Study of Host-Microbe Interactions in Zebrafish

Methods in Cell Biology

Volumn 105, Issue , 2011, Pages 87-116

  Milligan Myhre, Kathryn ^a   Charette, Jeremy R ^b   Phennicie, Ryan T ^b   Stephens, W Zac ^a   Rawls, John F ^c,d   Guillemin, Karen ^a   Kim, Carol H ^a,b  

^a UNIVERSITY OF OREGON   (United States)

^b UNIVERSITY OF MAINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Host; Inoculation; Microbe; Microbiota; Pathogen; Toxin

Indexed keywords

EID: 80053214377     PISSN: 0091679X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-381320-6.00004-7     Document Type: Chapter

References (105)

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. Aggad D., Mazel M., Boudinot P., Mogensen K.E., Hamming O.J., Hartmann R., Kotenko S., Herbomel P., Lutfalla G., Levraud J.P. The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains. J. Immunol. 2009, 183:3924-3931.
3. Aggad D., Stein C., Sieger D., Mazel M., Boudinot P., Herbomel P., Levraud J.P., Lutfalla G., Leptin M. In vivo analysis of Ifn-gamma1 and Ifn-gamma2 signaling in zebrafish. J. Immunol. 2010, 185:6774-6782.
4. Alonso M., Kim C.H., Johnson M.C., Pressley M., Leong J.A. The NV gene of snakehead rhabdovirus (SHRV) is not required for pathogenesis, and a heterologous glycoprotein can be incorporated into the SHRV envelope. J. Virol. 2004, 78:5875-5882.
5. Altmann S.M., Mellon M.T., Distel D.L., Kim C.H. Molecular and functional analysis of an interferon gene from the zebrafish. Danio rerio. J. Virol. 2003, 77:1992-2002.
6. Altmann S.M., Mellon M.T., Johnson M.C., Paw B.H., Trede N.S., Zon L.I., Kim C.H. Cloning and characterization of an Mx gene and its corresponding promoter from the zebrafish. Danio rerio. Dev. Comp. Immunol. 2004, 28:295-306.
7. Bates J.M., Akerlund J., Mittge E., Guillemin K. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2007, 2:371-382.
8. Bates J.M., Mittge E., Kuhlman J., Baden K.N., Cheesman S.E., Guillemin K. Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev. Biol. 2006, 297:374-386.
9. Bates C.S., Toukoki C., Neely M.N., Eichenbaum Z. Characterization of MtsR, a new metal regulator in group A streptococcus, involved in iron acquisition and virulence. Infect. Immun. 2005, 73:5743-5753.
10. Bouskra D., Brezillon C., Berard M., Werts C., Varona R., Boneca I.G., Eberl G. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 2008, 456:507-510.
11. 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.
12. Brugman S., Liu K.Y., Lindenbergh-Kortleve D., Samsom J.N., Furuta G.T., Renshaw S.A., Willemsen R., Nieuwenhuis E.E. Oxazolone-induced enterocolitis in zebrafish depends on the composition of the intestinal microbiota. Gastroenterology 2009, 137:1757-17670.
13. Bry L., Falk P.G., Midtvedt T., Gordon J.I. A model of host-microbial interactions in an open mammalian ecosystem. Science 1996, 273:1380-1383.
14. Buller N.B. Bacteria from Fish and Other Aquatic Animals: A Practical Identification Manual 2004, CABI Publishing, Wallingford, UK.
15. Burgos J.S., Ripoll-Gomez J., Alfaro J.M., Sastre I., Valdivieso F. Zebrafish as a new model for herpes simplex virus type 1 infection. Zebrafish 2008, 5:323-333.
16. Carvalho R., de Sonneville J., Stockhammer O.W., Savage N.D., Veneman W.J., Ottenhoff T.H., Dirks R.P., Meijer A.H., Spaink H.P. A high-throughput screen for tuberculosis progression. PLoS One 2011, 6:e16779.
17. Cebra J.J., Periwal S.B., Lee G., Lee F., Shroff K.E. Development and maintenance of the gut-associated lymphoid tissue (GALT): the roles of enteric bacteria and viruses. Dev. Immunol. 1998, 6:13-18.
18. Cheesman S.E., Neal J.T., Mittge E., Seredick B.M., Guillemin K. Epithelial cell proliferation in the developing zebrafish intestine is regulated by the Wnt pathway and microbial signaling via Myd88. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(suppl. 1):4570-4577.
19. Cho K.H., Caparon M.G. Patterns of virulence gene expression differ between biofilm and tissue communities of Streptococcus pyogenes. Mol. Microbiol. 2005, 57:1545-1556.
20. 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.
21. 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.
22. Clay H., Volkman H.E., Ramakrishnan L. Tumor necrosis factor signaling mediates resistance to mycobacteria by inhibiting bacterial growth and macrophage death. Immunity 2008, 29:283-294.
23. 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.
24. Davis J.M., Haake D.A., Ramakrishnan L. Leptospira interrogans stably infects zebrafish embryos, altering phagocyte behavior and homing to specific tissues. PLoS Negl. Trop. Dis. 2009, 3:e463.
25. Davis J.M., Ramakrishnan L. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 2009, 136:37-49.
26. Deng Y., Boon C., Eberl L., Zhang L.H. Differential modulation of Burkholderia cenocepacia virulence and energy metabolism by the quorum-sensing signal BDSF and its synthase. J. Bacteriol. 2009, 191:7270-7278.
27. Ellett F., Pase L., Hayman J.W., Andrianopoulos A., Lieschke G.J. mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood 2011, 117:e49-e56.
28. Encinas P., Rodriguez-Milla M.A., Novoa B., Estepa A., Figueras A., Coll J. Zebrafish fin immune responses during high mortality infections with viral haemorrhagic septicemia rhabdovirus. A proteomic and transcriptomic approach. BMC Genomics 2010, 11:518.
29. Falkow S. Molecular Koch's postulates applied to microbial pathogenicity. Rev. Infect. Dis. 1988, 10(suppl. 2):S274-S276.
30. Fraune S., Bosch T.C. Why bacteria matter in animal development and evolution. Bioessays 2010, 32:571-580.
31. Gao L.Y., Pak M., Kish R., Kajihara K., Brown E.J. A mycobacterial operon essential for virulence in vivo and invasion and intracellular persistence in macrophages. Infect. Immun. 2006, 74:1757-1767.
32. Garner J.N., Joshi B., Jagus R. Characterization of rainbow trout and zebrafish eukaryotic initiation factor 2alpha and its response to endoplasmic reticulum stress and IPNV infection. Dev. Comp. Immunol. 2003, 27:217-231.
33. Gray C., Loynes C.A., Whyte M.K., Crossman D.C., Renshaw S.A., Chico T.J. Simultaneous intravital imaging of macrophage and neutrophil behaviour during inflammation using a novel transgenic zebrafish. Thromb. Haemost. 2011, 105:811-819.
34. Harriff M.J., Bermudez L.E., Kent M.L. 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. 2007, 30:587-600.
35. Herbomel P., Thisse B., Thisse C. Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 1999, 126:3735-3745.
36. Hermann A.C., Kim C.H. Effects of arsenic on zebrafish innate immune system. Mar. Biotechnol. (NY) 2005, 7:494-505.
37. Hermann A.C., Millard P.J., Blake S.L., Kim C.H. Development of a respiratory burst assay using zebrafish kidneys and embryos. J. Immunol. Methods 2004, 292:119-129.
38. Hooper L.V., Wong M.H., Thelin A., Hansson L., Falk P.G., Gordon J.I. Molecular analysis of commensal host-microbial relationships in the intestine. Science 2001, 291:881-884.
39. Husebye E., Hellstrom P.M., Midtvedt T. Intestinal microflora stimulates myoelectric activity of rat small intestine by promoting cyclic initiation and aboral propagation of migrating myoelectric complex. Dig. Dis. Sci. 1994, 39:946-956.
40. Kandori H., Hirayama K., Takeda M., Doi K. Histochemical, lectin-histochemical and morphometrical characteristics of intestinal goblet cells of germfree and conventional mice. Exp. Anim. 1996, 45:155-160.
41. Kanther M., Rawls J.F. Host-microbe interactions in the developing zebrafish. Curr. Opin. Immunol. 2010, 22:10-19.
42. Kanther M., Sun X., Muhlbauer M., Mackey L.C., Flynn E.J., Bagnat M., Jobin C., Rawls J.F. Microbial colonization induces dynamic temporal and spatial patterns of NF-kappaB activation in the zebrafish digestive tract. Gastroenterology 2011, 146:197-207.
43. Kizy A.E., Neely M.N. First Streptococcus pyogenes signature-tagged mutagenesis screen identifies novel virulence determinants. Infect. Immun. 2009, 77:1854-1865.
44. Lam S.H., Chua H.L., Gong Z., Lam T.J., Sin Y.M. Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Dev. Comp. Immunol. 2004, 28:9-28.
45. LaPatra S.E., Barone L., Jones G.R., Zon L.I. Effects of infectious hematopoietic necrosis virus and infectious pancreatic necrosis virus infection on hematopoietic precursors of the zebrafish. Blood Cells Mol. Dis. 2000, 26:445-452.
46. Lawson N.D., Weinstein B.M. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 2002, 248:307-318.
47. Levraud J.P., Disson O., Kissa K., Bonne I., Cossart P., Herbomel P., Lecuit M. Real-time observation of Listeria monocytogenes-phagocyte interactions in living zebrafish larvae. Infect. Immun. 2009, 77:3651-3660.
48. Lin B., Chen S., Cao Z., Lin Y., Mo D., Zhang H., Gu J., Dong M., Liu Z., Xu A. Acute phase response in zebrafish upon Aeromonas salmonicida and Staphylococcus aureus infection: striking similarities and obvious differences with mammals. Mol. Immunol. 2007, 44:295-301.
49. Llamas M.A., van der Sar A., Chu B.C., Sparrius M., Vogel H.J., Bitter W. A novel extracytoplasmic function (ECF) sigma factor regulates virulence in Pseudomonas aeruginosa. PLoS Pathog. 2009, 5:e1000572.
50. Lowe B.A., Miller J.D., Neely M.N. Analysis of the polysaccharide capsule of the systemic pathogen Streptococcus iniae and its implications in virulence. Infect. Immun. 2007, 75:1255-1264.
51. Lu M.W., Chao Y.M., Guo T.C., Santi N., Evensen O., Kasani S.K., Hong J.R., Wu J.L. The interferon response is involved in nervous necrosis virus acute and persistent infection in zebrafish infection model. Mol. Immunol. 2008, 45:1146-1152.
52. Ludwig M., Palha N., Torhy C., Briolat V., Colucci-Guyon E., Bremont M., Herbomel P., Boudinot P., Levraud J.P. Whole-body analysis of a viral infection: vascular endothelium is a primary target of infectious hematopoietic necrosis virus in zebrafish larvae. PLoS Pathog. 2011, 7:e1001269.
53. Mathias J.R., Perrin B.J., Liu T.X., Kanki J., Look A.T., Huttenlocher A. Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J. Leukoc. Biol. 2006, 80:1281-1288.
54. Meijer A.H., Verbeek F.J., Salas-Vidal E., Corredor-Adamez M., Bussman J., van der Sar A.M., Otto G.W., Geisler R., Spaink H.P. Transcriptome profiling of adult zebrafish at the late stage of chronic tuberculosis due to Mycobacterium marinum infection. Mol. Immunol. 2005, 42:1185-1203.
55. Menudier A., Rougier F.P., Bosgiraud C. Comparative virulence between different strains of Listeria in zebrafish (Brachydanio rerio) and mice. Pathol. Biol. (Paris) 1996, 44:783-789.
56. Miller J.D., Neely M.N. Large-scale screen highlights the importance of capsule for virulence in the zoonotic pathogen Streptococcus iniae. Infect. Immun. 2005, 73:921-934.
57. Montanez G.E., Neely M.N., Eichenbaum Z. The streptococcal iron uptake (Siu) transporter is required for iron uptake and virulence in a zebrafish infection model. Microbiology 2005, 151:3749-3757.
58. Morgan J.L., Darling A.E., Eisen J.A. Metagenomic sequencing of an in vitro-simulated microbial community. PLoS One 2010, 5:e10209.
59. Moyer T.R., Hunnicutt D.W. Susceptibility of zebra fish Danio rerio to infection by Flavobacterium columnare and F. johnsoniae. Dis. Aquat. Organ. 2007, 76:39-44.
60. Nayak A.S., Lage C.R., Kim C.H. Effects of low concentrations of arsenic on the innate immune system of the zebrafish (Danio rerio). Toxicol. Sci. 2007, 98:118-124.
61. Neely M.N., Pfeifer J.D., Caparon M. Streptococcus-zebrafish model of bacterial pathogenesis. Infect. Immun. 2002, 70:3904-3914.
62. Novoa B., Romero A., Mulero V., Rodriguez I., Fernandez I., Figueras A. Zebrafish (Danio rerio) as a model for the study of vaccination against viral haemorrhagic septicemia virus (VHSV). Vaccine 2006, 24:5806-5816.
63. O'Toole R., Von Hofsten J., Rosqvist R., Olsson P.E., Wolf-Watz H. Visualisation of zebrafish infection by GFP-labelled Vibrio anguillarum. Microb. Pathog. 2004, 37:41-46.
64. Ordas A., Hegedus Z., Henkel C.V., Stockhammer O.W., Butler D., Jansen H.J., Racz P., Mink M., Spaink H.P., Meijer A.H. Deep sequencing of the innate immune transcriptomic response of zebrafish embryos to Salmonella infection. Fish Shellfish Immunol 2010, (Epub ahead of print) 2010 Sep 8. PMID: 20816807.
65. Parichy D.M., Ransom D.G., Paw B., Zon L.I., Johnson S.L. An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio. Development 2000, 127:3031-3044.
66. Petrie-Hanson L., Romano C.L., Mackey R.B., Khosravi P., Hohn C.M., Boyle C.R. Evaluation of zebrafish Danio rerio as a model for enteric septicemia of catfish (ESC). J. Aquat. Anim. Health 2007, 19:151-158.
67. Pham L.N., Kanther M., Semova I., Rawls J.F. Methods for generating and colonizing gnotobiotic zebrafish. Nat. Protoc. 2008, 3:1862-1875.
68. Phelan P.E., Mellon M.T., Kim C.H. Functional characterization of full-length TLR3, IRAK-4, and TRAF6 in zebrafish (Danio rerio). Mol. Immunol. 2005, 42:1057-1071.
69. Phelan P.E., Pressley M.E., Witten P.E., Mellon M.T., Blake S., Kim C.H. Characterization of snakehead rhabdovirus infection in zebrafish (Danio rerio). J. Virol. 2005, 79:1842-1852.
70. Phennicie R.T., Sullivan M.J., Singer J.T., Yoder J.A., Kim C.H. Specific resistance to Pseudomonas aeruginosa infection in zebrafish is mediated by the cystic fibrosis transmembrane conductance regulator. Infect. Immun. 2010, 78:4542-4550.
71. 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.
72. Pressley M.E., Phelan P.E., Witten P.E., Mellon M.T., Kim C.H. Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Dev. Comp. Immunol. 2005, 29:501-513.
73. Rawls J.F., Mahowald M.A., Goodman A.L., Trent C.M., Gordon J.I. In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebrafish gut. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:7622-7627.
74. Rawls J.F., Mahowald M.A., Ley R.E., Gordon J.I. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 2006, 127:423-433.
75. Rawls J.F., Samuel B.S., Gordon J.I. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:4596-4601.
76. Renshaw S.A., Loynes C.A., Trushell D.M., Elworthy S., Ingham P.W., Whyte M.K. A transgenic zebrafish model of neutrophilic inflammation. Blood 2006, 108:3976-3978.
77. Rhodes J., Hagen A., Hsu K., Deng M., Liu T.X., Look A.T., Kanki J.P. Interplay of pu.1 and gata1 determines myelo-erythroid progenitor cell fate in zebrafish. Dev. Cell 2005, 8:97-108.
78. Rodriguez I., Novoa B., Figueras A. Immune response of zebrafish (Danio rerio) against a newly isolated bacterial pathogen Aeromonas hydrophila. Fish Shellfish Immunol. 2008, 25:239-249.
79. Roeselers G., Mittge E., Parichy D., Cavanaugh C.M., Guillemin K., Rawls J.F. Evidence for a core gut microbiota in the zebrafish. ISME J. 2011, (Epub ahead of print) 2011 Apr 7. PMID: 21472014.
80. Rojo I., de Ilarduya O.M., Estonba A., Pardo M.A. Innate immune gene expression in individual zebrafish after Listonella anguillarum inoculation. Fish Shellfish Immunol. 2007, 23:1285-1293.
81. Sanders G.E., Batts W.N., Winton J.R. Susceptibility of zebrafish (Danio rerio) to a model pathogen, spring viremia of carp virus. Comp. Med. 2003, 53:514-521.
82. Savage D.C., Siegel J.E., Snellen J.E., Whitt D.D. Transit time of epithelial cells in the small intestines of germfree mice and ex-germfree mice associated with indigenous microorganisms. Appl. Environ. Microbiol. 1981, 42:996-1001.
83. Shotts E.B., Waltman W.D. A medium for the selective isolation of Edwardsiella ictaluri. J. Wildl. Dis. 1990, 26:214-218.
84. Singer J.T., Phennicie R.T., Sullivan M.J., Porter L.A., Shaffer V.J., Kim C.H. Broad-host-range plasmids for red fluorescent protein labeling of gram-negative bacteria for use in the zebrafish model system. Appl. Environ. Microbiol. 2010, 76:3467-3474.
85. Stockhammer O.W., Zakrzewska A., Hegedus Z., Spaink H.P., Meijer A.H. Transcriptome profiling and functional analyses of the zebrafish embryonic innate immune response to Salmonella infection. J. Immunol. 2009, 182:5641-5653.
86. Stoop E.J., Schipper T., Rosendahl Huber S.K., Nezhinsky A.E., Verbeek F.J., Gurcha S.S., Besra G.S., Vandenbroucke-Grauls C.M., Bitter W., van der Sar A.M. Zebrafish embryo screen for mycobacterial genes involved in the initiation of granuloma formation reveals a newly identified ESX-1 component. Dis. Model Mech 2011, 4:526-536.
87. Su F., Juarez M.A., Cooke C.L., Lapointe L., Shavit J.A., Yamaoka J.S., Lyons S.E. Differential regulation of primitive myelopoiesis in the zebrafish by Spi-1/Pu.1 and C/ebp1. Zebrafish 2007, 4:187-199.
88. Sullivan C., Charette J., Catchen J., Lage C.R., Giasson G., Postlethwait J.H., Millard P.J., Kim C.H. The gene history of zebrafish tlr4a and tlr4b is predictive of their divergent functions. J. Immunol. 2009, 183:5896-5908.
89. Sullivan C., Postlethwait J.H., Lage C.R., Millard P.J., Kim C.H. Evidence for evolving Toll-IL-1 receptor-containing adaptor molecule function in vertebrates. J. Immunol. 2007, 178:4517-4527.
90. 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.
91. 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.
92. 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.
93. van der Sar A.M., Musters R.J., van Eeden F.J., Appelmelk B.J., Vandenbroucke-Grauls C.M., Bitter W. Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections. Cell. Microbiol. 2003, 5:601-611.
94. van der Sar A.M., Stockhammer O.W., van der Laan C., Spaink H.P., Bitter W., Meijer A.H. MyD88 innate immune function in a zebrafish embryo infection model. Infect. Immun. 2006, 74:2436-2441.
95. Vasil M.L., Stonehouse M.J., Vasil A.I., Wadsworth S.J., Goldfine H., Bolcome R.E., Chan J. A complex extracellular sphingomyelinase of Pseudomonas aeruginosa inhibits angiogenesis by selective cytotoxicity to endothelial cells. PLoS Pathog. 2009, 5:e1000420.
96. 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.
97. Vojtech L.N., Sanders G.E., Conway C., Ostland V., Hansen J.D. Host immune response and acute disease in a zebrafish model of Francisella pathogenesis. Infect. Immun. 2009, 77:914-925.
98. 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.
99. Wang Z.L., Xu X.P., He B.L., Weng S.P., Xiao J., Wang L., Lin T., Liu X., Wang Q., Yu X.Q., et al. Infectious spleen and kidney necrosis virus ORF48R functions as a new viral vascular endothelial growth factor. J. Virol. 2008, 82:4371-4383.
100. Wang L., Zhang H.X., Zhang J.H., Chen W.H., Ruan X.F., Xia C. In vitro effects of recombinant zebrafish IFN on spring viremia of carp virus and infectious hematopoietic necrosis virus. J. Interferon Cytokine Res. 2006, 26:256-259.
101. Westerfield M. The Zebrafish Book 2000, University of Oregon Press, Eugene, OR.
102. Whipps C.M., Dougan S.T., Kent M.L. Mycobacterium haemophilum infections of zebrafish (Danio rerio) in research facilities. FEMS Microbiol. Lett. 2007, 270:21-26.
103. Wienholds E., Schulte-Merker S., Walderich B., Plasterk R.H. Target-selected inactivation of the zebrafish rag1 gene. Science 2002, 297:99-102.
104. Xiong X.P., Dong C.F., Xu X., Weng S.P., Liu Z.Y., He J.G. Proteomic analysis of zebrafish (Danio rerio) infected with infectious spleen and kidney necrosis virus. Dev. Comp. Immunol. 2011, 35:431-440.
105. Xu X., Zhang L., Weng S., Huang Z., Lu J., Lan D., Zhong X., Yu X., Xu A., He J. A zebrafish (Danio rerio) model of infectious spleen and kidney necrosis virus (ISKNV) infection. Virology 2008, 376:1-12.