The zebrafish guide to tuberculosis immunity and treatment

Cold Spring Harbor Symposia on Quantitative Biology

Volumn 78, Issue 1, 2013, Pages 179-192

  Ramakrishnan, Lalita ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC RESISTANCE; ARTICLE; CELL TYPE; CHEMOTAXIS; DISEASE MODEL; GRANULOMA; HOST PARASITE INTERACTION; IMMUNE RESPONSE; IMMUNITY; MACROPHAGE; MYCOBACTERIUM; NECROSIS; NONHUMAN; PATHOGENESIS; PHAGOCYTE; PRIORITY JOURNAL; TUBERCULOSIS; ZEBRA FISH; ANIMAL; CELL PROLIFERATION; CYTOLOGY; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; TREATMENT OUTCOME;

ANTIINFECTIVE AGENT; TUMOR NECROSIS FACTOR ALPHA;

ANIMALS; ANTI-BACTERIAL AGENTS; CELL PROLIFERATION; GRANULOMA; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; MACROPHAGES; MYCOBACTERIUM; PHAGOCYTES; TREATMENT OUTCOME; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA; ZEBRAFISH;

EID: 84904871938     PISSN: 00917451     EISSN: None     Source Type: Book Series    
DOI: 10.1101/sqb.2013.78.023283     Document Type: Article

References (81)

1. Adams DO. 1976. The granulomatous inflammatory response. A review. Am J Pathol 84: 164-192.
2. Adams KN, Takaki K, Connolly LE,Wiedenhoft H,Winglee K, Humbert O, Edelstein PH, Cosma CL, Ramakrishnan L. 2011. Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 145: 39-53.
3. 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 doi:10.1093/infdis/jiu095.
4. Aubry A, Chosidow O, Caumes E, Robert J, Cambau E. 2002. Sixty-three cases of Mycobacterium marinum infection: Clinical features, treatment, and antibiotic susceptibility of causative isolates. Arch Intern Med 162: 1746-1752.
5. Bates JH, Potts WE, Lewis M. 1965. Epidemiology of primary tuberculosis in an industrial school. N Engl J Med 272: 714-717.
6. Bedell VM, Wang Y, Campbell JM, Poshusta TL, Starker CG, Krug RG II, Tan W, Penheiter SG, Ma AC, Leung AY, et al. 2012. In vivo genome editing using a high-efficiency TALEN system. Nature 491: 114-118.
7. Behar SM, Martin CJ, Booty MG, Nishimura T, Zhao X, Gan HX, Divangahi M, Remold HG. 2011. Apoptosis is an innate defense function of macrophages against Mycobacterium tuberculosis. Mucosal Immunol 4: 279-287.
8. Bobrowitz ID. 1980. Reversible roentgenographic progression in the initial treatment of pulmonary tuberculosis. Am Rev Respir Dis 121: 735-742.
9. Bouley DM, Ghori N, Mercer KL, Falkow S, Ramakrishnan L. 2001. Dynamic nature of host-pathogen interactions in Mycobacterium marinum granulomas. Infect Immun 69: 7820-7831.
10. Camacho LR, Ensergueix D, Perez E, Gicquel B, Guilhot C. 1999. Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 34: 257-267.
11. Cambier CJ, Takaki KK, Larson RP, Hernandez RE, Tobin DM, Urdahl KB, Cosma CL, Ramakrishnan L. 2014. Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids. Nature 505: 218-222.
12. Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, Bushman FD, Collman RG. 2011. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 184: 957-963.
13. Clay H, Davis JM, Beery D, Huttenlocher A, Lyons SE, Ramakrishnan L. 2007. Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host Microbe 2: 29-39.
14. 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.
15. Comas I, Coscolla M, Luo T, Borrell S, Holt KE, Kato-Maeda M, Parkhill J, Malla B, Berg S, Thwaites G, et al. 2013. Outof-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet 45: 1176-1182.
16. Connolly LE, Edelstein PH, Ramakrishnan L. 2007.Whyis longterm therapy required to cure tuberculosis? PLoS Med 4: e120.
17. Cosma CL, Humbert O, Ramakrishnan L. 2004. Superinfecting mycobacteria home to established tuberculous granulomas. Nat Immunol 5: 828-835.
18. Cosma CL, Davis JM, Swaim LE, Volkman H, Ramakrishnan L. 2006. Zebrafish and frog models of Mycobacterium marinum infection. Curr Protoc Microbiol Chapter 10:Unit 10B.2. doi:10.1002/0471729256.mc10b02s3
19. 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.
20. Cox JS, Chen B, McNeil M, Jacobs WR Jr. 1999. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402: 79-83.
21. Critchley JA, Young F, Orton L, Garner P. 2013. Corticosteroids for prevention of mortality in people with tuberculosis: A systematic review and meta-analysis. Lancet Infect Dis 13: 223-237.
22. Davis JM, Ramakrishnan L. 2009. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136: 37-49.
23. Davis JM, Clay H, Lewis JL, Ghori N, Herbomel P, Ramakrishnan L. 2002. Real-time visualization of mycobacteriummacrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity 17: 693-702.
24. Decostere A, Hermans K, Haesebrouck F. 2004. Piscine mycobacteriosis:A literature review covering the agent and the disease it causes in fish and humans. Vet Microbiol 99: 159-166.
25. Dogru D, Kiper N, Ozcelik U, Yalcin E, Tezcan I. 2010. Tuberculosis in children with congenital immunodeficiency syndromes. Tuberk Toraks 58: 59-63.
26. Driver ER, Ryan GJ, Hoff DR, Irwin SM, Basaraba RJ, Kramnik I, Lenaerts AJ. 2012. Evaluation of a mouse model of necrotic granuloma formation using C3HeB/FeJ mice for testing of drugs against Mycobacterium tuberculosis. Antimicrob Agents Chemother 56: 3181-3195.
27. Egen JG, Rothfuchs AG, Feng CG, Winter N, Sher A, Germain RN. 2008. Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity 28: 271-284.
28. Elkington PT, Green JA, Emerson JE, Lopez-Pascua LD, Boyle JJ, O'Kane CM, Friedland JS. 2007. Synergistic up-regulation of epithelial cell matrix metalloproteinase-9 secretion in tuberculosis. Am J Respir Cell Mol Biol 37: 431-437.
29. Feng WX, Flores-Villanueva PO, Mokrousov I, Wu XR, Xiao J, Jiao WW, Sun L, Miao Q, Shen C, Shen D, et al. 2012. CCL2-2518 (A/G) polymorphisms and tuberculosis susceptibility: A meta-analysis. Int J Tuberc Lung Dis 16: 150-156.
30. Flores-Villanueva PO, Ruiz-Morales JA, Song CH, Flores LM, Jo EK, Montano M, Barnes PF, Selman M, Granados J. 2005. A functional promoter polymorphism in monocyte chemoattractant protein-1 is associated with increased susceptibility to pulmonary tuberculosis. J Exp Med 202: 1649-1658.
31. Flynn JL, Goldstein MM, Chan J, Triebold KJ, Pfeffer K, Lowenstein CJ, Schreiber R, Mak TW, Bloom BR. 1995. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2: 561-572.
32. Garcia Vidal C, Rodriguez Fernandez S, Martinez Lacasa J, Salavert M, Vidal R, Rodriguez Carballeira M, Garau J. 2005. Paradoxical response to antituberculous therapy in infliximab-treated patients with disseminated tuberculosis. Clin Infect Dis 40: 756-759.
33. Guinn KM, Hickey MJ, Mathur SK, Zakel KL, Grotzke JE, Lewinsohn DM, Smith S, Sherman DR. 2004. Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Mol Microbiol 51: 359-370.
34. Gupta S, Tyagi S, Almeida DV, Maiga MC, Ammerman NC, Bishai WR. 2013. Acceleration of tuberculosis treatment by adjunctive therapy with verapamil as an efflux inhibitor. Am J Respir Crit Care Med 188: 600-607.
35. Herbomel P, Levraud JP. 2005. Imaging early macrophage differentiation, migration, and behaviors in live zebrafish embryos. Methods Mol Med 105: 199-214.
36. Hetz CA, Hunn M, Rojas P, Torres V, Leyton L, Quest AF. 2002. Caspase-dependent initiation of apoptosis and necrosis by the Fas receptor in lymphoid cells: Onset of necrosis is associated with delayed ceramide increase. J Cell Sci 115: 4671-4683.
37. Hochreiter-Hufford A, Ravichandran KS. 2013. Clearing the dead: Apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb Perspect Biol 5: a008748.
38. Hsu T, Hingley-Wilson SM, Chen B, Chen M, Dai AZ, Morin PM, Marks CB, Padiyar J, Goulding C, Gingery M, et al. 2003. 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 100: 12420-12425.
39. Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK. 2013. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31: 227-229.
40. Iliopoulos A, Psathakis K, Aslanidis S, Skagias L, Sfikakis PP. 2006. Tuberculosis and granuloma formation in patients receiving anti-TNF therapy. Int J Tuberc Lung Dis 10: 588-590.
41. Janeway CA Jr. 1989. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54: 1-13.
42. Keane J. 2005. TNF-blocking agents and tuberculosis: New drugs illuminate an old topic. Rheumatology 44: 714-720.
43. Lee PP, Chan KW, Jiang L, Chen T, Li C, Lee TL, Mak PH, Fok SF, Yang X, Lau YL. 2008. Susceptibility to mycobacterial infections in children with X-linked chronic granulomatous disease: A review of 17 patients living in a region endemic for tuberculosis. Pediatr Infect Dis J 27: 224-230.
44. Lin PL, Myers A, Smith L, Bigbee C, Bigbee M, Fuhrman C, Grieser H, Chiosea I, Voitenek NN, Capuano SV, et al. 2010. 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 62: 340-350.
45. Lin PL, Ford CB, Coleman MT, Myers AJ, Gawande R, Ioerger T, Sacchettini J, Fortune SM, Flynn JL. 2014. Sterilization of granulomas is common in active and latent tuberculosis despite within-host variability in bacterial killing. Nat Med 20: 75-79.
46. Liu PT, Stenger S, Li H,Wenzel L, Tan BH, Krutzik SR, Ochoa MT, Schauber J, Wu K, Meinken C, et al. 2006. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311: 1770-1773.
47. Mitchison DA. 2005. The diagnosis and therapy of tuberculosis during the past 100 years. Am J Respir Crit Care Med 171: 699-706.
48. Movahedi M, Aghamohammadi A, Farhoudi A, Moin M, Pourpak Z, Gharagozlou M, Mansouri D, Babaei Jandaghi A, Shahnavaz N, Rezaei N, et al. 2003. Respiratory manifestations of chronic granulomatous disease; a clinical survey of patients from Iranian primary immunodeficiency registry. Iran J Allergy Asthma Immunol 2: 45-51.
49. Onwueme KC, Vos CJ, Zurita J, Ferreras JA, Quadri LE. 2005. The dimycocerosate ester polyketide virulence factors of mycobacteria. Prog Lipid Res 44: 259-302.
50. Parasa VR, Rahman MJ, Ngyuen Hoang AT, Svensson M, Brighenti S, Lerm M. 2013. Modeling Mycobacterium tuberculosis early granuloma formation in experimental human lung tissue. Dis Model Mech 7: 281-288.
51. Philips JA, Ernst JD. 2012. Tuberculosis pathogenesis and immunity. Annu Rev Pathol 7: 353-384.
52. Pichugin AV, Yan BS, Sloutsky A, Kobzik L, Kramnik I. 2009. Dominant role of the sst1 locus in pathogenesis of necrotizing lung granulomas during chronic tuberculosis infection and reactivation in genetically resistant hosts. Am J Pathol 174: 2190-2201.
53. Pietersen E, Ignatius E, Streicher EM, Mastrapa B, Padanilam X, Pooran A, Badri M, Lesosky M, van Helden P, Sirgel FA, et al. 2014. Long-term outcomes of patients with extensively drug-resistant tuberculosis in South Africa: A cohort study. Lancet doi:10.1016/S0140-6736(13)62675-6.
54. Pozos TC, Ramakrishnan L. 2004. New models for the study of Mycobacterium-host interactions. Curr Opin Immunol 16: 499-505.
55. Price NM, Gilman RH, Uddin J, Recavarren S, Friedland JS. 2003. Unopposed matrix metalloproteinase-9 expression in human tuberculous granuloma and the role of TNF-alphadependent monocyte networks. J Immunol 171: 5579-5586.
56. Ramakrishnan L. 1997. Images in clinical medicine. Mycobacterium marinum infection of the hand. N Engl J Med 337: 612.
57. Ramakrishnan L. 2012. Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol 12: 352-366.
58. Ramakrishnan L, Federspiel NA, Falkow S. 2000. Granulomaspecific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 288: 1436-1439.
59. Rengarajan J, Bloom BR, Rubin EJ. 2005. Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci 102: 8327-8332.
60. Rich AR. 1946. Pathogenesis of tuberculosis. Charles C. Thomas, Springfield, IL.
61. Roca FJ, Ramakrishnan L. 2013. TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 153: 521-534.
62. Rodrigues LC, Diwan VK, Wheeler JG. 1993. Protective effect of BCG against tuberculous meningitis and miliary tuberculosis:A meta-analysis. Int J Epidemiol 22: 1154-1158.
63. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, Monahan IM, Dolganov G, Efron B, Butcher PD, Nathan C, et al. 2003. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: Insights into the phagosomal environment. J Exp Med 198: 693-704.
64. Sheen P, O'Kane CM, Chaudhary K, Tovar M, Santillan C, Sosa J, Caviedes L, Gilman RH, Stamp G, Friedland JS. 2009. High MMP-9 activity characterises pleural tuberculosis correlating with granuloma formation. Eur Respir J 33: 134-141.
65. Sherman DR, Guinn KM, Hickey MJ, Mathur SK, Zakel KL, Smith S. 2004. Mycobacterium tuberculosis DRD1 is more virulent than M. bovis BCG in long-term murine infection. J Infect Dis 190: 123-126.
66. Swaim LE, Connolly LE, Volkman HE, Humbert O, Born DE, Ramakrishnan L. 2006. Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infect Immun 74: 6108-6117.
67. Szumowski JD, Adams KN, Edelstein PH, Ramakrishnan L. 2013. Antimicrobial efflux pumps and Mycobacterium tuberculosis drug tolerance: Evolutionary considerations. Curr Top Microbiol Immunol 374: 81-108.
68. 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.
69. 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.
70. Tameris MD, Hatherill M, Landry BS, Scriba TJ, Snowden MA, Lockhart S, Shea JE, McClain JB, Hussey GD, HanekomWA, et al. 2013. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: A randomised, placebo-controlled phase 2b trial. Lancet 381: 1021-1028.
71. Taylor JL, Hattle JM, Dreitz SA, Troudt JM, Izzo LS, Basaraba RJ, Orme IM, Matrisian LM, Izzo AA. 2006. Role for matrix metalloproteinase 9 in granuloma formation during pulmonary Mycobacterium tuberculosis infection. Infect Immun 74: 6135-6144.
72. Tobin DM, Ramakrishnan L. 2008. Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis. Cell Microbiol 10: 1027-1039.
73. Tobin DM, Ramakrishnan L. 2013. TB: The Yin and Yang of lipid mediators. Curr Opin Pharmacol 13: 641-645.
74. Tobin DM, Vary JC Jr, Ray JP, Walsh GS, Dunstan SJ, Bang ND, Hagge DA, Khadge S, King MC, Hawn TR, et al. 2010. The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 140: 717-730.
75. Tobin DM, Roca FJ, Oh SF, McFarland R, Vickery TW, Ray JP, Ko DC, Zou Y, Bang ND, Chau TT, et al. 2012. Host genotype- specific therapies can optimize the inflammatory response to mycobacterial infections. Cell 148: 434-446.
76. Tobin DM, Roca FJ, Ray JP, Ko DC, Ramakrishnan L. 2013. An enzyme that inactivates the inflammatory mediator leukotriene b4 restricts mycobacterial infection. PLoS One 8: e67828.
77. Volkman HE, Clay H, Beery D, Chang JC, Sherman DR, Ramakrishnan L. 2004. Tuberculous granuloma formation is enhanced by a mycobacterium virulence determinant. PLoS Biol 2: e367.
78. Volkman HE, Pozos TC, Zheng J, Davis JM, Rawls JF, Ramakrishnan L. 2010. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 327: 466-469.
79. Wakamoto Y, Dhar N, Chait R, Schneider K, Signorino-Gelo F, Leibler S, McKinney JD. 2013. Dynamic persistence of antibiotic- stressed mycobacteria. Science 339: 91-95.
80. Wells WF, Ratcliffe HL, Grumb C. 1948. On the mechanics of droplet nuclei infection; quantitative experimental air-borne tuberculosis in rabbits. Am J Hyg 47: 11-28.
81. Yang CT, Cambier CJ, Davis JM, Hall CJ, Crosier PS, Ramakrishnan L. 2012. Neutrophils exert protection in the early tuberculous granuloma by oxidative killing of mycobacteria phagocytosed from infected macrophages. Cell Host Microbe 12: 301-312.