Adventures within the speckled band: Heterogeneity, angiogenesis, and balanced inflammation in the tuberculous granuloma

Immunological Reviews

Volumn 264, Issue 1, 2015, Pages 276-287

  Matty, Molly A ^a,b   Roca, Francisco J ^c   Cronan, Mark R ^a   Tobin, David M ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Bacterial disease; In vivo imaging; Inflammation; Monocytes macrophages; Tuberculosis

Indexed keywords

TUMOR NECROSIS FACTOR; AUTACOID; CYTOKINE; ICOSANOID; TUBERCULOSTATIC AGENT;

ANGIOGENESIS; ARTICLE; CELL DEATH; GENETIC REGULATION; HUMAN; HYPOXIA; INFLAMMATION; LUNG GRANULOMA; NECROPTOSIS; PRIORITY JOURNAL; TUBERCULOUS GRANULOMA; ANIMAL; ANOXIA; GENETICS; GRANULOMA; IMMUNOLOGY; METABOLISM; MYCOBACTERIUM TUBERCULOSIS; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; TUBERCULOSIS;

ANIMALS; ANOXIA; ANTITUBERCULAR AGENTS; CYTOKINES; EICOSANOIDS; GRANULOMA; HUMANS; INFLAMMATION MEDIATORS; MYCOBACTERIUM TUBERCULOSIS; NEOVASCULARIZATION, PATHOLOGIC; TUBERCULOSIS;

EID: 84923148272     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12273     Document Type: Article

References (108)

1. Russell DG. Who puts the tubercle in tuberculosis? Nat Rev Microbiol 2007;5:39-47.
2. Ramakrishnan L. Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol 2012;12:352-366.
3. Davis JM, Clay H, Lewis JL, Ghori N, Herbomel P, Ramakrishnan L. Real-time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity 2002;17:693-702.
4. Davis JM, Ramakrishnan L. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 2009;136:37-49.
5. Stinear TP, et al. Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome Res 2008;18:729-741.
6. Min KW, Ko JY, Park CK. Histopathological spectrum of cutaneous tuberculosis and non-tuberculous mycobacterial infections. J Cutan Pathol 2012;39:582-595.
7. Cosma CL, Swaim LE, Volkman H, Ramakrishnan L, Davis JM. Zebrafish and frog models of Mycobacterium marinum infection. Curr Protocols Microbiol 2006;10:10B 12.
8. Swaim LE, Connolly LE, Volkman HE, Humbert O, Born DE, Ramakrishnan L. Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infect Immun 2006;74:6108-6117.
9. Cosma CL, Humbert O, Ramakrishnan L. Superinfecting mycobacteria home to established tuberculous granulomas. Nat Immunol 2004;5:828-835.
10. Cosma CL, Humbert O, Sherman DR, Ramakrishnan L. Trafficking of superinfecting Mycobacterium organisms into established granulomas occurs in mammals and is independent of the Erp and ESX-1 mycobacterial virulence loci. J Infect Dis 2008;198:1851-1855.
11. Egen JG, Rothfuchs AG, Feng CG, Winter N, Sher A, Germain RN. Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity 2008;28:271-284.
12. 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.
13. Adams KN, et al. Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 2011;145:39-53.
14. Takaki K, Cosma CL, Troll MA, Ramakrishnan L. An in vivo platform for rapid high-throughput antitubercular drug discovery. Cell Rep 2012;2:175-184.
15. Lin PL, et al. Sterilization of granulomas is common in active and latent tuberculosis despite within-host variability in bacterial killing. Nat Med 2014;20:75-79.
16. Mattila JT, et al. Microenvironments in tuberculous granulomas are delineated by distinct populations of macrophage subsets and expression of nitric oxide synthase and arginase isoforms. J Immunol 2013;191:773-784.
17. Mayer-Barber K, Barber DL. Innate and adaptive cellular immune responses to Mycobacterium tuberculosis infection. Cold Spring Harb Perspect Med 2015; doi:10:1101/cshperspect.a018424. In press.
18. Yang CT, Cambier CJ, Davis JM, Hall CJ, Crosier PS, Ramakrishnan L. Neutrophils exert protection in the early tuberculous granuloma by oxidative killing of mycobacteria phagocytosed from infected macrophages. Cell Host Microbe 2012;12:301-312.
19. Desvignes L, Ernst JD. Interferon-gamma-responsive nonhematopoietic cells regulate the immune response to Mycobacterium tuberculosis. Immunity 2009;31:974-985.
20. Martin CJ, et al. Efferocytosis is an innate antibacterial mechanism. Cell Host Microbe 2012;12:289-300.
21. Repasy T, et al. Intracellular bacillary burden reflects a burst size for Mycobacterium tuberculosis in vivo. PLoS Pathog 2013;9:e1003190.
22. Srivastava S, Ernst JD, Desvignes L. Beyond macrophages: the diversity of mononuclear cells in tuberculosis. Immunol Rev 2014;262:179-192.
23. Wolf AJ, et al. Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J Immunol 2007;179:2509-2519.
24. Barry CE 3rd, et al. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol 2009;7:845-855.
25. Rustad TR, Sherrid AM, Minch KJ, Sherman DR. Hypoxia: a window into Mycobacterium tuberculosis latency. Cell Microbiol 2009;11:1151-1159.
26. Rittershaus ES, Baek SH, Sassetti CM. The normalcy of dormancy: common themes in microbial quiescence. Cell Host Microbe 2013;13:643-651.
27. Wayne LG, Hayes LG. An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 1996;64:2062-2069.
28. Gomez JE, McKinney JD. M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis 2004;84:29-44.
29. Kumar A, et al. Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J Biol Chem 2008;283:18032-18039.
30. Shiloh MU, Manzanillo P, Cox JS. Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection. Cell Host Microbe 2008;3:323-330.
31. Ohno H, et al. The effects of reactive nitrogen intermediates on gene expression in Mycobacterium tuberculosis. Cell Microbiol 2003;5:637-648.
32. Galagan JE, et al. The Mycobacterium tuberculosis regulatory network and hypoxia. Nature 2013;499:178-183.
33. Via LE, et al. Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 2008;76:2333-2340.
34. Wayne LG, Sramek HA. Metronidazole is bactericidal to dormant cells of Mycobacterium tuberculosis. Antimicrob Agents Chemother 1994;38:2054-2058.
35. Lin PL, et al. Metronidazole prevents reactivation of latent Mycobacterium tuberculosis infection in macaques. Proc Natl Acad Sci USA 2012;109:14188-14193.
36. Carroll MW, et al. Efficacy and safety of metronidazole for pulmonary multidrug-resistant tuberculosis. Antimicrob Agents Chemother 2013;57:3903-3909.
37. Oehlers SH, et al. Interception of host angiogenic signalling limits mycobacterial growth. Nature 2014; doi: 10.1038/nature13967 [Epub 24 November 2014].
38. Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin Oncol 2002;29:15-18.
39. Naumov GN, et al. A model of human tumor dormancy: an angiogenic switch from the nonangiogenic phenotype. J Natl Cancer Inst 2006;98:316-325.
40. Tsai MC, et al. Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cell Microbiol 2006;8:218-232.
41. Aly S, Laskay T, Mages J, Malzan A, Lang R, Ehlers S. Interferon-gamma-dependent mechanisms of mycobacteria-induced pulmonary immunopathology: the role of angiostasis and CXCR3-targeted chemokines for granuloma necrosis. J Pathol 2007;212:295-305.
42. Ulrichs T, et al. Differential organization of the local immune response in patients with active cavitary tuberculosis or with nonprogressive tuberculoma. J Infect Dis 2005;192:89-97.
43. Matsuyama W, et al. Increased serum level of vascular endothelial growth factor in pulmonary tuberculosis. Am J Respir Crit Care Med 2000;162:1120-1122.
44. Matsuyama W, et al. Expression of vascular endothelial growth factor in tuberculous meningitis. J Neurol Sci 2001;186:75-79.
45. Podar K, et al. The small-molecule VEGF receptor inhibitor pazopanib (GW786034B) targets both tumor and endothelial cells in multiple myeloma. Proc Natl Acad Sci USA 2006;103:19478-19483.
46. Fong TA, et al. SU5416 is a potent and selective inhibitor of the vascular endothelial growth factor receptor (Flk-1/KDR) that inhibits tyrosine kinase catalysis, tumor vascularization, and growth of multiple tumor types. Cancer Res 1999;59:99-106.
47. Opie EL, Aronson JD. Tubercle bacilli in latent tuberculosis lesions and in lung tissue without tuberculosis lesions. Arch Pathol Lab Med 1927;4:1-21.
48. Welsh KJ, Hunter RL, Actor JK. Trehalose 6, 6'-dimycolate-a coat to regulate tuberculosis immunopathogenesis. Tuberculosis 2013;93(Suppl):S3-S9.
49. Sakamoto K, et al. Mycobacterial trehalose dimycolate reprograms macrophage global gene expression and activates matrix metallo-proteinases. Infect Immun 2013;81:764-776.
50. Saita N, Fujiwara N, Yano I, Soejima K, Kobayashi K. Trehalose 6, 6'-dimycolate (cord factor) of Mycobacterium tuberculosis induces corneal angiogenesis in rats. Infect Immun 2000;68:5991-5997.
51. Stamm LM, et al. Mycobacterium marinum escapes from phagosomes and is propelled by actin-based motility. J Exp Med 2003;198:1361-1368.
52. Hsu T, et al. The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci USA 2003;100:12420-12425.
53. Gao LY, Guo S, McLaughlin B, Morisaki H, Engel JN, Brown EJ. A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 2004;53:1677-1693.
54. Stanley SA, Johndrow JE, Manzanillo P, Cox JS. The Type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J Immunol 2007;178:3143-3152.
55. Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS. Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 2012;11:469-480.
56. Volkman HE, Pozos TC, Zheng J, Davis JM, Rawls JF, Ramakrishnan L. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 2010;327:466-469.
57. Taylor JL, et al. Role for matrix metalloproteinase 9 in granuloma formation during pulmonary Mycobacterium tuberculosis infection. Infect Immun 2006;74:6135-6144.
58. Cambier CJ, et al. Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids. Nature 2014;505:218-222.
59. Bafica A, et al. Host control of Mycobacterium tuberculosis is regulated by 5-lipoxygenase-dependent lipoxin production. J Clin Invest 2005;115:1601-1606.
60. Serhan C, Ward P, Gilroy D. Fundamentals of Inflammation. Cambridge, UK: Cambridge University Press, 2010.
61. 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.
62. Divangahi M, et al. Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat Immunol 2009;10:899-906.
63. Tobin DM, et al. Host genotype-specific therapies can optimize the inflammatory response to mycobacterial infections. Cell 2012;148:434-446.
64. Tobin DM, et al. The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 2010;140:717-730.
65. 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.
66. Haeggstrom JZ. Leukotriene A4 hydrolase/aminopeptidase, the gatekeeper of chemotactic leukotriene B4 biosynthesis. J Biol Chem 2004;279:50639-50642.
67. Mayer-Barber KD, et al. Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk. Nature 2014;511:99-103.
68. Rook GA, Taverne J, Leveton C, Steele J. The role of gamma-interferon, vitamin D3 metabolites and tumour necrosis factor in the pathogenesis of tuberculosis. Immunology 1987;62:229-234.
69. Silva CL, Faccioli LH, Rocha GM. The role of cachectin/TNF in the pathogenesis of tuberculosis. Braz J Med Biol Res 1988;21:489-492.
70. Hoffman M, Weinberg JB. Tumor necrosis factor-alpha induces increased hydrogen peroxide production and Fc receptor expression, but not increased Ia antigen expression by peritoneal macrophages. J Leukoc Biol 1987;42:704-707.
71. Gardam MA, et al. Anti-tumour necrosis factor agents and tuberculosis risk: mechanisms of action and clinical management. Lancet Infect Dis 2003;3:148-155.
72. Gomez-Reino JJ, Carmona L, Valverde VR, Mola EM, Montero MD, Group B. Treatment of rheumatoid arthritis with tumor necrosis factor inhibitors may predispose to significant increase in tuberculosis risk: a multicenter active-surveillance report. Arthritis Rheum 2003;48:2122-2127.
73. Marino S, et al. Differences in reactivation of tuberculosis induced from anti-TNF treatments are based on bioavailability in granulomatous tissue. PLoS Comput Biol 2007;3:1909-1924.
74. Flynn JL, et al. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 1995;2:561-572.
75. Ehlers S, Benini J, Kutsch S, Endres R, Rietschel ET, Pfeffer K. Fatal granuloma necrosis without exacerbated mycobacterial growth in tumor necrosis factor receptor p55 gene-deficient mice intravenously infected with Mycobacterium avium. Infect Immun 1999;67:3571-3579.
76. Clay H, Volkman HE, Ramakrishnan L. Tumor necrosis factor signaling mediates resistance to mycobacteria by inhibiting bacterial growth and macrophage death. Immunity 2008;29:283-294.
77. MacMicking JD. Cell-autonomous effector mechanisms against Mycobacterium tuberculosis. Cold Spring Harbor Perspect Med 2014;4:pii: a018507.
78. Bekker LG, Moreira AL, Bergtold A, Freeman S, Ryffel B, Kaplan G. Immunopathologic effects of tumor necrosis factor alpha in murine mycobacterial infection are dose dependent. Infect Immun 2000;68:6954-6961.
79. Lin PL, et al. 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 2010;62:340-350.
80. Capuano SV 3rd, et al. Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection. Infect Immun 2003;71:5831-5844.
81. Driver ER, et al. Evaluation of a mouse model of necrotic granuloma formation using C3HeB/FeJ mice for testing of drugs against Mycobacterium tuberculosis. Antimicrob Agents Chemother 2012;56:3181-3195.
82. Dutta NK, Illei PB, Jain SK, Karakousis PC. Characterization of a novel necrotic granuloma model of latent tuberculosis infection and reactivation in mice. Am J Pathol 2014;184:2045-2055.
83. Rath PC, Aggarwal BB. TNF-induced signaling in apoptosis. J Clin Immunol 1999;19:350-364.
84. Wallach D, Kang TB, Kovalenko A. The extrinsic cell death pathway and the elan mortel. Cell Death Differ 2008;15:1533-1541.
85. Eimon PM, et al. Delineation of the cell-extrinsic apoptosis pathway in the zebrafish. Cell Death Differ 2006;13:1619-1630.
86. Sakata S, et al. Conserved function of caspase-8 in apoptosis during bony fish evolution. Gene 2007;396:134-148.
87. Srinivasan L, Ahlbrand S, Briken V. Interaction of Mycobacterium tuberculosis with host cell death pathways. Cold Spring Harbor Perspect Med 2014;4:pii: a022459.
88. Aguilo JI, et al. ESX-1-induced apoptosis is involved in cell-to-cell spread of Mycobacterium tuberculosis. Cell Microbiol 2013;15:1994-2005.
89. 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.
90. Keane J, Remold HG, Kornfeld H. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 2000;164:2016-2020.
91. Velmurugan K, et al. Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog 2007;3:e110.
92. Rodrigues MF, et al. Tumour necrosis factor receptors and apoptosis of alveolar macrophages during early infection with attenuated and virulent Mycobacterium bovis. Immunology 2013;139:503-512.
93. Keane J, et al. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun 1997;65:298-304.
94. Hinchey J, et al. Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis. J Clin Invest 2007;117:2279-2288.
95. 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.
96. Tobin DM, Ramakrishnan L. TB: the Yin and Yang of lipid mediators. Curr Opin Pharmacol 2013;13:641-645.
97. Tobin DM, Roca FJ, Ray JP, Ko DC, Ramakrishnan L. An enzyme that inactivates the inflammatory mediator leukotriene b4 restricts mycobacterial infection. PLoS ONE 2013;8:e67828.
98. Thwaites GE, et al. Dexamethasone for the treatment of tuberculous meningitis in adolescents and adults. N Engl J Med 2004;351:1741-1751.
99. Yang J, Chen J, Yue J, Liu L, Han M, Wang H. Relationship between human LTA4H polymorphisms and extra-pulmonary tuberculosis in an ethnic Han Chinese population in Eastern China. Tuberculosis 2014;94:657-663.
100. Roca FJ, Ramakrishnan L. TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 2013;153:521-534.
101. Cho YS, et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009;137:1112-1123.
102. He S, et al. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 2009;137:1100-1111.
103. Holler N, et al. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 2000;1:489-495.
104. Vandenabeele P, Declercq W, Van Herreweghe F, Vanden Berghe T. The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Sci Signal 2010;3:re4.
105. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 2010;11:700-714.
106. Baines CP, et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005;434:658-662.
107. Elojeimy S, et al. New insights on the use of desipramine as an inhibitor for acid ceramidase. FEBS Lett 2006;580:4751-4756.
108. Quarato G, et al. The cyclophilin inhibitor alisporivir prevents hepatitis C virus-mediated mitochondrial dysfunction. Hepatology 2012;55:1333-1343.