Immersion infection of germ-free zebrafish with Listeria monocytogenes induces transient expression of innate immune response genes

Frontiers in Microbiology

Volumn 6, Issue APR, 2015, Pages

  Shan, Ying ^a   Fang, Chun ^a   Cheng, Changyong ^a   Wang, Yong ^b   Peng, Jinrong ^b   Fang, Weihuan ^a,b  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Germ free zebrafish; Immersion; Infection model; Innate immune responses; Listeria monocytogenes

Indexed keywords

CYTOCHROME P450 1A; GELATINASE B; INTERLEUKIN 1BETA;

AGRICULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; EMBRYO; GENE EXPRESSION; HATCHING; INFECTION; INNATE IMMUNITY; LARVA; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGE; MORTALITY; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA ISOLATION; SURVIVAL RATE; YOLK SAC; ZEBRA FISH INFECTION;

ANIMALIA; BACTERIA (MICROORGANISMS); DANIO RERIO; LISTERIA MONOCYTOGENES; MURINAE;

EID: 84930942315     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00373     Document Type: Article

References (46)

1. Barksby, H. E., Lea, S. R., Preshaw, P. M., and Taylor, J. J. (2007). The expanding family of interleukin-1 cytokines and their role in destructive inflammatory disorders. Clin. Exp. Immunol. 149, 217-225. doi: 10.1111/j.1365-2249.2007.03441.x.
2. Bates, J. M., Mittge, E., Kuhlman, J., Baden, K. N., Cheesman, S. E., and Guillemin, K. (2006). Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev. Biol. 297, 374-386. doi: 10.1016/j.ydbio.2006.05.006.
3. Bécavin, C., Bouchier, C., Lechat, P., Archambaud, C., Creno, S., Gouin, E., et al. (2014). Comparison of widely used Listeria Monocytogenes strains egd, 10403s, and egd-E highlights genomic differences underlying variations in pathogenicity. mBio. 5:e00969-14. doi: 10.1128/mBio.00969-14.
4. Benard, E. L., van der Sar, A. M., Ellett, F., Lieschke, G. J., Spaink, H. P., and Meijer, A. H. (2012). Infection of zebrafish embryos with intracellular bacterial pathogens. J. Vis. Exp. 61:3781. doi: 10.3791/3781.
5. Brosch, R., Catimel, B., Milon, G., Buchrieser, C., Vindel, E., and Rocourt, J. (1993). Virulence heterogeneity of Listeria Monocytogenes strains from various sources (food, human, animal) in immunocompetent mice and its association with typing characteristics. J. Food Prot. 56, 297-301.
6. Carvalho, R., de Sonneville, J., Stockhammer, O. W., Savage, N. D., Veneman, W. J., Ottenhoff, T. H., et al. (2011). A high-throughput screen for tuberculosis progression. PLoS ONE 6:e16779. doi: 10.1371/journal.pone.0016779.
7. Chao, C.-C., Hsu, P.-C., Jen, C.-F., Chen, I.-H., Wang, C.-H., Chan, H.-C., et al. (2010). Zebrafish as a model host for Candida Albicans Infection. Infect. Immun. 78, 2512-2521. doi: 10.1128/IAI.01293-09.
8. Chen, J., Chen, Q., Jiang, J., Hu, H., Ye, J., and Fang, W. (2010). Serovar 4b complex predominates among Listeria monocytogenes isolates from imported aquatic products in China. Foodborne Pathog. Dis. 7, 31-41. doi: 10.1089/fpd.2009.0353.
9. Clay, H., Davis, J., Beery, D., Huttenlocher, A., Lyons, S. E., and Ramakrishnan, L. (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.
10. Cossart, P. (2007). Listeriology (1926-2007): the rise of a model pathogen. Microbes Infect. 9, 1143-1146. doi: 10.1016/j.micinf.2007.05.001.
11. Cui, C., Benard, E. L., Kanwal, Z., Stockhammer, O. W., van der Vaart, M., Zakrzewska, A., et al. (2011). Infectious disease modeling and innate immune function in zebrafish embryos. Methods Cell Biol. 105, 273-308. doi: 10.1016/B978-0-12-381320-6.00012-6.
12. Davis, J., Clay, H., Lewis, J. L., Ghori, N., Herbomel, P., and Ramakrishnan, L. (2002). Real-yime 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.
13. Davis, J., and 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.
14. Degrandi, D., Hoffmann, R., Beuter-Gunia, C., and Pfeffer, K. (2009). The proinflammatory cytokine-induced Irg1 protein associates with mitochondria. J. Interferon Cytokine Res. 29, 55-68. doi: 10.1089/jir.2008.0013.
15. Dinarello, C. A. (2009). Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 27, 519-550. doi: 10.1146/annurev.immunol.021908.132612.
16. Do, K. N., Fink, L. N., Jensen, T. E., Gautier, L., and Parlesak, A. (2012). Tlr2 controls intestinal carcinogen detoxication by Cyp1a1. PLoS ONE 7:e32309. doi: 10.1371/journal.pone.0032309.
17. Fortineau, N., Trieu-Cuot, P., Gaillot, O., Pellegrini, E., Berche, P., and Gaillard, J. L. (2000). Optimization of green fluorescent protein expression vectors for in vitro and in vivo detection of Listeria monocytogenes. Res. Microbiol. 151, 353-360. doi: 10.1016/S0923-2508(00)00158-3.
18. Herbomel, P., Thisse, B., and Thisse, C. (1999). Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126, 3735-3745.
19. Jennifer H, G., and Hazel, S. (2009). Zebrafish brain ventricle injection. J. Vis. Exp. 26:1218. doi: 10.3791/1218.
20. Johansson, J., Mandin, P., Renzoni, A., Chiaruttini, C., Springer, M., and Cossart, P. (2002). An Rna thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110, 551-561. doi: 10.1016/S0092-8674(02)00905-4.
21. Kanther, M., Sun, X., Mühlbauer, M., Mackey, L. C., Flynn, E. J., Bagnat, M., et al. (2011). Microbial colonization induces dynamic temporal and spatial patterns of Nf-Kb activation in the zebrafish digestive tract. Gastroenterology 141, 197-207. doi: 10.1053/j.gastro.2011.03.042.
22. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310. doi: 10.1002/aja.1002030302.
23. Levraud, J.-P., Disson, O., Kissa, K., Bonne, I., Cossart, P., Herbomel, P., et al. (2009). Real-time observation of Listeria monocytogenes-Phagocyte interactions in living zebrafish larvae. Infect. Immun. 77, 3651-3660. doi: 10.1128/IAI.00408-09.
24. Li, L., Yan, B., Shi, Y.-Q., Zhang, W.-Q., and Wen, Z.-L. (2012). Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration. J. Biol. Chem. 287, 25353-25360. doi: 10.1074/jbc.M112.349126.
25. Li, Y., and Hu, B. (2012). Establishment of multi-site infection model in zebrafish larvae for studying Staphylococcus aureus infectious disease. J. Genet. Genomics 39, 521-534. doi: 10.1016/j.jgg.2012.07.006.
26. Meijer, A. H., Gabby Krens, S. F., Medina Rodriguez, I. A., He, S., Bitter, W., Ewa Snaar-Jagalska, B., et al. (2004). Expression analysis of the toll-like receptor and tir domain adaptor families of zebrafish. Mol. Immunol. 40, 773-783. doi: 10.1016/j.molimm.2003.10.003.
27. Meijer, A. H., and Spaink, H. P. (2011). Host-pathogen interactions made transparent with the zebrafish model. Curr. Drug Targets 12, 1000-1017. doi: 10.2174/138945011795677809.
28. Menudier, A., Rougier, F. P., and Bosgiraud, C. (1996). Comparative virulence between different strains of Listeria in Zebrafish (Brachydanio Rerio) and Mice. Pathol. Biol. 44, 783-789.
29. Novoa, B., and Figueras, A. (2012). "Zebrafish: model for the study of inflammation, and the innate immune response to infectious diseases," in Current Topics in Innate Immunity II, eds J. D. Lambris and G. Hajishengallis (New York: Springer), 253-275.
30. Pham, L. N., Kanther, M., Semova, I., and Rawls, J. F. (2008). Methods for generating and colonizing gnotobiotic Zebrafish. Nat. Protoc. 3, 1862-1875. doi: 10.1038/nprot.2008.186.
31. Pressley, M. E., Phelan, P. E., Witten, P. E., Mellon, M. T., and Kim, C. H. (2005). Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Dev. Comp. Immunol. 29, 501-513. doi: 10.1016/j.dci.2004.10.007.
32. Prouty, M. G., Correa, N. E., Barker, L. P., Jagadeeswaran, P., and Klose, K. E. (2003). Zebrafish-Mycobacterium marinum model for mycobacterial pathogenesis. FEMS Microbiol. Lett. 225, 177-182. doi: 10.1016/S0378-1097(03)00446-4.
33. Rendueles, O., Ferrières, L., Frétaud, M., Bégaud, E., Herbomel, P., Levraud, J. P., et al. (2012). A new Zebrafish model of oro-intestinal pathogen colonization reveals a key role for adhesion in protection by probiotic bacteria. PLoS Pathog. J. 8:e1002815. doi: 10.1371/journal.ppat.1002815.
34. Rodas-Suárez, O. R., Flores-Pedroche, J. F., Betancourt-Rule, J. M., Quiñones-Ramírez, E. I., and Vázquez-Salinas, C. (2006). Occurrence and antibiotic sensitivity of Listeria monocytogenes strains isolated from oysters, fish, and estuarine water. Appl. Environ. Microbiol. 72, 7410-7412. doi: 10.1128/AEM.00956-06.
35. Sanders, G. E., Batts, W. N., and Winton, J. R. (2003). Susceptibility of zebrafish (Danio rerio) to a model pathogen, spring viremia of carp virus. Comp. Med. 53, 514-521.
36. Schlech, W. F. III, Chase, D. P., and Badley, A. (1993). A model of food-borne Listeria Monocytogenes infection in the sprague-dawley rat using gastric inoculation: development and effect of gastric acidity on infective dose. Int. J. Food Microbiol. 18, 15-24. doi: 10.1016/0168-1605(93)90003-Y.
37. Stavru, F., Archambaud, C., and Cossart, P. (2011). Cell biology and immunology of Listeria monocytogenes infections: novel insights. Immunol. Rev. 240, 160-184. doi: 10.1111/j.1600-065X.2010.00993.x.
38. Stockhammer, O. W., Zakrzewska, A., Hegedûs, Z., Spaink, H. P., and Meijer, A. H. (2009). Transcriptome profiling and functional analyses of the zebrafish embryonic innate immune response to Salmonella Infection. J. Immunol. 182, 5641-5653. doi: 10.4049/jimmunol.0900082.
39. Tobin, D. M., May, R. C., and Wheeler, R. T. (2012). Zebrafish: a see-through host and a fluorescent toolbox to probe host-pathogen interaction. PLoS Pathog. J. 8:e1002349. doi: 10.1371/journal.ppat.1002349.
40. Toh, M. C., Goodyear, M., Daigneault, M., Allen-Vercoe, E., and Van Raay, T. J. (2013). Colonizing the embryonic Zebrafish gut with anaerobic bacteria derived from the human gastrointestinal tract. Zebrafish 10, 194-198. doi: 10.1089/zeb.2012.0814.
41. Trede, N. S., Langenau, D. M., Traver, D., Look, A. T., and Zon, L. I. (2004). The use of zebrafish to understand immunity. Immunity 20, 367-379. doi: 10.1016/S1074-7613(04)00084-6.
42. Van Der Sar, A. M., Musters, R. J., Van Eeden, F. J., Appelmelk, B. J., Vandenbroucke-Grauls, C. M., and Bitter, W. (2003). Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections. Cell. Microbiol. 5, 601-611. doi: 10.1046/j.1462-5822.2003.00303.x.
43. van Soest, J. J., Stockhammer, O. W., Ordas, A., Bloemberg, G. V., Spaink, H. P., and Meijer, A. H. (2011). Comparison of static immersion and intravenous injection systems for exposure of zebrafish embryos to the natural pathogen Edwardsiella tarda. BMC Immunol. 12:58. doi: 10.1186/1471-2172-12-58.
44. Volkman, H. E., Pozos, T. C., Zheng, J., Davis, J. M., Rawls, J. F., and Ramakrishnan, L. (2010). Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 327, 466-469. doi: 10.1126/science.1179663.
45. Yamazaki, K., Teraoka, H., Dong, W., Stegeman, J. J., and Hiraga, T. (2002). Cdna cloning and expressions of cytochrome P450 1a in zebrafish embryos. J. Vet. Med. Sci. 64, 829-833. doi: 10.1292/jvms.64.829.
46. Yoong, S., O'Connell, B., Soanes, A., Crowhurst, M. O., Lieschke, G. J., and Ward, A. C. (2007). Characterization of the zebrafish matrix metalloproteinase 9 gene and its developmental expression pattern. Gene Expr. Patterns 7, 39-46. doi: 10.1016/j.modgep.2006.05.005.