An in vivo platform for rapid high-throughput antitubercular drug discovery

Cell Reports

Volumn 2, Issue 1, 2012, Pages 175-184

  Takaki, Kevin ^a   Cosma, Christine L ^a   Troll, Mark A ^b   Ramakrishnan, Lalita ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b Aaron Thermal Technologies   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ETHAMBUTOL; ISONIAZID; MOXIFLOXACIN; RIFAMPICIN; TUBERCULOSTATIC AGENT;

AGRICULTURE; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; DRUG TARGETING; EMBRYO; FLUORESCENCE; FLUOROMETRY; HIGH THROUGHPUT SCREENING; IN VIVO STUDY; MYCOBACTERIUM MARINUM; NONHUMAN; TOXICITY; ZEBRA FISH;

ANIMAL HUSBANDRY; ANIMALS; ANTI-BACTERIAL AGENTS; ANTITUBERCULAR AGENTS; AUTOMATION, LABORATORY; CRYOANESTHESIA; DRUG DISCOVERY; DRUG SYNERGISM; FLUOROMETRY; HIGH-THROUGHPUT SCREENING ASSAYS; LARVA; MODELS, BIOLOGICAL; REPRODUCIBILITY OF RESULTS; TIME FACTORS; ZEBRAFISH;

BACTERIA (MICROORGANISMS); DANIO RERIO; MYCOBACTERIUM; MYCOBACTERIUM MARINUM;

EID: 84864296849     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.06.008     Document Type: Article

References (68)

1. Adams K.N., Takaki K., Connolly L.E., Wiedenhoft H., Winglee K., Humbert O., Edelstein P.H., Cosma C.L., Ramakrishnan L. Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 2011, 145:39-53.
2. Agarwal N., Lamichhane G., Gupta R., Nolan S., Bishai W.R. Cyclic AMP intoxication of macrophages by a Mycobacterium tuberculosis adenylate cyclase. Nature 2009, 460:98-102.
3. Becker J.R., Robinson T.Y., Sachidanandan C., Kelly A.E., Coy S., Peterson R.T., MacRae C.A. In vivo natriuretic peptide reporter assay identifies chemical modifiers of hypertrophic cardiomyopathy signalling. Cardiovasc. Res. 2012, 93:463-470.
4. Bhatt A., Fujiwara N., Bhatt K., Gurcha S.S., Kremer L., Chen B., Chan J., Porcelli S.A., Kobayashi K., Besra G.S., Jacobs W.R. Deletion of kasB in Mycobacterium tuberculosis causes loss of acid-fastness and subclinical latent tuberculosis in immunocompetent mice. Proc. Natl. Acad. Sci. USA 2007, 104:5157-5162.
5. Brannon M.K., Davis J.M., Mathias J.R., Hall C.J., Emerson J.C., Crosier P.S., Huttenlocher A., Ramakrishnan L., Moskowitz S.M. Pseudomonas aeruginosa Type III secretion system interacts with phagocytes to modulate systemic infection of zebrafish embryos. Cell. Microbiol. 2009, 11:755-768.
6. Brodin P., Christophe T. High-content screening in infectious diseases. Curr. Opin. Chem. Biol. 2011, 15:534-539.
7. Cao Y., Semanchik N., Lee S.H., Somlo S., Barbano P.E., Coifman R., Sun Z. Chemical modifier screen identifies HDAC inhibitors as suppressors of PKD models. Proc. Natl. Acad. Sci. USA 2009, 106:21819-21824.
8. Chao C.C., Hsu P.C., Jen C.F., Chen I.H., Wang C.H., Chan H.C., Tsai P.W., Tung K.C., Wang C.H., Lan C.Y., Chuang Y.J. Zebrafish as a model host for Candida albicans infection. Infect. Immun. 2010, 78:2512-2521.
9. 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.
10. Christophe T., Jackson M., Jeon H.K., Fenistein D., Contreras-Dominguez M., Kim J., Genovesio A., Carralot J.P., Ewann F., Kim E.H., et al. High content screening identifies decaprenyl-phosphoribose 2' epimerase as a target for intracellular antimycobacterial inhibitors. PLoS Pathog. 2009, 5:e1000645.
11. Clatworthy A.E., Lee J.S., Leibman M., Kostun Z., Davidson A.J., Hung D.T. Pseudomonas aeruginosa infection of zebrafish involves both host and pathogen determinants. Infect. Immun. 2009, 77:1293-1303.
12. Clay H., Davis J.M., Beery D., Huttenlocher A., Lyons S.E., Ramakrishnan L. Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host Microbe 2007, 2:29-39.
13. Cosma C.L., Humbert O., Ramakrishnan L. Superinfecting mycobacteria home to established tuberculous granulomas. Nat. Immunol. 2004, 5:828-835.
14. Cosma C.L., Davis J.M., Swaim L.E., Volkman H., Ramakrishnan L. Zebrafish and frog models of Mycobacterium marinum infection. Current Protocols in Microbiology 2006, John Wiley and Sons, New York, pp. 10B.2.1-10B.2.33.
15. Cosma C.L., Klein K., Kim R., Beery D., Ramakrishnan L. Mycobacterium marinum Erp is a virulence determinant required for cell wall integrity and intracellular survival. Infect. Immun. 2006, 74:3125-3133.
16. Cusick M.F., Libbey J.E., Trede N.S., Eckels D.D., Fujinami R.S. Human T cell expansion and experimental autoimmune encephalomyelitis inhibited by Lenaldekar, a small molecule discovered in a zebrafish screen. J. Neuroimmunol. 2012, 244:35-44.
17. Das B.C., McCartin K., Liu T.C., Peterson R.T., Evans T. A forward chemical screen in zebrafish identifies a retinoic acid derivative with receptor specificity. PLoS ONE 2010, 5:e10004.
18. Davis J.M., Ramakrishnan L. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 2009, 136:37-49.
19. Davis J.M., Clay H., Lewis J.L., 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.
20. Donald P.R., McIlleron H. Antituberculosis drugs. Tuberculosis: A Comprehensive Clinical Reference 2009, 608-617. Saunders Elsevier, Philadelphia. H.S. Schaff, A. Zumla (Eds.).
21. Dorman S.E., Johnson J.L., Goldberg S., Muzanye G., Padayatchi N., Bozeman L., Heilig C.M., Bernardo J., Choudhri S., Grosset J.H., et al. Substitution of moxifloxacin for isoniazid during intensive phase treatment of pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 2009, 180:273-280. Tuberculosis Trials Consortium.
22. Etchin J., Kanki J.P., Look A.T. Zebrafish as a model for the study of human cancer. Methods Cell Biol. 2011, 105:309-337.
23. Gao L.Y., Laval F., Lawson E.H., Groger R.K., Woodruff A., Morisaki J.H., Cox J.S., Daffe M., Brown E.J. Requirement for kasB in Mycobacterium mycolic acid biosynthesis, cell wall impermeability and intracellular survival: implications for therapy. Mol. Microbiol. 2003, 49:1547-1563.
24. Jindani A., Doré C.J., Mitchison D.A. Bactericidal and sterilizing activities of antituberculosis drugs during the first 14 days. Am. J. Respir. Crit. Care Med. 2003, 167:1348-1354.
25. Kremer L., Douglas J.D., Baulard A.R., Morehouse C., Guy M.R., Alland D., Dover L.G., Lakey J.H., Jacobs W.R., Brennan P.J., et al. Thiolactomycin and related analogues as novel anti-mycobacterial agents targeting KasA and KasB condensing enzymes in Mycobacterium tuberculosis. J. Biol. Chem. 2000, 275:16857-16864.
26. Kuijl C., Savage N.D., Marsman M., Tuin A.W., Janssen L., Egan D.A., Ketema M., van den Nieuwendijk R., van den Eeden S.J., Geluk A., et al. Intracellular bacterial growth is controlled by a kinase network around PKB/AKT1. Nature 2007, 450:725-730.
27. Kumar D., Nath L., Kamal M.A., Varshney A., Jain A., Singh S., Rao K.V. Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis. Cell 2010, 140:731-743.
28. Laggner C., Kokel D., Setola V., Tolia A., Lin H., Irwin J.J., Keiser M.J., Cheung C.Y., Minor D.L., Roth B.L., et al. Chemical informatics and target identification in a zebrafish phenotypic screen. Nat. Chem. Biol. 2012, 8:144-146.
29. Martin C.S., Moriyama A., Zon L.I. Hematopoietic stem cells, hematopoiesis and disease: lessons from the zebrafish model. Genome Medicine 2011, 3:83.
30. McGrath P., Li C.Q. Zebrafish: a predictive model for assessing drug-induced toxicity. Drug Discov. Today 2008, 13:394-401.
31. McKinney J.D. In vivo veritas: the search for TB drug targets goes live. Nat. Med. 2000, 6:1330-1333.
32. Milan D.J., Peterson T.A., Ruskin J.N., Peterson R.T., MacRae C.A. Drugs that induce repolarization abnormalities cause bradycardia in zebrafish. Circulation 2003, 107:1355-1358.
33. Milan D.J., Kim A.M., Winterfield J.R., Jones I.L., Pfeufer A., Sanna S., Arking D.E., Amsterdam A.H., Sabeh K.M., Mably J.D., et al. Drug-sensitized zebrafish screen identifies multiple genes, including GINS3, as regulators of myocardial repolarization. Circulation 2009, 120:553-559.
34. Mione M.C., Trede N.S. The zebrafish as a model for cancer. Dis Model Mech 2010, 3:517-523.
35. Mitchison D.A., Chang K.C. Experimental models of tuberculosis: can we trust the mouse?. Am. J. Respir. Crit. Care Med. 2009, 180:201-202.
36. Moellering R.C. Discovering new antimicrobial agents. Int. J. Antimicrob. Agents 2011, 37:2-9.
37. Napier R.J., Rafi W., Cheruvu M., Powell K.R., Zaunbrecher M.A., Bornmann W., Salgame P., Shinnick T.M., Kalman D. Imatinib-sensitive tyrosine kinases regulate mycobacterial pathogenesis and represent therapeutic targets against tuberculosis. Cell Host Microbe 2011, 10:475-485.
38. Ni T.T., Rellinger E.J., Mukherjee A., Xie S., Stephens L., Thorne C.A., Kim K., Hu J., Lee E., Marnett L., et al. Discovering small molecules that promote cardiomyocyte generation by modulating Wnt signaling. Chem. Biol. 2011, 18:1658-1668.
39. Ou H., Simon J.A., Rubel E.W., Raible D.W. Screening for chemicals that affect hair cell death and survival in the zebrafish lateral line. Hear. Res. 2012, 288:58-66.
40. Payne D.J., Gwynn M.N., Holmes D.J., Pompliano D.L. Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat. Rev. Drug Discov. 2007, 6:29-40.
41. Peterson R.T., Fishman M.C. Discovery and use of small molecules for probing biological processes in zebrafish. Methods Cell Biol. 2004, 76:569-591.
42. Peterson R.T., Macrae C.A. Systematic approaches to toxicology in the zebrafish. Annu. Rev. Pharmacol. Toxicol. 2012, 52:433-453.
43. Pethe K., Sequeira P.C., Agarwalla S., Rhee K., Kuhen K., Phong W.Y., Patel V., Beer D., Walker J.R., Duraiswamy J., et al. A chemical genetic screen in Mycobacterium tuberculosis identifies carbon-source-dependent growth inhibitors devoid of in vivo efficacy. Nat Commun 2010, 1:57.
44. Prajsnar T.K., Cunliffe V.T., Foster S.J., Renshaw S.A. A novel vertebrate model of Staphylococcus aureus infection reveals phagocyte-dependent resistance of zebrafish to non-host specialized pathogens. Cell. Microbiol. 2008, 10:2312-2325.
45. Pratt W., Fekety R. The antimicrobial drugs 1986, Oxford University Press, New York.
46. Ramakrishnan L., Federspiel N.A., Falkow S. Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 2000, 288:1436-1439.
47. Rudner L.A., Brown K.H., Dobrinski K.P., Bradley D.F., Garcia M.I., Smith A.C., Downie J.M., Meeker N.D., Look A.T., Downing J.R., et al. Shared acquired genomic changes in zebrafish and human T-ALL. Oncogene 2011, 30:4289-4296.
48. Schwegmann A., Brombacher F. Host-directed drug targeting of factors hijacked by pathogens. Sci. Signal. 2008, 1:re8.
49. Shcherbo D., Murphy C.S., Ermakova G.V., Solovieva E.A., Chepurnykh T.V., Shcheglov A.S., Verkhusha V.V., Pletnev V.Z., Hazelwood K.L., Roche P.M., et al. Far-red fluorescent tags for protein imaging in living tissues. Biochem. J. 2009, 418:567-574.
50. Stern H.M., Murphey R.D., Shepard J.L., Amatruda J.F., Straub C.T., Pfaff K.L., Weber G., Tallarico J.A., King R.W., Zon L.I. Small molecules that delay S phase suppress a zebrafish bmyb mutant. Nat. Chem. Biol. 2005, 1:366-370.
51. Stover C.K., Warrener P., VanDevanter D.R., Sherman D.R., Arain T.M., Langhorne M.H., Anderson S.W., Towell J.A., Yuan Y., McMurray D.N., et al. A small-molecule nitroimidazopyran drug candidate for the treatment of tuberculosis. Nature 2000, 405:962-966.
52. Szabady R.L., Lokuta M.A., Walters K.B., Huttenlocher A., Welch R.A. Modulation of neutrophil function by a secreted mucinase of Escherichia coli O157:H7. PLoS Pathog. 2009, 5:e1000320.
53. Tan J.L., Zon L.I. Chemical screening in zebrafish for novel biological and therapeutic discovery. Methods Cell Biol. 2011, 105:493-516.
54. Tobin D.M., Ramakrishnan L. Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis. Cell. Microbiol. 2008, 10:1027-1039.
55. Tobin D.M., Vary J.C., Ray J.P., Walsh G.S., Dunstan S.J., Bang N.D., Hagge D.A., Khadge S., King M.C., Hawn T.R., et al. The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 2010, 140:717-730.
56. Tobin D.M., Roca F.J., Oh S.F., McFarland R., Vickery T.W., Ray J.P., Ko D.C., Zou Y., Bang N.D., Chau T.T., et al. Host genotype-specific therapies can optimize the inflammatory response to mycobacterial infections. Cell 2012, 148:434-446.
57. Traver D., Herbomel P., Patton E.E., Murphey R.D., Yoder J.A., Litman G.W., Catic A., Amemiya C.T., Zon L.I., Trede N.S. The zebrafish as a model organism to study development of the immune system. Adv. Immunol. 2003, 81:253-330.
58. Trede N.S., Langenau D.M., Traver D., Look A.T., Zon L.I. The use of zebrafish to understand immunity. Immunity 2004, 20:367-379.
59. Tweedy B.L., Lesney M.S. 1950s: Prescriptions and Polio. The Pharmaceutical Century 2000, American Chemical Society, Washington, DC.
60. Udwadia Z.F., Amale R.A., Ajbani K.K., Rodrigues C. Totally drug-resistant tuberculosis in India. Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America 2012, 54:579-581.
61. Valdivia R.H., Cirillo D.M., Lee A.K., Bouley D.M., Falkow S. mig-14 is a horizontally acquired, host-induced gene required for salmonella enterica lethal infection in the murine model of typhoid fever. Infect. Immun. 2000, 68:7126-7131.
62. Vergunst A.C., Meijer A.H., Renshaw S.A., O'Callaghan D. Burkholderia cenocepacia creates an intramacrophage replication niche in zebrafish embryos, followed by bacterial dissemination and establishment of systemic infection. Infect. Immun. 2010, 78:1495-1508.
63. Volkman H.E., Clay H., Beery D., Chang J.C., Sherman D.R., Ramakrishnan L. Tuberculous granuloma formation is enhanced by a mycobacterium virulence determinant. PLoS Biol. 2004, 2:e367.
64. 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.
65. White R.M., Cech J., Ratanasirintrawoot S., Lin C.Y., Rahl P.B., Burke C.J., Langdon E., Tomlinson M.L., Mosher J., Kaufman C., et al. DHODH modulates transcriptional elongation in the neural crest and melanoma. Nature 2011, 471:518-522.
66. Wiles T.J., Bower J.M., Redd M.J., Mulvey M.A. Use of zebrafish to probe the divergent virulence potentials and toxin requirements of extraintestinal pathogenic Escherichia coli. PLoS Pathog. 2009, 5:e1000697.
67. Zignol M., van Gemert W., Falzon D., Sismanidis C., Glaziou P., Floyd K., Raviglione M. Surveillance of anti-tuberculosis drug resistance in the world: an updated analysis, 2007-2010. Bull. World Health Organ. 2012, 90:111-119D.
68. Zon L.I., Peterson R.T. In vivo drug discovery in the zebrafish. Nat. Rev. Drug Discov. 2005, 4:35-44.