Mycobacterium tuberculosis: Manipulator of protective immunity

International Journal of Molecular Sciences

Volumn 17, Issue 3, 2016, Pages

  Korb, Vanessa C ^a   Chuturgoon, Anil A ^a   Moodley, Devapregasan ^a,b  

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Foamy macrophage; Granuloma; Mycobacterium; Tuberculosis

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; TUMOR NECROSIS FACTOR ALPHA;

CELL DEATH; DENDRITIC CELL; DISEASE TRANSMISSION; GRANULOMA; HUMAN; HYPOXIA; IMMUNE EVASION; IMMUNITY; IMMUNOPATHOLOGY; LIPID METABOLISM; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; MYCOBACTERIUM TUBERCULOSIS; PHAGOSOME; PHENOTYPE; REVIEW; ANIMAL; IMMUNOLOGY; MICROBIOLOGY; PATHOGENICITY; TUBERCULOMA;

ANIMALS; HUMANS; IMMUNE EVASION; MACROPHAGES; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOMA;

EID: 84959226315     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17030131     Document Type: Review

References (99)

1. World Health Organisation (WHO). Global Tuberculosis Report 2014; World Health Organisation: Geneva, Switzerland, 2014.
2. Philips, J.A.; Ernst, J.D. Tuberculosis pathogenesis and immunity. Annu. Rev. Pathol. 2012, 7, 353-384. [CrossRef] [PubMed]
3. Dheda, K.; Booth, H.; Huggett, J.F.; Johnson, M.A.; Zumla, A.; Rook, G.A. Lung remodeling in pulmonary tuberculosis. J. Infect. Dis. 2005, 192, 1201-1210. [CrossRef] [PubMed]
4. Jo, E.K.; Yang, C.S.; Choi, C.H.; Harding, C.V. Intracellular signalling cascades regulating innate immune responses to mycobacteria: Branching out from Toll-like receptors. Cell. Microbiol. 2007, 9, 1087-1098. [CrossRef] [PubMed]
5. Russell, D.G.; Cardona, P.-J.; Kim, M.-J.; Allain, S.; Altare, F. Foamy macrophages and the progression of the human tuberculosis granuloma. Nat. Immunol. 2009, 10, 943-948. [CrossRef] [PubMed]
6. Pandey, A.K.; Sassetti, C.M. Mycobacterial persistence requires the utilization of host cholesterol. Proc. Natl. Acad. Sci. USA 2008, 105, 4376-4380. [CrossRef] [PubMed]
7. Thoma-Uszynski, S.; Stenger, S.; Takeuchi, O.; Ochoa, M.T.; Engele, M.; Sieling, P.A.; Barnes, P.F.; Röllinghoff, M.; Bölcskei, P.L.; Wagner, M., et al. Induction of direct antimicrobial activity through mammalian Toll-like receptors. Science 2001, 291, 1544-1547. [CrossRef] [PubMed]
8. Underhill, D.M.; Ozinsky, A.; Smith, K.D.; Aderem, A. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl. Acad. Sci. USA 1999, 96, 14459-14463. [CrossRef] [PubMed]
9. Means, T.K.; Wang, S.; Lien, E.; Yoshimura, A.; Golenbock, D.T.; Fenton, M.J. Human Toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J. Immunol. 1999, 163, 3920-3927. [PubMed]
10. Pecora, N.D.; Gehring, A.J.; Canaday, D.H.; Boom, W.H.; Harding, C.V. Mycobacterium tuberculosis LprA is a lipoprotein agonist of TLR-2 that regulates innate immunity and APC function. J. Immunol. 2006, 177, 422-429. [CrossRef] [PubMed]
11. Sutcliffe, I.C.; Harrington, D.J. Lipoproteins of Mycobacterium tuberculosis: An abundant and functionally diverse class of cell envelope components. FEMS Microbiol. Rev. 2004, 28, 645-659. [CrossRef] [PubMed]
12. Harding, C.V.; Boom, W.H. Regulation of antigen presentation by Mycobacterium tuberculosis: A role for Toll-like receptors. Nat. Rev. Microbiol. 2010, 8, 296-307. [CrossRef] [PubMed]
13. McBride, A.; Konowich, J.; Salgame, P. Host defense and recruitment of Foxp3+ T-regulatory cells to the lungs in chronic Mycobacterium tuberculosis infection requires Toll-like receptor 2. PLoS Pathog. 2013, 9, e1003397. [CrossRef] [PubMed]
14. Jang, S.; Uematsu, S.; Akira, S.; Salgame, P. IL-6 and IL-10 induction from dendritic cells in response to Mycobacterium tuberculosis is predominantly dependent on TLR-2-mediated recognition. J. Immunol. 2004, 173, 3392-3397. [CrossRef] [PubMed]
15. Fortune, S.M.; Solache, A.; Jaeger, A.; Hill, P.J.; Belisle, J.T.; Bloom, B.R.; Rubin, E.J.; Ernst, J.D. Mycobacterium tuberculosis inhibits macrophage responses to IFN- through myeloid differentiation factor 88-dependent and-independent mechanisms. J. Immunol. 2004, 172, 6272-6280. [CrossRef] [PubMed]
16. Gehring, A.J.; Dobos, K.M.; Belisle, J.T.; Harding, C.V.; Boom, W.H. Mycobacterium tuberculosis LprG (Rv1411c): A novel TLR-2 ligand that inhibits human macrophage class II MHC antigen processing. J. Immunol. 2004, 173, 2660-2668. [CrossRef] [PubMed]
17. Flynn, J.L.; Chan, J. What’s good for the host is good for the bug. Trends Microbiol. 2005, 13, 98-102. [CrossRef] [PubMed]
18. Ulrichs, T.; Kaufmann, S.H. New insights into the function of granulomas in human tuberculosis. J. Pathol. 2006, 208, 261-269. [CrossRef] [PubMed]
19. Russell, D.G. Who puts the tubercle in tuberculosis? Nat. Rev. Microbiol. 2007, 5, 39-47. [CrossRef] [PubMed]
20. Slight, S.R.; Khader, S.A. Chemokines shape the immune responses to tuberculosis. Cytokine Growth Factor Rev. 2013, 24, 105-113. [CrossRef] [PubMed]
21. Algood, H.M.S.; Chan, J.; Flynn, J.L. Chemokines and tuberculosis. Cytokine Growth Factor Rev. 2003, 14, 467-477. [CrossRef]
22. Gonzalez-Juarrero, M.; Orme, I.M. Characterization of murine lung dendritic cells infected with Mycobacterium tuberculosis. Infect. Immun. 2001, 69, 1127-1133. [CrossRef] [PubMed]
23. Dorhoi, A.; Reece, S.T.; Kaufmann, S.H. For better or for worse: The immune response against Mycobacterium tuberculosis balances pathology and protection. Immunol. Rev. 2011, 240, 235-251. [CrossRef] [PubMed]
24. Blomgran, R.; Ernst, J.D. Lung neutrophils facilitate activation of naive antigen-specific CD4+ T-cells during Mycobacterium tuberculosis infection. J. Immunol. 2011, 186, 7110-7119. [CrossRef] [PubMed]
25. Reece, S.T.; Kaufmann, S.H. Floating between the poles of pathology and protection: Can we pin down the granuloma in tuberculosis? Curr. Opin. Microbiol. 2012, 15, 63-70. [CrossRef] [PubMed]
26. Madan-Lala, R.; Sia, J.K.; King, R.; Adekambi, T.; Monin, L.; Khader, S.A.; Pulendran, B.; Rengarajan, J. Mycobacterium tuberculosis impairs dendritic cell functions through the serine hydrolase Hip1. J. Immunol. 2014, 192, 4263-4272. [CrossRef] [PubMed]
27. Natarajan, K.; Latchumanan, V.K.; Singh, B.; Singh, S.; Sharma, P. Down-regulation of T-helper 1 responses to mycobacterial antigens due to maturation of dendritic cells by 10-kDa Mycobacterium tuberculosis secretory antigen. J. Infect. Dis. 2003, 187, 914-928. [CrossRef] [PubMed]
28. Srivastava, V.; Manchanda, M.; Gupta, S.; Singla, R.; Behera, D.; Das, G.; Natarajan, K. Toll-like receptor 2 and DC-SIGNR1 differentially regulate suppressors of cytokine signaling 1 in dendritic cells during Mycobacterium tuberculosis infection. J. Biol. Chem. 2009, 284, 25532-25541. [CrossRef] [PubMed]
29. Corbett, E.L.; Watt, C.J.; Walker, N.; Maher, D.; Williams, B.G.; Raviglione, M.C.; Dye, C. The growing burden of tuberculosis: Global trends and interactions with the HIV epidemic. Arch. Intern. Med. 2003, 163, 1009-1021. [CrossRef] [PubMed]
30. Flynn, J.L.; Chan, J.; Triebold, K.J.; Dalton, D.K.; Stewart, T.A.; Bloom, B.R. An essential role for interferon- in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 1993, 178, 2249-2254. [CrossRef] [PubMed]
31. Green, A.M.; Difazio, R.; Flynn, J.L. IFN- 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. [CrossRef] [PubMed]
32. Cáceres, N.; Tapia, G.; Ojanguren, I.; Altare, F.; Gil, O.; Pinto, S.; Vilaplana, C.; Cardona, P.-J. Evolution of foamy macrophages in the pulmonary granulomas of experimental tuberculosis models. Tuberculosis 2009, 89, 175-182. [CrossRef] [PubMed]
33. Peyron, P.; Vaubourgeix, J.; Poquet, Y.; Levillain, F.; Botanch, C.; Bardou, F.; Daffé, M.; Emile, J.-F.; Marchou, B.; Cardona, P.-J., et al. Foamy macrophages from tuberculous patients’ granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog. 2008, 4, e1000204. [CrossRef] [PubMed]
34. Alatas, F.; Alatas, O.; Metintas, M.; Ozarslan, A.; Erginel, S.; Yildirim, H. Vascular endothelial growth factor levels in active pulmonary tuberculosis. CHEST J. 2004, 125, 2156-2159. [CrossRef]
35. Tsai, M.C.; Chakravarty, S.; Zhu, G.; Xu, J.; Tanaka, K.; Koch, C.; Tufariello, J.; Flynn, J.; Chan, J. Characterization of the tuberculous granuloma in murine and human lungs: Cellular composition and relative tissue oxygen tension. Cell. Microbiol. 2006, 8, 218-232. [CrossRef] [PubMed]
36. Robinson, M.A.; Baumgardner, J.E.; Good, V.P.; Otto, C.M. Physiological and hypoxic O2 tensions rapidly regulate no production by stimulated macrophages. Am. J. Physiol. Cell Physiol. 2008, 294, 1079-1087. [CrossRef] [PubMed]
37. Kaplan, G.; Post, F.A.; Moreira, A.L.; Wainwright, H.; Kreiswirth, B.N.; Tanverdi, M.; Mathema, B.; Ramaswamy, S.V.; Walther, G.; Steyn, L.M., et al. Mycobacterium tuberculosis growth at the cavity surface: A microenvironment with failed immunity. Infect. Immun. 2003, 71, 7099-7108. [CrossRef] [PubMed]
38. Volkman, H.E.; Pozos, T.C.; Zheng, J.; Davis, J.M.; Rawls, J.F.; Ramakrishnan, L. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 2010, 327, 466-469. [CrossRef] [PubMed]
39. Agarwal, N.; Bishai, W.R. Subversion from the sidelines. Science 2010, 327, 417-418. [CrossRef] [PubMed]
40. Rhoades, E.; Hsu, F.; Torrelles, J.; Turk, J.; Chatterjee, D.; Russell, D. Identification and macrophage-activating activity of glycolipids released from intracellular Mycobacterium bovis BCG. Mol. Microbiol. 2003, 48, 875-888. [CrossRef] [PubMed]
41. Bansal, K.; Kapoor, N.; Narayana, Y.; Puzo, G.; Gilleron, M.; Balaji, K.N. PIM2 induced COX-2 and MMP-9 expression in macrophages requires PI3K and notch1 signaling. PLoS ONE 2009, 4, e4911. [CrossRef] [PubMed]
42. Taylor, J.L.; Hattle, J.M.; Dreitz, S.A.; Troudt, J.M.; Izzo, L.S.; Basaraba, R.J.; Orme, I.M.; Matrisian, L.M.; Izzo, A.A. Role for matrix metalloproteinase 9 in granuloma formation during pulmonary Mycobacterium tuberculosis infection. Infect. Immun. 2006, 74, 6135-6144. [CrossRef] [PubMed]
43. Dao, D.; Kremer, L.; Guérardel, Y.; Molano, A.; Jacobs, W.; Porcelli, S.; Briken, V. Mycobacterium tuberculosis lipomannan induces apoptosis and interleukin-12 production in macrophages. Infect. Immun. 2004, 72, 2067-2074. [CrossRef] [PubMed]
44. Jones, B.W.; Means, T.K.; Heldwein, K.A.; Keen, M.A.; Hill, P.J.; Belisle, J.T.; Fenton, M.J. Different Toll-like receptor agonists induce distinct macrophage responses. J. Leukoc. Biol. 2001, 69, 1036-1044. [PubMed]
45. Gilleron, M.; Ronet, C.; Mempel, M.; Monsarrat, B.; Gachelin, G.; Puzo, G. Acylation state of the phosphatidylinositol mannosides from Mycobacterium bovis bacillus calmette guerin and ability to induce granuloma and recruit natural killer t-cells. J. Biol. Chem. 2001, 276, 34896-34904. [CrossRef] [PubMed]
46. Perez, R.L.; Roman, J.; Roser, S.; Little, C.; Olsen, M.; Indrigo, J.; Hunter, R.L.; Actor, J.K. Cytokine message and protein expression during lung granuloma formation and resolution induced by the mycobacterial cord factor trehalose-6,61-dimycolate. J. Interferon Cytokine Res. 2000, 20, 795-804. [CrossRef] [PubMed]
47. Russell, D.; Purdy, G.; Owens, R.; Rohde, K.; Yates, R. Mycobacterium tuberculosis and the four-minute phagosome: By arresting the maturation of phagosomes, M-tuberculosis avoids being delivered to lysosomes. ASM News 2005, 71, 459-463.
48. Deretic, V.; Singh, S.; Master, S.; Harris, J.; Roberts, E.; Kyei, G.; Davis, A.; de Haro, S.; Naylor, J.; Lee, H.H., et al. Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell. Microbiol. 2006, 8, 719-727. [CrossRef] [PubMed]
49. Vergne, I.; Chua, J.; Singh, S.B.; Deretic, V. Cell biology of Mycobacterium tuberculosis phagosome. Annu. Rev. Cell Dev. Biol. 2004, 20, 367-394. [CrossRef] [PubMed]
50. Sturgill-Koszycki, S.; Schlesinger, P.H.; Chakraborty, P.; Haddix, P.L.; Collins, H.L.; Fok, A.K.; Allen, R.D.; Gluck, S.L.; Heuser, J.; Russell, D.G. Lack of acidification in mycobacterium phagosomes produced by exclusion of the vesicular proton-atpase. Science 1994, 263, 678-681. [CrossRef] [PubMed]
51. Wong, D.; Bach, H.; Sun, J.; Hmama, Z.; Av-Gay, Y. Mycobacterium tuberculosis protein tyrosine phosphatase (PtpA) excludes host vacuolar H+-ATPase to inhibit phagosome acidification. Proc. Natl. Acad. Sci. USA 2011, 108, 19371-19376. [CrossRef] [PubMed]
52. Vergne, I.; Chua, J.; Deretic, V. Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca2+/calmodulin-PI3K hVPS34 cascade. J. Exp. Med. 2003, 198, 653-659. [CrossRef] [PubMed]
53. Fratti, R.A.; Backer, J.M.; Gruenberg, J.; Corvera, S.; Deretic, V. Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J. Cell Biol. 2001, 154, 631-644. [CrossRef] [PubMed]
54. Shukla, S.; Richardson, E.; Athman, J.; Shi, L.; Wearsch, P.; McDonald, D.; Banaei, N.; Boom, W.; Jackson, M.; Harding, C. Mycobacterium tuberculosis lipoprotein LprG binds lipoarabinomannan and determines its localization in the cell wall envelope and affects phagolysosomal fusion. PLoS Pathog. 2014, 10, e1004596.
55. Saleh, M.T.; Belisle, J.T. Secretion of an acid phosphatase (SapM) by Mycobacterium tuberculosis that is similar to eukaryotic acid phosphatases. J. Bacteriol. 2000, 182, 6850-6853. [CrossRef] [PubMed]
56. Harding, C.V.; Geuze, H.J. Class II MHC molecules are present in macrophage lysosomes and phagolysosomes that function in the phagocytic processing of Listeria monocytogenes for presentation to T-cells. J. Cell Biol. 1992, 119, 531-542. [CrossRef] [PubMed]
57. Ramachandra, L.; Noss, E.; Boom, W.H.; Harding, C.V. Processing of Mycobacterium tuberculosis antigen 85b involves intraphagosomal formation of peptide-major histocompatibility complex II complexes and is inhibited by live bacilli that decrease phagosome maturation. J. Exp. Med. 2001, 194, 1421-1432. [CrossRef] [PubMed]
58. Beatty, W.L.; Ullrich, H.-J.; Russell, D.G. Mycobacterial surface moieties are released from infected macrophages by a constitutive exocytic event. Eur. J. Cell Biol. 2001, 80, 31-40. [CrossRef] [PubMed]
59. Beatty, W.L.; Rhoades, E.R.; Ullrich, H.J.; Chatterjee, D.; Heuser, J.E.; Russell, D.G. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 2000, 1, 235-247. [CrossRef] [PubMed]
60. Beatty, W.L.; Russell, D.G. Identification of mycobacterial surface proteins released into subcellular compartments of infected macrophages. Infect. Immun. 2000, 68, 6997-7002. [CrossRef] [PubMed]
61. Prados-Rosales, R.; Baena, A.; Martinez, L.R.; Luque-Garcia, J.; Kalscheuer, R.; Veeraraghavan, U.; Camara, C.; Nosanchuk, J.D.; Besra, G.S.; Chen, B., et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR-2-dependent manner in mice. J. Clin. Investig. 2011, 121, 1471-1483. [CrossRef] [PubMed]
62. Schaible, U.E.; Winau, F.; Sieling, P.A.; Fischer, K.; Collins, H.L.; Hagens, K.; Modlin, R.L.; Brinkmann, V.; Kaufmann, S.H. Apoptosis facilitates antigen presentation to T-lymphocytes through MHC-I and CD1 in tuberculosis. Nat. Med. 2003, 9, 1039-1046. [CrossRef] [PubMed]
63. Harth, G.; Lee, B.-Y.; Wang, J.; Clemens, D.L.; Horwitz, M.A. Novel insights into the genetics, biochemistry, and immunocytochemistry of the 30-kilodalton major extracellular protein of Mycobacterium tuberculosis. Infect. Immun. 1996, 64, 3038-3047. [PubMed]
64. Lyadova, I.V.; Tsiganov, E.N.; Kapina, M.A.; Shepelkova, G.S.; Sosunov, V.V.; Radaeva, T.V.; Majorov, K.B.; Shmitova, N.S.; van den Ham, H.-J.; Ganusov, V.V., et al. In mice, tuberculosis progression is associated with intensive inflammatory response and the accumulation of GR-1dim cells in the lungs. PLoS ONE 2010, 5, e10469. [CrossRef] [PubMed]
65. Kwan, C.K.; Ernst, J.D. HIV and tuberculosis: A deadly human syndemic. Clin. Microbiol. Rev. 2011, 24, 351-376. [CrossRef] [PubMed]
66. Hunter, R.L.; Jagannath, C.; Actor, J.K. Pathology of postprimary tuberculosis in humans and mice: Contradiction of long-held beliefs. Tuberculosis 2007, 87, 267-278. [CrossRef] [PubMed]
67. Welsh, K.J.; Risin, S.A.; Actor, J.K.; Hunter, R.L. Immunopathology of postprimary tuberculosis: Increased T-regulatory cells and DEC-205-positive foamy macrophages in cavitary lesions. J. Immunol. Res. 2010, 2011, 307631. [CrossRef] [PubMed]
68. Rhoades, E.R.; Geisel, R.E.; Butcher, B.A.; McDonough, S.; Russell, D.G. Cell wall lipids from Mycobacterium bovis BCG are inflammatory when inoculated within a gel matrix: Characterization of a new model of the granulomatous response to mycobacterial components. Tuberculosis 2005, 85, 159-176. [CrossRef] [PubMed]
69. Galkina, E.; Ley, K. Immune and inflammatory mechanisms of atherosclerosis. Annu. Rev. Immunol. 2009, 27, 165-197. [CrossRef] [PubMed]
70. Baldán, Á.; Gomes, A.V.; Ping, P.; Edwards, P.A. Loss of ABCG1 results in chronic pulmonary inflammation. J. Immunol. 2008, 180, 3560-3568. [CrossRef] [PubMed]
71. D’Avila, H.; Melo, R.C.; Parreira, G.G.; Werneck-Barroso, E.; Castro-Faria-Neto, H.C.; Bozza, P.T. Mycobacterium bovis bacillus calmette-guerin induces TLR-2-mediated formation of lipid bodies: Intracellular domains for eicosanoid synthesis in vivo. J. Immunol. 2006, 176, 3087-3097. [CrossRef] [PubMed]
72. Ordway, D.; Henao-Tamayo, M.; Orme, I.M.; Gonzalez-Juarrero, M. Foamy macrophages within lung granulomas of mice infected with Mycobacterium tuberculosis express molecules characteristic of dendritic cells and anti-apoptotic markers of the TNF receptor-associated factor family. J. Immunol. 2005, 175, 3873-3881. [CrossRef] [PubMed]
73. Ríos-Barrera, V.A.; Campos-Peña, V.; Aguilar-León, D.; Lascurain, L.R.; Meraz-Ríos, M.A.; Moreno, J.; Figueroa-Granados, V.; Hernández-Pando, R. Macrophage and T-lymphocyte apoptosis during experimental pulmonary tuberculosis: Their relationship to mycobacterial virulence. Eur. J. Immunol. 2006, 36, 345-353. [CrossRef] [PubMed]
74. Hernandez-Pando, R.; Orozco, H.; Arriaga, E.; Sampieri, A.; Larriva-Sahd, J.; Madrid-Marina, V. Analysis of the local kinetics and localization of interleukin-1α, tumour necrosis factor-α and transforming growth factor-β, during the course of experimental pulmonary tuberculosis. Immunology 1997, 90, 607-617. [CrossRef] [PubMed]
75. Nabeshima, S.; Nomoto, M.; Matsuzaki, G.; Kishihara, K.; Taniguchi, H.; Yoshida, S.-I.; Nomoto, K. T-cell hyporesponsiveness induced by activated macrophages through nitric oxide production in mice infected with Mycobacterium tuberculosis. Infect. Immun. 1999, 67, 3221-3226. [PubMed]
76. Silva, A.R.; Pacheco, P.; Vieira-de-Abreu, A.; Maya-Monteiro, C.M.; D’Alegria, B.; Magalhães, K.G.; de Assis, E.F.; Bandeira-Melo, C.; Castro-Faria-Neto, H.C.; Bozza, P.T. Lipid bodies in oxidized LDL-induced foam cells are leukotriene-synthesizing organelles: A MCP-1/CCL2 regulated phenomenon. Biochim. Biophys. Acta 2009, 1791, 1066-1075. [CrossRef] [PubMed]
77. Brennan, P.J.; Nikaido, H. The envelope of mycobacteria. Annu. Rev. Biochem. 1995, 64, 29-63. [CrossRef] [PubMed]
78. Singh, V.; Jamwal, S.; Jain, R.; Verma, P.; Gokhale, R.; Rao, K.V. Mycobacterium tuberculosis-driven targeted recalibration of macrophage lipid homeostasis promotes the foamy phenotype. Cell Host Microbe 2012, 12, 669-681. [CrossRef] [PubMed]
79. Garton, N.J.; Christensen, H.; Minnikin, D.E.; Adegbola, R.A.; Barer, M.R. Intracellular lipophilic inclusions of mycobacteria in vitro and in sputum. Microbiology 2002, 148, 2951-2958. [CrossRef] [PubMed]
80. Caire-Brändli, I.; Papadopoulos, A.; Malaga, W.; Marais, D.; Canaan, S.; Thilo, L.; de Chastellier, C. Reversible lipid accumulation and associated division arrest of Mycobacterium avium in lipoprotein-induced foamy macrophages may resemble key events during latency and reactivation of tuberculosis. Infect. Immun. 2014, 82, 476-490. [CrossRef] [PubMed]
81. Daniel, J.; Maamar, H.; Deb, C.; Sirakova, T.D.; Kolattukudy, P.E. Mycobacterium tuberculosis uses host triacylglycerol to accumulate lipid droplets and acquires a dormancy-like phenotype in lipid-loaded macrophages. PLoS Pathog. 2011, 7, e1002093. [CrossRef] [PubMed]
82. Reed, M.B.; Gagneux, S.; DeRiemer, K.; Small, P.M.; Barry, C.E. The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J. Bacteriol. 2007, 189, 2583-2589. [CrossRef] [PubMed]
83. Deb, C.; Lee, C.-M.; Dubey, V.S.; Daniel, J.; Abomoelak, B.; Sirakova, T.D.; Pawar, S.; Rogers, L.; Kolattukudy, P.E. A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS ONE 2009, 4, e6077. [CrossRef] [PubMed]
84. Galagan, J.E.; Minch, K.; Peterson, M.; Lyubetskaya, A.; Azizi, E.; Sweet, L.; Gomes, A.; Rustad, T.; Dolganov, G.; Glotova, I., et al. The Mycobacterium tuberculosis regulatory network and hypoxia. Nature 2013, 499, 178-183. [CrossRef] [PubMed]
85. McKinney, J.D.; zu Bentrup, K.H.; Muñoz-Elías, E.J.; Miczak, A.; Chen, B.; Chan, W.-T.; Swenson, D.; Sacchettini, J.C.; Jacobs, W.R., Jr.; Russell, D.G. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 2000, 406, 735-738. [CrossRef] [PubMed]
86. Brennan, P. Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis 2003, 83, 91-97. [CrossRef]
87. Low, K.L.; Rao, P.S.; Shui, G.; Bendt, A.K.; Pethe, K.; Dick, T.; Wenk, M.R. Triacylglycerol utilization is required for regrowth of in vitro hypoxic non-replicating Mycobacterium bovis bacillus calmette-guerin. J. Bacteriol. 2009, 191, 5037-5043. [CrossRef] [PubMed]
88. Deb, C.; Daniel, J.; Sirakova, T.D.; Abomoelak, B.; Dubey, V.S.; Kolattukudy, P.E. A novel lipase belonging to the hormone-sensitive lipase family induced under starvation to utilize stored triacylglycerol in Mycobacterium tuberculosis. J. Biol. Chem. 2006, 281, 3866-3875. [CrossRef] [PubMed]
89. Fenhalls, G.; Stevens, L.; Moses, L.; Bezuidenhout, J.; Betts, J.C.; van Helden, P.; Lukey, P.T.; Duncan, K. In situ detection of Mycobacterium tuberculosis transcripts in human lung granulomas reveals differential gene expression in necrotic lesions. Infect. Immun. 2002, 70, 6330-6338. [CrossRef] [PubMed]
90. Yang, X.; Nesbitt, N.M.; Dubnau, E.; Smith, I.; Sampson, N.S. Cholesterol metabolism increases the metabolic pool of propionate in Mycobacterium tuberculosis. Biochemistry 2009, 48, 3819-3821. [CrossRef] [PubMed]
91. Lee, W.; VanderVen, B.C.; Fahey, R.J.; Russell, D.G. Intracellular Mycobacterium tuberculosis exploits host-derived fatty acids to limit metabolic stress. J. Biol. Chem. 2013, 288, 6788-6800. [CrossRef] [PubMed]
92. Elkington, P.T.; D’Armiento, J.M.; Friedland, J.S. Tuberculosis immunopathology: The neglected role of extracellular matrix destruction. Sci. Transl. Med. 2011, 3, 71-76. [CrossRef] [PubMed]
93. Chang, J.C.; Wysocki, A.; Tchou-Wong, K.-M.; Moskowitz, N.; Zhang, Y.; Rom, W. Effect of Mycobacterium tuberculosis and its components on macrophages and the release of matrix metalloproteinases. Thorax 1996, 51, 306-311. [CrossRef] [PubMed]
94. Elkington, P.; Nijran, K.; Patel, N.; Tezera, L.; Fryer, T.; Al-Nahhas, A.; Friedland, J.; Belton, M. Hypoxia increases matrix metalloproteinase-driven immunopathology during tuberculosis infection: Evidence from in vitro studies and patients with active pulmonary disease. Am. J. Respir. Crit. Care Med. 2013, 187, A1022.
95. Gan, H.; Lee, J.; Ren, F.; Chen, M.; Kornfeld, H.; Remold, H.G. Mycobacterium tuberculosis blocks crosslinking of annexin-1 and apoptotic envelope formation on infected macrophages to maintain virulence. Nat. Immunol. 2008, 9, 1189-1197. [CrossRef] [PubMed]
96. Behar, S.M.; Divangahi, M.; Remold, H.G. Evasion of innate immunity by Mycobacterium tuberculosis: Is death an exit strategy? Nat. Rev. Microbiol. 2010, 8, 668-674. [CrossRef] [PubMed]
97. Gil, O.; Guirado, E.; Gordillo, S.; Díaz, J.; Tapia, G.; Vilaplana, C.; Ariza, A.; Ausina, V.; Cardona, P.-J. Intragranulomatous necrosis in lungs of mice infected by aerosol with Mycobacterium tuberculosis is related to bacterial load rather than to any one cytokine or T-cell type. Microbes Infect. 2006, 8, 628-636. [CrossRef] [PubMed]
98. Divangahi, M.; Chen, M.; Gan, H.; Desjardins, D.; Hickman, T.T.; Lee, D.M.; Fortune, S.; Behar, S.M.; Remold, H.G. Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat. Immunol. 2009, 10, 899-906. [CrossRef] [PubMed]
99. Chen, M.; Divangahi, M.; Gan, H.; Shin, D.S.; Hong, S.; Lee, D.M.; Serhan, C.N.; Behar, S.M.; Remold, H.G. 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. [CrossRef] [PubMed]