2-dependent trafficking of F4/80dim macrophages and CD11cdim/intermediate dendritic cells is crucial for T cell recruitment to lungs infected with Mycobacterium tuberculosis. J Immunol 2004;172:7647-7653.
94. Serbina NV, Jia T, Hohl TM, Pamer EG. Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 2008;26:421-452.
95. Quinones MP, et al. CC chemokine receptor (CCR)-2 prevents arthritis development following infection by Mycobacterium avium. J Mol Med 2006;84:503-512.
96. Antonelli LR, et al. Intranasal Poly-IC treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogen-permissive monocyte/macrophage population. J Clin Invest 2010;120:1674-1682.
97. Barnes PF, et al. Predictors of short-term prognosis in patients with pulmonary tuberculosis. J Infect Dis 1988;158:366-371.
98. Berry MP, et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 2010;466:973-977.
99. Martineau A, et al. Neutrophil-mediated innate immune resistance to mycobacteria. J Clin Invest 2007;117:1988-1994.
100. Lenaerts AJ, et al. Location of persisting mycobacteria in a Guinea pig model of tuberculosis revealed by r207910. Antimicrob Agents Chemother 2007;51:3338-3345.
101. Ackart DF, et al. Expression of antimicrobial drug tolerance by attached communities of Mycobacterium tuberculosis. Pathog Dis 2014;70:359-369.
102. Keller C, Hoffmann R, Lang R, Brandau S, Hermann C, Ehlers S. Genetically determined susceptibility to tuberculosis in mice causally involves accelerated and enhanced recruitment of granulocytes. Infect Immun 2006;74:4295-4309.
103. Majorov KB, Eruslanov EB, Rubakova EI, Kondratieva TK, Apt AS. Analysis of cellular phenotypes that mediate genetic resistance to tuberculosis using a radiation bone marrow chimera approach. Infect Immun 2005;73:6174-6178.
104. Eruslanov E, et al. Neutrophil responses to Mycobacterium tuberculosis infection in genetically susceptible and resistant mice. Infect Immun 2005;73:1744-1753.
105. Mitsos L-M, et al. Genetic control of susceptibility to infection with Mycobacterium tuberculosis in mice. Genes Immunit 2000;1:467-477.
106. Dorhoi A, et al. The adaptor molecule CARD9 is essential for tuberculosis control. J Exp Med 2010;207:777-792.
107. Kolls JK, Khader SA. The role of Th17 cytokines in primary mucosal immunity. Cytokine Growth Factor Rev 2010;21:443-448.
108. Gomez MI, Prince A. Airway epithelial cell signaling in response to bacterial pathogens. Pediatr Pulmonol 2008;43:11-19.
109. Parker D, Prince A. Innate immunity in the respiratory epithelium. Am J Respir Cell Mol Biol 2011;45:189-201.
110. Nouailles G, et al. CXCL5-secreting pulmonary epithelial cells drive destructive neutrophilic inflammation in tuberculosis. J Clin Invest 2014;124.
111. Feng Y, et al. Platelets direct monocyte differentiation into epithelioid-like multinucleated giant foam cells with suppressive capacity upon mycobacterial stimulation. J Infect Dis 2014;210:1700-1710.
112. Dorhoi A, et al. Type I IFN signaling triggers immunopathology in tuberculosis-susceptible mice by modulating lung phagocyte dynamics. Eur J Immunol 2014;44:2380-2393.
113. Volpe E, et al. Gene expression profiling of human macrophages at late time of infection with Mycobacterium tuberculosis. Immunology 2006;118:449-460.
114. Marzo E, Vilaplana C, Tapia G, Diaz J, Garcia V, Cardona PJ. Damaging role of neutrophilic infiltration in a mouse model of progressive tuberculosis. Tuberculosis 2014;94:55-64.
115. Gopal R, et al. S100A8/A9 proteins mediate neutrophilic inflammation and lung pathology during tuberculosis. Am J Respir Crit Care Med 2013;188:1137-1146.
116. Ryckman C, Vandal K, Rouleau P, Talbot M, Tessier PA. Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J Immunol 2003;170:3233-3242.
117. Vogl T, et al. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 2007;13:1042-1049.
118. Boettcher S, et al. Cutting edge: LPS-induced emergency myelopoiesis depends on TLR4-expressing nonhematopoietic cells. J Immunol 2012;188:5824-5828.
119. Killick KE, Ni Cheallaigh C, O'Farrelly C, Hokamp K, MacHugh DE, Harris J. Receptor-mediated recognition of mycobacterial pathogens. Cell Microbiol 2013;15:1484-1495.
120. Dorhoi A, et al. MicroRNA-223 controls susceptibility to tuberculosis by regulating lung neutrophil recruitment. J Clin Invest 2013;123:4836-4848.
121. Spinelli SV, et al. Altered microRNA expression levels in mononuclear cells of patients with pulmonary and pleural tuberculosis and their relation with components of the immune response. Mol Immunol 2013;53:265-269.
122. Tobin DM, et al. Host genotype-specific therapies can optimize the inflammatory response to mycobacterial infections. Cell 2012;148:434-446.