Protection and pathology in TB: learning from the zebrafish model

Seminars in Immunopathology

Volumn 38, Issue 2, 2016, Pages 261-273

  Meijer, Annemarie H ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Autophagy; Granuloma; Inflammation; Innate immunity; Mycobacterium marinum; Tuberculosis

Indexed keywords

CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CXCR3; CXCL11 CHEMOKINE; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR;

ADAPTIVE IMMUNITY; ADULT ANIMAL; ANIMAL EMBRYO; AUTOPHAGY; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; CELL DEATH; DISEASE COURSE; GRANULOMA; HINDBRAIN VENTRICLE INFECTION; HUMAN; IMMUNOPATHOGENESIS; INNATE IMMUNITY; INTRAVENOUS INFECTION; INVESTIGATIVE PROCEDURES; LARVA; MACROPHAGE FUNCTION; MICROINJECTION; MYCOBACTERIUM MARINUM; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHIL; NONHUMAN; NOTOCHORD INFECTION; OTIC VESICLE INFECTION; PHAGOCYTE; PRIORITY JOURNAL; REVIEW; SUBCUTANEOUS INFECTION; TAIL FIN INFECTION; TRUNK INFECTION; TUBERCULOSIS; TYPE VII SECRETION SYSTEM; YOLK INFECTION; ZEBRA FISH; ANIMAL; DISEASE MODEL; IMMUNOLOGY; MACROPHAGE; METABOLISM; MICROBIOLOGY; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY;

ANIMALS; AUTOPHAGY; DISEASE MODELS, ANIMAL; GRANULOMA; HUMANS; MACROPHAGES; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHILS; TOLL-LIKE RECEPTORS; TUBERCULOSIS; ZEBRAFISH;

EID: 84959495927     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-015-0522-4     Document Type: Review

References (139)

1. Russell DG (2011) Mycobacterium tuberculosis and the intimate discourse of a chronic infection. Immunol Rev 240:252–268. doi:10.1111/j.1600-065X.2010.00984.x
2. Ramakrishnan L (2012) Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol 12:352–366. doi:10.1038/nri3211
3. Dutta NK, Karakousis PC (2014) Latent tuberculosis infection: myths, models, and molecular mechanisms. Microbiol Mol Biol Rev 78:343. doi:10.1128/MMBR.00010-14
4. Russell DG (2006) Who puts the tubercle in tuberculosis? Nat Rev Microbiol 5:39–47. doi:10.1038/nrmicro1538
5. Hawn TR, Matheson AI, Maley SN, Vandal O (2013) Host-directed therapeutics for tuberculosis: can we harness the host? Microbiol Mol Biol Rev 77:608–627. doi:10.1128/MMBR.00032-13
6. O’Toole R (2010) Experimental models used to study human tuberculosis. In: Elsevier, pp 75–89
7. Peña JC, Ho W (2014) Monkey models of tuberculosis: lessons learned. Infect Immun 83:852–862. doi:10.1128/IAI.02850-14
8. Ramakrishnan L (2014) The zebrafish guide to tuberculosis immunity and treatment. Cold Spring Harb Symp Quant Biol. doi:10.1101/sqb.2013.78.023283
9. Cronan MR, Tobin DM (2014) Fit for consumption: zebrafish as a model for tuberculosis. Dis Model Mech 7:777–784. doi:10.1242/dmm.016089
10. Matty MA, Roca FJ, Cronan MR, Tobin DM (2015) Adventures within the speckled band: heterogeneity, angiogenesis, and balanced inflammation in the tuberculous granuloma. Immunol Rev 264:276–287. doi:10.1111/imr.12273
11. Stinear TP, Seemann T, Harrison PF et al (2008) Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome Res 18:729–741. doi:10.1101/gr.075069.107
12. Johnson MG, Stout JE (2015) Twenty-eight cases of Mycobacterium marinum infection: retrospective case series and literature review. Infection 1–8. doi:10.1007/s15010-015-0776-8
13. Prouty MG, Correa NE, Barker LP et al (2003) Zebrafish-Mycobacterium marinum model for mycobacterial pathogenesis. FEMS Microbiol Lett 225:177–182. doi:10.1016/S0378-1097(03)00446-4
14. van der Sar AM, Abdallah AM, Sparrius M et al (2004) Mycobacterium marinum strains can be divided into two distinct types based on genetic diversity and virulence. Infect Immun 72:6306–6312. doi:10.1128/IAI.72.11.6306-6312.2004
15. Swaim LE, Connolly LE, Volkman HE et al (2006) Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infect Immun 74:6108–6117. doi:10.1128/IAI.00887-06
16. Stamm LM, Brown EJ (2004) Mycobacterium marinum: the generalization and specialization of a pathogenic mycobacterium. Microbes Infect 6:1418–1428. doi:10.1016/j.micinf.2004.10.003
17. Tobin DM, Ramakrishnan L (2008) Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis. Cell Microbiol 10:1027–1039. doi:10.1111/j.1462-5822.2008.01133.x
18. Volkman HE, Clay H, Beery D et al (2004) Tuberculous granuloma formation is enhanced by a mycobacterium virulence determinant. PLoS Biol 2, e367. doi:10.1371/journal.pbio.0020367
19. Davis JM, Clay H, Lewis JL et al (2002) Real-time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity 17:693–702. doi:10.1016/S1074-7613(02)00475-2
20. Davis JM, Ramakrishnan L (2009) The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136:37–49. doi:10.1016/j.cell.2008.11.014
21. Cosma CL, Humbert O, Ramakrishnan L (2004) Superinfecting mycobacteria home to established tuberculous granulomas. Nat Immunol 5:828–835. doi:10.1038/ni1091
22. Cosma CL, Humbert O, Sherman DR, Ramakrishnan L (2008) 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 198:1851–1855. doi:10.1086/593175
23. Egen JG, Rothfuchs AG, Feng CG et al (2008) Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity 28:271–284. doi:10.1016/j.immuni.2007.12.010
24. Lin PL, Ford CB, Coleman MT et al (2013) Sterilization of granulomas is common in active and latent tuberculosis despite within-host variability in bacterial killing. Nat Med 20:75–79. doi:10.1038/nm.3412
25. Harriff MJ, Bermudez LE, Kent ML (2007) Experimental exposure of zebrafish, Danio rerio (Hamilton), to Mycobacterium marinum and Mycobacterium peregrinum reveals the gastrointestinal tract as the primary route of infection: a potential model for environmental mycobacterial infection. J Fish Dis 30:587–600. doi:10.1111/j.1365-2761.2007.00839.x
26. Meijer AH, Verbeek FJ, Salas-Vidal E et al (2005) Transcriptome profiling of adult zebrafish at the late stage of chronic tuberculosis due to Mycobacterium marinum infection. Mol Immunol 42:1185–1203. doi:10.1016/j.molimm.2004.11.014
27. Hegedus Z, Zakrzewska A, Agoston VC et al (2009) Deep sequencing of the zebrafish transcriptome response to mycobacterium infection. Mol Immunol 46:2918–2930. doi:10.1016/j.molimm.2009.07.002
28. van der Sar AM, Spaink HP, Zakrzewska A et al (2009) Specificity of the zebrafish host transcriptome response to acute and chronic mycobacterial infection and the role of innate and adaptive immune components. Mol Immunol 46:2317–2332. doi:10.1016/j.molimm.2009.03.024
29. Weerdenburg EM, Abdallah AM, Mitra S et al (2012) ESX-5-deficient Mycobacterium marinum is hypervirulent in adult zebrafish. Cell Microbiol 14:728–739. doi:10.1111/j.1462-5822.2012.01755.x
30. van Leeuwen LM, van der Kuip M, Youssef SA et al (2014) Modeling tuberculous meningitis in zebrafish using Mycobacterium marinum. Dis Model Mech 7:1111–1122. doi:10.1242/dmm.015453
31. Oehlers SH, Cronan MR, Scott NR et al (2014) Interception of host angiogenic signalling limits mycobacterial growth. Nature. doi:10.1038/nature13967
32. Kramnik I, Dietrich WF, Demant P, Bloom BR (2000) Genetic control of resistance to experimental infection with virulent Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 97:8560–8565. doi:10.1073/pnas.150227197
33. Reece ST, Loddenkemper C, Askew DJ et al (2010) Serine protease activity contributes to control of Mycobacterium tuberculosis in hypoxic lung granulomas in mice. J Clin Invest 120:3365–3376. doi:10.1172/JCI42796
34. Cyktor JC, Carruthers B, Kominsky RA et al (2013) IL-10 inhibits mature fibrotic granuloma formation during Mycobacterium tuberculosis infection. J Immunol 190:2778–2790. doi:10.4049/jimmunol.1202722
35. Parikka M, Hammarén MM, Harjula SE et al (2012) Mycobacterium marinum causes a latent infection that can be reactivated by gamma irradiation in adult zebrafish. PLoS Pathog 8, e1002944. doi:10.1371/journal.ppat.1002944
36. Sridevi JP, Suryadevara P, Janupally R et al (2015) Identification of potential Mycobacterium tuberculosis topoisomerase I inhibitors: a study against active, dormant and resistant tuberculosis. Eur J Pharm Sci 72:81–92. doi:10.1016/j.ejps.2015.02.017
37. Datta M, Via LE, Kamoun WS et al (2015) Anti-vascular endothelial growth factor treatment normalizes tuberculosis granuloma vasculature and improves small molecule delivery. Proc Natl Acad Sci U S A 112:1827–1832. doi:10.1073/pnas.1424563112
38. Oksanen KE, Halfpenny NJA, Sherwood E et al (2013) An adult zebrafish model for preclinical tuberculosis vaccine development. Vaccine 31:5202–5209. doi:10.1016/j.vaccine.2013.08.093
39. van der Vaart M, van Soest JJ, Spaink HP, Meijer AH (2013) Functional analysis of a zebrafish myd88 mutant identifies key transcriptional components of the innate immune system. Dis Model Mech 6:841–854. doi:10.1242/dmm.010843
40. Hammarén MM, Oksanen KE, Nisula HM et al (2014) Adequate Th2-type response associates with restricted bacterial growth in latent mycobacterial infection of zebrafish. PLoS Pathog 10, e1004190. doi:10.1371/journal.ppat.1004190
41. Ojanen MJT, Turpeinen H, Cordova ZM et al (2015) The proprotein convertase subtilisin/kexin furinA regulates zebrafish host response against Mycobacterium marinum. Infect Immun 83:1431–1442. doi:10.1128/IAI.03135-14
42. Gao L, Guo S, McLaughlin B et al (2004) A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 53:1677–1693. doi:10.1111/j.1365-2958.2004.04261.x
43. Watkins BY, Joshi SA, Ball DA et al (2012) Mycobacterium marinum SecA2 promotes stable granulomas and induces tumor necrosis factor alpha in vivo. Infect Immun 80:3512–3520. doi:10.1128/IAI.00686-12
44. Stoop EJM, Mishra AK, Driessen NN et al (2013) Mannan core branching of lipo(arabino)mannan is required for mycobacterial virulence in the context of innate immunity. Cell Microbiol 15:2093–2108. doi:10.1111/cmi.12175
45. Wang H, Dong D, Tang S et al (2013) PPE38 of Mycobacterium marinum triggers the cross-talk of multiple pathways involved in the host response, as revealed by subcellular quantitative proteomics. J Proteome Res 12:2055. doi:10.1021/pr301017e
46. Mohanty S, Jagannathan L, Ganguli G et al (2015) A mycobacterial phosphoribosyltransferase promotes bacillary survival by inhibiting oxidative stress and autophagy pathways in macrophages and zebrafish. J Biol Chem 290:13321–13343. doi:10.1074/jbc.M114.598482
47. Wang Q, Zhu L, Jones V et al (2015) CpsA, a LytR-CpsA-Psr family protein in Mycobacterium marinum, is required for cell wall integrity and virulence. Infect Immun 83:2844–2854. doi:10.1128/IAI.03081-14
48. Houben ENG, Korotkov KV, Bitter W (2013) Take five - Type VII secretion systems of mycobacteria. Biochim Biophys Acta 1843:1707–1716. doi:10.1016/j.bbamcr.2013.11.003
49. Pym AS, Brodin P, Brosch R et al (2002) Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 46:709–717. doi:10.1046/j.1365-2958.2002.03237.x
50. Kimmel CB, Ballard WW, Kimmel SR et al (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310. doi:10.1002/aja.1002030302
51. Herbomel P, Thisse B, Thisse C (1999) Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126:3735–3745
52. Le Guyader D, Redd MJ, Colucci-Guyon E et al (2007) Origins and unconventional behavior of neutrophils in developing zebrafish. Blood 111:132–141. doi:10.1182/blood-2007-06-095398
53. Stachura DL, Traver D (2011) Cellular dissection of zebrafish hematopoiesis. Methods Cell Biol 101:75–110. doi:10.1016/B978-0-12-387036-0.00004-9
54. Torraca V, Masud S, Spaink HP, Meijer AH (2014) Macrophage-pathogen interactions in infectious diseases: new therapeutic insights from the zebrafish host model. Dis Model Mech 7:785–797. doi:10.1242/dmm.015594
55. Volkman HE, Pozos TC, Zheng J et al (2010) Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 327:466–469. doi:10.1126/science.1179663
56. Roca FJ, Ramakrishnan L (2013) TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell. doi:10.1016/j.cell.2013.03.022
57. van der Vaart M, Korbee CJ, Lamers GEM et al (2014) The DNA damage-regulated autophagy modulator DRAM1 links mycobacterial recognition via TLR-MYD88 to autophagic defense. Cell Host Microbe 15:753–767. doi:10.1016/j.chom.2014.05.005
58. Tobin DM, Vary JC, Ray JP et al (2010) The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 140:717–730. doi:10.1016/j.cell.2010.02.013
59. Torraca V, Cui C, Boland R et al (2015) The CXCR3-CXCL11 signaling axis mediates macrophage recruitment and dissemination of mycobacterial infection. Dis Model Mech 8:253–269. doi:10.1242/dmm.017756
60. Schulte-Merker S, Stainier DYR (2014) Out with the old, in with the new: reassessing morpholino knockdowns in light of genome editing technology. Development 141:3103–3104. doi:10.1242/dev.112003
61. Shah AN, Davey CF, Whitebirch AC et al (2015) Rapid reverse genetic screening using CRISPR in zebrafish. Nat Methods 12:535–540. doi:10.1038/nmeth.3360
62. Ablain J, Durand EM, Yang S et al (2015) A CRISPR/Cas9 vector system for tissue-specific gene disruption in zebrafish. Dev Cell 32:756–764. doi:10.1016/j.devcel.2015.01.032
63. Carvalho R, de Sonneville J, Stockhammer OW et al (2011) A high-throughput screen for tuberculosis progression. PLoS One 6, e16779. doi:10.1371/journal.pone.0016779
64. Takaki K, Cosma CL, Troll MA, Ramakrishnan L (2012) An in vivo platform for rapid high-throughput antitubercular drug discovery. Cell Rep 2:175–184. doi:10.1016/j.celrep.2012.06.008
65. Ordas A, Raterink R, Cunningham F et al (2015) Testing tuberculosis drug efficacy in a zebrafish high-throughput translational medicine screen. Antimicrob Agents Chemother 59:753–762. doi:10.1128/AAC.03588-14
66. Benard EL, van der Sar AM, Ellett F et al (2012) Infection of zebrafish embryos with intracellular bacterial pathogens. J Vis Exp e3781. doi:10.3791/3781
67. Takaki K, Davis JM, Winglee K, Ramakrishnan L (2013) Evaluation of the pathogenesis and treatment of Mycobacterium marinum infection in zebrafish. Nat Protoc 8:1114–1124. doi:10.1038/nprot.2013.068
68. Yang C, Cambier CJ, Davis JM et al (2012) Neutrophils exert protection in the early tuberculous granuloma by oxidative killing of mycobacteria phagocytosed from infected macrophages. Cell Host Microbe 12:301–312. doi:10.1016/j.chom.2012.07.009
69. Benard EL, Roobol SJ, Spaink HP, Meijer AH (2014) Phagocytosis of mycobacteria by zebrafish macrophages is dependent on the scavenger receptor Marco, a key control factor of pro-inflammatory signalling. Dev Comp Immunol 47:223–233. doi:10.1016/j.dci.2014.07.022
70. Stoop EJM, Schipper T, Rosendahl Huber SK et al (2011) Zebrafish embryo screen for mycobacterial genes involved in the initiation of granuloma formation reveals a newly identified ESX-1 component. Dis Model Mech 4:526–536. doi:10.1242/dmm.006676
71. Fenaroli F, Westmoreland D, Benjaminsen J et al (2014) Nanoparticles as drug delivery system against tuberculosis in zebrafish embryos: direct visualization and treatment. ACS Nano 8:7014–7026. doi:10.1021/nn5019126
72. Adams KN, Takaki K, Connolly LE et al (2011) Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 145:39–53. doi:10.1016/j.cell.2011.02.022
73. Adams KN, Szumowski JD, Ramakrishnan L (2014) Verapamil, and its metabolite norverapamil, inhibit macrophage-induced, bacterial efflux pump-mediated tolerance to multiple anti-tubercular drugs. J Infect Dis 210:456–466. doi:10.1093/infdis/jiu095
74. Makarov V, Lechartier B, Zhang M et al (2014) Towards a new combination therapy for tuberculosis with next generation benzothiazinones. EMBO Mol Med 6:372–383. doi:10.1002/emmm.201303575
75. Veneman WJ, Marín-Juez R, de Sonneville J, et al (2014) Establishment and optimization of a high throughput setup to study Staphylococcus epidermidis and Mycobacterium marinum infection as a model for drug discovery. J Vis Exp e51649. doi:10.3791/51649
76. Cambier CJ, Takaki KK, Larson RP et al (2014) Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids. Nature 505:218–222. doi:10.1038/nature12799
77. Clay H, Davis JM, Beery D et al (2007) Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host Microbe 2:29–39. doi:10.1016/j.chom.2007.06.004
78. Deng Q, Sarris M, Bennin DA et al (2013) Localized bacterial infection induces systemic activation of neutrophils through Cxcr2 signaling in zebrafish. J Leukoc Biol 93:761–769. doi:10.1189/jlb.1012534
79. Alibaud L, Rombouts Y, Trivelli X et al (2011) A Mycobacterium marinum TesA mutant defective for major cell wall-associated lipids is highly attenuated in Dictyostelium discoideum and zebrafish embryos. Mol Microbiol 80:919–934. doi:10.1111/j.1365-2958.2011.07618.x
80. Nguyen-Chi M, Phan QT, Gonzalez C et al (2014) Transient infection of the zebrafish notochord with E. coli induces chronic inflammation. Dis Model Mech 7:871–882. doi:10.1242/dmm.014498
81. Eum S, Kong J, Hong M et al (2009) Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB. Chest 137:122–128. doi:10.1378/chest.09-0903
82. Lowe DM, Redford PS, Wilkinson RJ et al (2012) Neutrophils in tuberculosis: friend or foe? Trends Immunol 33:14–25. doi:10.1016/j.it.2011.10.003
83. Colucci-Guyon E, Tinevez J, Renshaw SA, Herbomel P (2011) Strategies of professional phagocytes in vivo: unlike macrophages, neutrophils engulf only surface-associated microbes. J Cell Sci 124:3053–3059. doi:10.1242/jcs.082792
84. Belon C, Gannoun-Zaki L, Lutfalla G et al (2014) Mycobacterium marinum MgtC plays a role in phagocytosis but is dispensable for intracellular multiplication. PLoS One 9, e116052. doi:10.1371/journal.pone.0116052
85. Zakrzewska A, Cui C, Stockhammer OW et al (2010) Macrophage-specific gene functions in Spi1-directed innate immunity. Blood 116:e1–e11. doi:10.1182/blood-2010-01-262873
86. Hosseini R, Lamers GE, Hodzic Z et al (2014) Correlative light and electron microscopy imaging of autophagy in a zebrafish infection model. Autophagy 10:1844–1857. doi:10.4161/auto.29992
87. Clay H, Volkman HE, Ramakrishnan L (2008) Tumor necrosis factor signaling mediates resistance to mycobacteria by inhibiting bacterial growth and macrophage death. Immunity 29:283–294. doi:10.1016/j.immuni.2008.06.011
88. Benard EL, Racz PI, Rougeot J et al (2014) Macrophage-expressed Perforins Mpeg1 and Mpeg1.2 have an anti-bacterial function in zebrafish. J Innate Immun. doi:10.1159/000366103
89. Elks PM, van der Vaart M, van Hensbergen V et al (2014) Mycobacteria counteract a TLR-mediated nitrosative defense mechanism in a zebrafish infection model. PLoS One 9, e100928. doi:10.1371/journal.pone.0100928
90. Walters KB, Green JM, Surfus JC et al (2010) Live imaging of neutrophil motility in a zebrafish model of WHIM syndrome. Blood 116:2803–2811. doi:10.1182/blood-2010-03-276972
91. Elks PM, Brizee S, van der Vaart M et al (2013) Hypoxia inducible factor signaling modulates susceptibility to mycobacterial infection via a nitric oxide dependent mechanism. PLoS Pathog 9, e1003789. doi:10.1371/journal.ppat.1003789
92. Dorhoi A, Iannaccone M, Maertzdorf J et al (2014) Reverse translation in tuberculosis: neutrophils provide clues for understanding development of active disease. Front Immunol 5:36. doi:10.3389/fimmu.2014.00036
93. Berry MPR, Graham CM, McNab FW et al (2010) An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466:973–977. doi:10.1038/nature09247
94. Verrall AJ, Netea MG, Alisjahbana B et al (2014) Early clearance of Mycobacterium tuberculosis: a new frontier in prevention. Immunology 141:506–513
95. Cambier CJ, Falkow S, Ramakrishnan L (2014) Host evasion and exploitation schemes of Mycobacterium tuberculosis. Cell 159:1497–1509. doi:10.1016/j.cell.2014.11.024
96. Arbues A, Lugo-Villarino G, Neyrolles O et al (2014) Playing hide-and-seek with host macrophages through the use of mycobacterial cell envelope phthiocerol dimycocerosates and phenolic glycolipids. Front Cell Infect Microbiol 4:173. doi:10.3389/fcimb.2014.00173
97. Serbina NV, Pamer EG (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 7:311–317. doi:10.1038/ni1309
98. Peters W, Scott HM, Chambers HF et al (2001) Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 98:7958–7963. doi:10.1073/pnas.131207398
99. Scott HM, Flynn JL (2002) Mycobacterium tuberculosis in chemokine receptor 2-deficient mice: influence of dose on disease progression. Infect Immun 70:5946–5954. doi:10.1128/IAI.70.11.5946-5954.2002
100. Serbina NV, Jia T, Hohl TM, Pamer EG (2008) Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 26:421–452. doi:10.1146/annurev.immunol.26.021607.090326
101. Sierra-Filardi E, Nieto C, Domínguez-Soto A et al (2014) CCL2 shapes macrophage polarization by GM-CSF and M-CSF: identification of CCL2/CCR2-dependent gene expression profile. J Immunol 192:3858–3867. doi:10.4049/jimmunol.1302821
102. Flores-Villanueva PO, Ruiz-Morales JA, Song C et al (2005) A functional promoter polymorphism in monocyte chemoattractant protein-1 is associated with increased susceptibility to pulmonary tuberculosis. J Exp Med 202:1649–1658. doi:10.1084/jem.20050126
103. Fuller CL, Flynn JL, Reinhart TA (2003) In situ study of abundant expression of proinflammatory chemokines and cytokines in pulmonary granulomas that develop in cynomolgus macaques experimentally infected with Mycobacterium tuberculosis. Infect Immun 71:7023–7034. doi:10.1128/IAI.71.12.7023-7034.2003
104. Lee K, Chung W, Jung Y et al (2015) CXCR3 ligands as clinical markers for pulmonary tuberculosis. Int J Tuberc Lung Dis 19:191–199. doi:10.5588/ijtld.14.0525
105. Chakravarty SD, Xu J, Lu B et al (2007) The chemokine receptor CXCR3 attenuates the control of chronic Mycobacterium tuberculosis infection in BALB/c mice. J Immunol 178:1723–1735
106. Seiler P, Aichele P, Bandermann S et al (2003) Early granuloma formation after aerosol Mycobacterium tuberculosis infection is regulated by neutrophils via CXCR3-signaling chemokines. Eur J Immunol 33:2676–2686. doi:10.1002/eji.200323956
107. Deiuliis JA, Oghumu S, Duggineni D et al (2014) CXCR3 modulates obesity-induced visceral adipose inflammation and systemic insulin resistance. Obesity (Silver Spring) 22:1264–1274. doi:10.1002/oby.20642
108. Oghumu S, Varikuti S, Terrazas C et al (2014) CXCR3 deficiency enhances tumor progression by promoting macrophage M2 polarization in a murine breast cancer model. Immunology 143:109–119. doi:10.1111/imm.12293
109. Rougeot J, Zakrzewska A, Kanwal Z et al (2014) RNA sequencing of FACS-sorted immune cell populations from zebrafish infection models to identify cell specific responses to intracellular pathogens. Methods Mol Biol 1197:261–274. doi:10.1007/978-1-4939-1261-2_15
110. Dorhoi A, Kaufmann SHE (2014) Perspectives on host adaptation in response to Mycobacterium tuberculosis: modulation of inflammation. Semin Immunol 26:533–542. doi:10.1016/j.smim.2014.10.002
111. Mayer-Barber KD, Sher A (2015) Cytokine and lipid mediator networks in tuberculosis. Immunol Rev 264:264–275. doi:10.1111/imr.12249
112. Tobin DM, Roca FJ, Oh SF et al (2012) Host genotype-specific therapies can optimize the inflammatory response to mycobacterial infections. Cell 148:434–446. doi:10.1016/j.cell.2011.12.023
113. Kanwal Z, Zakrzewska A, den Hertog J et al (2013) Deficiency in hematopoietic phosphatase ptpn6/Shp1 hyperactivates the innate immune system and impairs control of bacterial infections in zebrafish embryos. J Immunol 190:1631–1645. doi:10.4049/jimmunol.1200551
114. Tobin DM, Roca FJ, Ray JP et al (2013) An enzyme that inactivates the inflammatory mediator leukotriene B4 restricts mycobacterial infection. PLoS One 8, e67828. doi:10.1371/journal.pone.0067828
115. Mayer-Barber KD, Andrade BB, Oland SD et al (2014) Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk. Nature 511:99–103. doi:10.1038/nature13489
116. Behar SM, Divangahi M, Remold HG (2010) Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy? Nat Rev Microbiol 8:668–674. doi:10.1038/nrmicro2387
117. Chen M, Divangahi M, Gan H et al (2008) Lipid mediators in innate immunity against tuberculosis: opposing roles of PGE2 and LXA4 in the induction of macrophage death. J Exp Med 205:2791–2801. doi:10.1084/jem.20080767
118. Gutierrez MG, Master SS, Singh SB et al (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119:753–766. doi:10.1016/j.cell.2004.11.038
119. Deretic V, Saitoh T, Akira S (2013) Autophagy in infection, inflammation and immunity. Nat Rev Immunol 13:722–737. doi:10.1038/nri3532
120. Kumar D, Nath L, Kamal MA et al (2010) Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis. Cell 140:731–743. doi:10.1016/j.cell.2010.02.012
121. Sundaramurthy V, Barsacchi R, Samusik N et al (2013) Integration of chemical and RNAi multiparametric profiles identifies triggers of intracellular mycobacterial killing. Cell Host Microbe 13:129–142. doi:10.1016/j.chom.2013.01.008
122. Schiebler M, Brown K, Hegyi K et al (2014) Functional drug screening reveals anticonvulsants as enhancers of mTOR-independent autophagic killing of Mycobacterium tuberculosis through inositol depletion. EMBO Mol Med. doi:emmm.201404137/emmm.201404137
123. Stanley SA, Barczak AK, Silvis MR et al (2014) Identification of host-targeted small molecules that restrict intracellular Mycobacterium tuberculosis growth. PLoS Pathog 10, e1003946. doi:10.1371/journal.ppat.1003946
124. Watson RO, Manzanillo PS, Cox JS (2012) Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150:803–815. doi:10.1016/j.cell.2012.06.040
125. Meijer AH, van der Vaart M (2014) DRAM1 promotes the targeting of mycobacteria to selective autophagy. Autophagy 10:2389–2391. doi:10.4161/15548627.2014.984280
126. Ponpuak M, Davis AS, Roberts EA et al (2010) Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties. Immunity 32:329–341. doi:10.1016/j.immuni.2010.02.009
127. van der Wel NN, Hava D, Houben D et al (2007) M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129:1287–1298. doi:10.1016/j.cell.2007.05.059
128. Simeone R, Sayes F, Song O et al (2015) Cytosolic access of Mycobacterium tuberculosis: critical impact of phagosomal acidification control and demonstration of occurrence in vivo. PLoS Pathog 11, e1004650. doi:10.1371/journal.ppat.1004650
129. Sanjuan MA, Dillon CP, Tait SWG et al (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450:1253–1257. doi:10.1038/nature06421
130. Sanchez-Wandelmer J, Reggiori F (2013) Amphisomes: out of the autophagosome shadow? EMBO J 32:3116–3118. doi:10.1038/emboj.2013.246
131. Kim YC, Guan K (2015) mTOR: a pharmacologic target for autophagy regulation. J Clin Invest 125:25–32. doi:10.1172/JCI73939
132. Crighton D, Wilkinson S, O'Prey J et al (2006) DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126:121–134. doi:10.1016/j.cell.2006.05.034
133. Collins AC, Cai H, Li T et al (2015) Cyclic GMP-AMP synthase is an innate immune DNA sensor for mycobacterium tuberculosis. Cell Host Microbe 17:820–828. doi:10.1016/j.chom.2015.05.005
134. Wassermann R, Gulen MF, Sala C et al (2015) Mycobacterium tuberculosis differentially activates cGAS- and Inflammasome-dependent intracellular immune responses through ESX-1. Cell Host Microbe 17:799–810. doi:10.1016/j.chom.2015.05.003
135. Watson RO, Bell SL, MacDuff DA et al (2015) The cytosolic sensor cGAS detects mycobacterium tuberculosis DNA to induce type I interferons and activate autophagy. Cell Host Microbe 17:811–819. doi:10.1016/j.chom.2015.05.004
136. Netea MG (2013) Training innate immunity: the changing concept of immunological memory in innate host defence. Eur J Clin Invest 43:881–884. doi:10.1111/eci.12132
137. Netea MG, Van Crevel R (2014) BCG-induced protection: effects on innate immune memory. Semin Immunol 26:512–517. doi:10.1016/j.smim.2014.09.006
138. Buffen K, Oosting M, Quintin J et al (2014) Autophagy controls BCG-induced trained immunity and the response to intravesical BCG therapy for bladder cancer. PLoS Pathog 10, e1004485. doi:10.1371/journal.ppat.1004485
139. Tobin DM (2015) Host-directed therapies for tuberculosis. Cold Spring Harbor Perspect Med. doi:10.1101/cshperspect.a021196