Zebrafish as a model for zoonotic aquatic pathogens

Developmental and Comparative Immunology

Volumn 46, Issue 1, 2014, Pages 96-107

  Rowe, Hannah M ^a   Withey, Jeffrey H ^a   Neely, Melody N ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aquaculture; Aquatic pathogens; Bacteria; Environmental reservoir; Zebrafish; Zoonotic

Indexed keywords

FLUMEQUINE; SULFONAMIDE; TRIMETHOPRIM;

AEROMONAS HYDROPHILA; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; AQUATIC ENVIRONMENT; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BACTERIAL VIRULENCE; DISEASE MODEL; DISEASE TRANSMISSION; EDWARDSIELLA TARDA; HOST PATHOGEN INTERACTION; HUMAN VERSUS ANIMAL COMPARISON; INNATE IMMUNITY; MYCOBACTERIUM; MYCOBACTERIUM MARINUM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; STREPTOCOCCUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS INIAE; SYMPTOMATOLOGY; VACCINATION; VIBRIO; VIBRIO ALGINLYTICUS; VIBRIO CHOLERAE; VIBRIO VULNIFICUS; WATER CONTAMINATION; ZEBRA FISH; ZOONOSIS; ANIMAL; BACTERIA; BACTERIAL PHENOMENA AND FUNCTIONS; CLASSIFICATION; HUMAN; IMMUNOLOGY; MICROBIOLOGY;

BACTERIA (MICROORGANISMS); DANIO RERIO;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; BACTERIAL PHYSIOLOGICAL PHENOMENA; HOST-PATHOGEN INTERACTIONS; HUMANS; WATER MICROBIOLOGY; ZEBRAFISH;

EID: 84900469574     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2014.02.014     Document Type: Review

References (131)

1. Abdallah A.M., Gey van Pittius N.C., Champion P.A., Cox J., Luirink J., Vandenbroucke-Grauls C.M., Appelmelk B.J., Bitter W. Type VII secretion-mycobacteria show the way. Nat. Rev. Microbiol. 2007, 5:883-891.
2. Agnew W., Barnes A.C. Streptococcus iniae: an aquatic pathogen of global veterinary significance and a challenging candidate for reliable vaccination. Vet. Microbiol. 2007, 122:1-15.
3. Allen J.P., Neely M.N. Trolling for the ideal model host: zebrafish take the bait. Future Microbiol. 2010, 5:563-569.
4. Allen J.P., Neely M.N. The Streptococcus iniae transcriptional regulator CpsY is required for protection from neutrophil-mediated killing and proper growth in vitro. Infect. Immun. 2011, 79:4638-4648.
5. Allen J.P., Neely M.N. CpsY influences Streptococcus iniae cell wall adaptations important for neutrophil intracellular survival. Infect. Immun. 2012, 80:1707-1715.
6. Auerbach P.S., Yajko D.M., Nassos P.S., Kizer K.W., McCosker J.E., Geehr E.C., Hadley W.K. Bacteriology of the marine environment: implications for clinical therapy. Ann. Emerg. Med. 1987, 16:643-649.
7. Austin B. Vibrios as causal agents of zoonoses. Vet. Microbiol. 2010, 140:310-317.
8. Bi Z.X., Liu Y.J., Lu C.P. Contribution of AhyR to virulence of Aeromonas hydrophila J-1. Res. Vet. Sci. 2007, 83:150-156.
9. Blake P.A., Weaver R.E., Hollis D.G. Diseases of humans (other than cholera) caused by vibrios. Annu. Rev. Microbiol. 1980, 34:341-367.
10. Bonamonte D., De Vito D., Vestita M., Delvecchio S., Ranieri L.D., Santantonio M., Angelini G. Aquarium-borne Mycobacterium marinum skin infection. Report of 15 cases and review of the literature. Eur. J. Dermatol. 2013, 23:510-516.
11. Bromage E.S., Owens L. Infection of barramundi Lates calcarifer with Streptococcus iniae: effects of different routes of exposure. Dis. Aquat. Org. 2002, 52:199-205.
12. Bryan J.D., Liles R., Cvek U., Trutschl M., Shelver D. Global transcriptional profiling reveals Streptococcus agalactiae genes controlled by the MtaR transcription factor. BMC Genomics 2008, 9:607.
13. Cantas L., Midtlyng P.J., Sorum H. Impact of antibiotic treatments on the expression of the R plasmid tra genes and on the host innate immune activity during pRAS1 bearing Aeromonas hydrophila infection in zebrafish (Danio rerio). BMC Microbiol. 2012, 12:37.
14. Cao Y., He S., Zhou Z., Zhang M., Mao W., Zhang H., Yao B. Orally administered thermostable N-acyl homoserine lactonase from Bacillus sp. strain AI96 attenuates Aeromonas hydrophila infection in zebrafish. Appl. Environ. Microbiol. 2012, 78:1899-1908.
15. Champion P.A., Cox J.S. Protein secretion systems in Mycobacteria. Cell. Microbiol. 2007, 9:1376-1384.
16. Chang W.J., Hwang P.P. Development of zebrafish epidermis. Birth defects research. Embryo Today: Rev. Part C 2011, 93:205-214.
17. 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.
18. 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.
19. Cleary P.P., Prahbu U., Dale J.B., Wexler D.E., Handley J. Streptococcal C5a peptidase is a highly specific endopeptidase. Infect. Immun. 1992, 60:5219-5223.
20. Cocchiaro, J.L., Rawls, J.F., 2013. Microgavage of zebrafish larvae. J. Visualized Exp. JoVE, e4434.
21. Collymore, C., Rasmussen, S., Tolwani, R.J., 2013. Gavaging adult zebrafish. J. Visualized Exp.: JoVE 78.
22. Cosma, C.L., Swaim, L.E., Volkman, H., Ramakrishnan, L., Davis, J.M., 2006. Zebrafish and frog models of Mycobacterium marinum infection. Curr. Protoc. Microbiol. Chapter 10, Unit 10B.12.
23. Cui Z., Samuel-Shaker D., Watral V., Kent M.L. Attenuated Mycobacterium marinum protects zebrafish against mycobacteriosis. J. Fish Dis. 2010, 33:371-375.
24. 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.
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. Dechet A.M., Yu P.A., Koram N., Painter J. Nonfoodborne Vibrio infections: an important cause of morbidity and mortality in the United States, 1997-2006. Clin. Infect. Dis. 2008, 46:970-976.
27. Delannoy C.M., Crumlish M., Fontaine M.C., Pollock J., Foster G., Dagleish M.P., Turnbull J.F., Zadoks R.N. Human Streptococcus agalactiae strains in aquatic mammals and fish. BMC Microbiol. 2013, 13:41.
28. Deng Q., Yoo S.K., Cavnar P.J., Green J.M., Huttenlocher A. Dual roles for Rac2 in neutrophil motility and active retention in zebrafish hematopoietic tissue. Dev. Cell 2011, 21:735-745.
29. Deng W., Tang X., Hou M., Li C., Xie J. New insights into the pathogenesis of tuberculosis revealed by Mycobacterium marinum: the zebrafish model from the systems biology perspective. Crit. Rev. Eukaryot. Gene Expr. 2011, 21:337-345.
30. Dong X., Fan X., Wang B., Shi X., Zhang X.H. Invasin of Edwardsiella tarda is essential for its haemolytic activity, biofilm formation and virulence towards fish. J. Appl. Microbiol. 2013, 115:12-19.
31. Edmond K.M., Kortsalioudaki C., Scott S., Schrag S.J., Zaidi A.K., Cousens S., Heath P.T. Group B streptococcal disease in infants aged younger than 3 months: systematic review and meta-analysis. Lancet 2012, 379:547-556.
32. Evans J.J., Bohnsack J.F., Klesius P.H., Whiting A.A., Garcia J.C., Shoemaker C.A., Takahashi S. Phylogenetic relationships among Streptococcus agalactiae isolated from piscine, dolphin, bovine and human sources: a dolphin and piscine lineage associated with a fish epidemic in Kuwait is also associated with human neonatal infections in Japan. J. Med. Microbiol. 2008, 57:1369-1376.
33. Evans J.J., Klesius P.H., Gilbert P.M., Shoemaker C.A., Al Sarawi M.A., Landsberg J., Duremdez R., Al Marzouk A., Al Zenki S. Characterization of beta-haemolytic Group B Streptococcus agalactiae in cultured seabream, Sparus auratus L., and wild mullet, Liza klunzingeri (Day), in Kuwait. J. Fish Dis. 2002, 25:505-513.
34. Ferreira J., Grochowsky J., Krakower D., Zuromskis P., Baden R., Cheifetz A.S. Mycobacterium marinum: an increasingly common opportunistic infection in patients on infliximab. Am. J. Gastroenterol. 2012, 107:1268-1269.
35. Finkelstein R., Oren I. Soft tissue infections caused by marine bacterial pathogens: epidemiology, diagnosis, and management. Curr. Infect. Dis. Rep. 2011, 13:470-477.
36. Fischetti V.A. Streptococcal M protein: molecular design and biological behavior. Clin. Microbiol. Rev. 1989, 2:285-314.
37. Formal S.B., Kundel D., Schneider H., Kunevn, Sprinz H. Studies with Vibrio cholerae in the ligated loop of the rabbit intestine. Br. J. Exp. Pathol. 1961, 42:504-510.
38. Foxman B., Gillespie B.W., Manning S.D., Marrs C.F. Risk factors for group B streptococcal colonization: potential for different transmission systems by capsular type. Ann. Epidemiol. 2007, 17:854-862.
39. Gao X., Cui Y., Levenson R.M., Chung L.W., Nie S. In vivo cancer targeting and imaging with semiconductor quantum dots. Nat. Biotechnol. 2004, 22:969-976.
40. Gauthier D.T., Rhodes M.W. Mycobacteriosis in fishes: a review. Vet. J. 2009, 180:33-47. (London, England: 1997).
41. Halpern M., Broza Y.B., Mittler S., Arakawa E., Broza M. Chironomid egg masses as a natural reservoir of Vibrio cholerae non-O1 and non-O139 in freshwater habitats. Microb. Ecol. 2004, 47:341-349.
42. Hansen J.D., Strassburger P. Description of an ectothermic TCR coreceptor, CD8 alpha, in rainbow trout. J. Immunol. 2000, 164:3132-3139.
43. Hanson B.R., Runft D.L., Streeter C., Kumar A., Carion T.W., Neely M.N. Functional analysis of the CpsA protein of Streptococcus agalactiae. J. Bacteriol. 2012, 194:1668-1678.
44. 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.
45. Harvie E.A., Green J.M., Neely M.N., Huttenlocher A. Innate Immune Response to Streptococcus iniae Infection in Zebrafish Larvae. Infect. Immun. 2013, 81:110-121.
46. He H., Wang Q., Sheng L., Liu Q., Zhang Y. Functional characterization of Vibrio alginolyticus twin-arginine translocation system: its roles in biofilm formation, extracellular protease activity, and virulence towards fish. Curr. Microbiol. 2011, 62:1193-1199.
47. Hood M.A., Ness G.E., Rodrick G.E. Isolation of Vibrio cholerae serotype O1 from the eastern oyster, Crassostrea virginica. Appl. Environ. Microbiol. 1981, 41:559-560.
48. Hoshina T., Sano T., Morimoto Y. A streptococcus pathogenic to fish. J. Tokyo Univ. Fish. 1958, 44:57-68.
49. Huang Y., Xu X., Liu Y., Wu K., Zhang W., Liu P., Zeng X., Sun J., Jiang Y., Wang H. Successful treatment of refractory cutaneous infection caused by Mycobacterium marinum with a combined regimen containing amikacin. Clin. Interv. Aging 2012, 7:533-538.
50. Igbinosa I.H., Igumbor E.U., Aghdasi F., Tom M., Okoh A.I. Emerging Aeromonas species infections and their significance in public health. SciWorldJ 2012, 2012:625023.
51. Jacobs J.M., Stine C.B., Baya A.M., Kent M.L. A review of mycobacteriosis in marine fish. J. Fish Dis. 2009, 32:119-130.
52. Janda J.M., Abbott S.L. Infections associated with the genus Edwardsiella: the role of Edwardsiella tarda in human disease. Clin. Infect. Dis. 1993, 17:742-748.
53. Janda J.M., Abbott S.L. The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin. Microbiol. Rev. 2010, 23:35-73.
54. Kanther M., Rawls J.F. Host-microbe interactions in the developing zebrafish. Curr. Opin. Immunol. 2010, 22:10-19.
55. Khajanchi B.K., Sha J., Kozlova E.V., Erova T.E., Suarez G., Sierra J.C., Popov V.L., Horneman A.J., Chopra A.K. N-acylhomoserine lactones involved in quorum sensing control the type VI secretion system, biofilm formation, protease production, and in vivo virulence in a clinical isolate of Aeromonas hydrophila. Microbiology 2009, 155:3518-3531.
56. Klose K.E. The suckling mouse model of cholera. Trends Microbiol. 2000, 8:189-191.
57. Koh T.H., Sng L.H., Yuen S.M., Thomas C.K., Tan P.L., Tan S.H., Wong N.S. Streptococcal cellulitis following preparation of fresh raw seafood. Zoonoses Public Health 2009, 56:206-208.
58. Koskiniemi S., Sellin M., Norgren M. Identification of two genes, cpsX and cpsY, with putative regulatory function on capsule expression in group B streptococci. FEMS Immunol. Med. Microbiol. 1998, 21:159-168.
59. Krishnan N., Robertson B.D., Thwaites G. The mechanisms and consequences of the extra-pulmonary dissemination of Mycobacterium tuberculosis. Tuberculosis (Edinburgh, Scotland) 2010, 90:361-366.
60. 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.
61. Lau S.K., Woo P.C., Tse H., Leung K.W., Wong S.S., Yuen K.Y. Invasive Streptococcus iniae infections outside North America. J. Clin. Microbiol. 2003, 41:1004-1009.
62. Lesley R., Ramakrishnan L. Insights into early mycobacterial pathogenesis from the zebrafish. Curr. Opin. Microbiol. 2008, 11:277-283.
63. Levraud J.P., Colucci-Guyon E., Redd M.J., Lutfalla G., Herbomel P. In vivo analysis of zebrafish innate immunity. Meth. Mol. Biol. (Clifton, N.J.) 2008, 415:337-363.
64. Li J., Ni X.D., Liu Y.J., Lu C.P. Detection of three virulence genes alt, ahp and aerA in Aeromonas hydrophila and their relationship with actual virulence to zebrafish. J. Appl. Microbiol. 2011, 110:823-830.
65. Li Y.J., Hu B. Establishment of multi-site infection model in zebrafish larvae for studying Staphylococcus aureus infectious disease. J. Genet. Genomics Yi chuan xue bao 2012, 39:521-534.
66. Locke J.B., Aziz R.K., Vicknair M.R., Nizet V., Buchanan J.T. Streptococcus iniae M-like protein contributes to virulence in fish and is a target for live attenuated vaccine development. PLoS One 2008, 3:e2824.
67. López-Muñoz A., Roca F.J., Meseguer J., Mulero V. New insights into the evolution of IFNs: zebrafish group II IFNs induce a rapid and transient expression of IFN-dependent genes and display powerful antiviral activities. J. Immunol. 2009, 182:3440-3449.
68. 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.
69. Meeker N.D., Trede N.S. Immunology and zebrafish: spawning new models of human disease. Dev. Comp. Immunol. 2008, 32:745-757.
70. Meijer A.H., Spaink H.P. Host-pathogen interactions made transparent with the zebrafish model. Curr. Drug Targets 2011, 12:1000-1017.
71. 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.
72. Mohanty B.R., Sahoo P.K. Edwardsiellosis in fish: a brief review. J. Biosci. 2007, 32:1331-1344.
73. Monette S., Dallaire A.D., Mingelbier M., Groman D., Uhland C., Richard J.P., Paillard G., Johannson L.M., Chivers D.P., Ferguson H.W., Leighton F.A., Simko E. Massive mortality of common carp (Cyprinus carpio carpio) in the St. Lawrence River in 2001: diagnostic investigation and experimental induction of lymphocytic encephalitis. Vet. Pathol. 2006, 43:302-310.
74. Neely M., Pfeifer J., Caparon M.G. Streptococcus-zebrafish model of bacterial pathogenesis. Infect. Immun. 2002, 70:3904-3914.
75. O'Toole G.A., Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 1998, 28:449-461.
76. Oksanen K.E., Halfpenny N.J., Sherwood E., Harjula S.K., Hammaren M.M., Ahava M.J., Pajula E.T., Lahtinen M.J., Parikka M., Ramet M. An adult zebrafish model for preclinical tuberculosis vaccine development. Vaccine 2013, 31:5202-5209.
77. Pan C.Y., Wu J.L., Hui C.F., Lin C.H., Chen J.Y. Insights into the antibacterial and immunomodulatory functions of the antimicrobial peptide, epinecidin-1, against Vibrio vulnificus infection in zebrafish. Fish Shellfish Immunol. 2011, 31:1019-1025.
78. Paranjpye R.N., Myers M.S., Yount E.C., Thompson J.L. Zebrafish as a model for Vibrio parahaemolyticus virulence. Microbiology 2013, 159:2605-2615.
79. Park S.B., Aoki T., Jung T.S. Pathogenesis of and strategies for preventing Edwardsiella tarda infection in fish. Vet. Res. 2012, 43:67.
80. Patterson H., Saralahti A., Parikka M., Dramsi S., Trieu-Cuot P., Poyart C., Rounioja S., Ramet M. Adult zebrafish model of bacterial meningitis in Streptococcus agalactiae infection. Dev. Comp. Immunol. 2012, 38:447-455.
81. Pereira U.P., Mian G.F., Oliveira I.C., Benchetrit L.C., Costa G.M., Figueiredo H.C. Genotyping of Streptococcus agalactiae strains isolated from fish, human and cattle and their virulence potential in Nile tilapia. Vet. Microbiol. 2010, 140:186-192.
82. Peterson T.S., Ferguson J.A., Watral V.G., Mutoji K.N., Ennis D.G., Kent M.L. Paramecium caudatum enhances transmission and infectivity of Mycobacterium marinum and M. chelonae in zebrafish Danio rerio. Dis. Aquat. Org. 2013, 106:229-239.
83. 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.
84. Phelps H.A., Neely M.N. Evolution of the zebrafish model: from development to immunity and infectious disease. Zebrafish 2005, 2:87-103.
85. Phillips G.N., Flicker P.F., Cohen C., Manjula B.N., Fischetti V.A. Streptococcal M protein: alpha-helical coiled-coil structure and arrangement on the cell surface. Proc. Natl. Acad. Sci. USA 1981, 78:4689-4693.
86. Pier G., Madin S. Streptococcous iniae sp.nov., a beta-hemolytic streptococcus isolated from an Amazon fresh-water dolphin, Inia geoffrensis. Int. J. Syst. Bacteriol. 1976, 26:545-553.
87. Pozos T.C., Ramakrishnan L. New models for the study of Mycobacterium-host interactions. Curr. Opin. Immunol. 2004, 16:499-505.
88. 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.
89. Ramakrishnan L. Looking within the zebrafish to understand the tuberculous granuloma. Adv. Exp. Med. Biol. 2013, 783:251-266.
90. Rawlings T.K., Ruiz G.M., Colwell R.R. Association of Vibrio cholerae O1 El Tor and O139 Bengal with the Copepods Acartia tonsa and Eurytemora affinis. Appl. Environ. Microbiol. 2007, 73:7926-7933.
91. Rawls J.F., Samuel B.S., Gordon J.I. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. USA 2004, 101:4596-4601.
92. 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.
93. Runft D.L., Mitchell K.C., Abuaita B.H., Allen J.P., Bajer S., Ginsburg K., Neely M.N., Withey J.H. Zebrafish as a natural host model for Vibrio cholerae colonization and transmission. Appl. Environ. Microbiol. 2014, 80:1710-1717.
94. Sack D.A., Sack R.B., Nair G.B., Siddique A.K. Cholera. Lancet 2004, 363:223-233.
95. Schlenker C., Surawicz C.M. Emerging infections of the gastrointestinal tract. Best Pract. Res. Clin. Gastroenterol. 2009, 23:89-99.
96. Senderovich Y., Izhaki I., Halpern M. Fish as reservoirs and vectors of Vibrio cholerae. PLoS One 2010, 5:e8607.
97. Shelver D., Rajagopal L., Harris T.O., Rubens C.E. MtaR, a regulator of methionine transport, is critical for survival of group B streptococcus in vivo. J. Bacteriol. 2003, 185:6592-6599.
98. Shoemaker C.A., Klesius P.H., Evans J.J. Prevalence of Streptococcus iniae in tilapia, hybrid striped bass, and channel catfish on commercial fish farms in the United States. Am. J. Vet. Res. 2001, 62:174-177.
99. Skoff T.H., Farley M.M., Petit S., Craig A.S., Schaffner W., Gershman K., Harrison L.H., Lynfield R., Mohle-Boetani J., Zansky S., Albanese B.A., Stefonek K., Zell E.R., Jackson D., Thompson T., Schrag S.J. Increasing burden of invasive group B streptococcal disease in Nonpregnant Adults, 1990, Äì2007. Clin. Infect. Dis. 2009, 49:85.
100. Spira W.M., Sack R.B. Kinetics of early cholera infection in the removable intestinal tie-adult rabbit diarrhea model. Infect. Immun. 1982, 35:952-957.
101. Spira W.M., Sack R.B., Froehlich J.L. Simple adult rabbit model for Vibrio cholerae and enterotoxigenic Escherichia coli diarrhea. Infect. Immun. 1981, 32:739-747.
102. Stoop E.J., Mishra A.K., Driessen N.N., van Stempvoort G., Bouchier P., Verboom T., van Leeuwen L.M., Sparrius M., Raadsen S.A., van Zon M., van der Wel N.N., Besra G.S., Geurtsen J., Bitter W., Appelmelk B.J., van der Sar A.M. Mannan core branching of lipo(arabino)mannan is required for mycobacterial virulence in the context of innate immunity. Cell. Microbiol. 2013, 15:2093-2108.
103. Sullivan C., Kim C.H. Zebrafish as a model for infectious disease and immune function. Fish Shellfish Immunol. 2008, 25:341-350.
104. Sun J.R., Yan J.C., Yeh C.Y., Lee S.Y., Lu J.J. Invasive infection with Streptococcus iniae in Taiwan. J. Med. Microbiol. 2007, 56:1246-1249.
105. 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.
106. Tamada T., Koganemaru H., Matsumoto K., Hitomi S. Urosepsis caused by Edwardsiella tarda. J. Infect. Chemother.: Off. J. Jpn Soc. Chemother. 2009, 15:191-194.
107. Tobin D.M., Ramakrishnan L. Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis. Cell. Microbiol. 2008, 10:1027-1039.
108. 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.
109. van der Sar A.M., Appelmelk B.J., Vandenbroucke-Grauls C.M., Bitter W. A star with stripes: zebrafish as an infection model. Trends Microbiol. 2004, 12:451-457.
110. van der Woude A.D., Stoop E.J., Stiess M., Wang S., Ummels R., van Stempvoort G., Piersma S.R., Cascioferro A., Jimenez C.R., Houben E.N., Luirink J., Pieters J., van der Sar A.M., Bitter W. Analysis of SecA2-dependent substrates in Mycobacterium marinum identifies protein kinase G (PknG) as a virulence effector. Cell Microbiol. 2013, 16:280-295.
111. van Soest J.J., Stockhammer O.W., Ordas A., Bloemberg G.V., Spaink H.P., Meijer A.H. Comparison of static immersion and intravenous injection systems for exposure of zebrafish embryos to the natural pathogen Edwardsiella tarda. BMC Immunol. 2011, 12:58.
112. Vezzulli L., Pruzzo C., Huq A., Colwell R.R. Environmental reservoirs of Vibrio cholerae and their role in cholera. Environ. Microbiol. Rep. 2010, 2:27-33.
113. Vilches S., Jimenez N., Tomas J.M., Merino S. Aeromonas hydrophila AH-3 type III secretion system expression and regulatory network. Appl. Environ. Microbiol. 2009, 75:6382-6392.
114. 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.
115. Wang H., Ji D., Shao J., Zhang S. Maternal transfer and protective role of antibodies in zebrafish Danio rerio. Mol. Immunol. 2012, 51:332-336.
116. Wang I.K., Kuo H.L., Chen Y.M., Lin C.L., Chang H.Y., Chuang F.R., Lee M.H. Extraintestinal manifestations of Edwardsiella tarda infection. Int. J. Clin. Pract. 2005, 59:917-921.
117. Wang K., Liu E., Song S., Wang X., Zhu Y., Ye J., Zhang H. Characterization of Edwardsiella tarda rpoN: roles in sigma(70) family regulation, growth, stress adaption and virulence toward fish. Arch. Microbiol. 2012, 194:493-504.
118. Wang Q., Liu Q., Cao X., Yang M., Zhang Y. Characterization of two TonB systems in marine fish pathogen Vibrio alginolyticus: their roles in iron utilization and virulence. Arch. Microbiol. 2008, 190:595-603.
119. Wang Z., Zhang S., Tong Z., Li L., Wang G. Maternal transfer and protective role of the alternative complement components in zebrafish Danio rerio. PLoS One 2009, 4:e4498.
120. Watral V., Kent M.L. Pathogenesis of Mycobacterium spp. in zebrafish (Danio rerio) from research facilities. Comp. Biochem. Physiol. Toxicol. Pharmacol. CBP 2007, 145:55-60.
121. Weerdenburg E.M., Abdallah A.M., Mitra S., de Punder K., van der Wel N.N., Bird S., Appelmelk B.J., Bitter W., van der Sar A.M. ESX-5-deficient Mycobacterium marinum is hypervirulent in adult zebrafish. Cell. Microbiol. 2012, 14:728-739.
122. Weinstein M.R., Litt M., Kertesz D.A., Wyper P., Rose D., Coulter M., McGeer A., Facklam R., Ostach C., Willey B., Borczyk A., Low D.E. Invasive infections due to a fish pathogen, Streptococcus iniae. New Engl. J. Med. 1997, 337:589-594.
123. Weinstein M.R., Low D.E., McGeer A., Willey B., Rose D., Coulter M., Wyper P., Borczyk A., Lovgren M. Invasive infection due to Streptococcus iniae: a new or previously unrecognized disease. CCDR 1996, 22:129-132.
124. Weinstein, M.R., Low, D.E., McGeer, A., Willey, B., Rose, D., Coulter, M., Wyper, P., Borczyk, A., Lovgren, M., 1996b. Invasive infection with Streptococcus iniae-Ontario, 1995-1996. MMWR Weekly.
125. Whipps C.M., Lieggi C., Wagner R. Mycobacteriosis in zebrafish colonies. ILAR J. Natl. Res. Council, Instit. Lab. Anim. Resour. 2012, 53:95-105.
126. Wu T.S., Chiu C.H., Yang C.H., Leu H.S., Huang C.T., Chen Y.C., Wu T.L., Chang P.Y., Su L.H., Kuo A.J., Chia J.H., Lu C.C., Lai H.C. Fish tank granuloma caused by Mycobacterium marinum. PLoS One 2012, 7:e41296.
127. Xiao J., Chen T., Wang Q., Zhang Y. Comparative analysis of the roles of catalases KatB and KatG in the physiological fitness and pathogenesis of fish pathogen Edwardsiella tarda. Lett. Appl. Microbiol. 2012, 54:425-432.
128. Yang D., Liu Q., Ni C., Li S., Wu H., Wang Q., Xiao J., Zhang Y. Gene expression profiling in live attenuated Edwardsiella tarda vaccine immunized and challenged zebrafish: insights into the basic mechanisms of protection seen in immunized fish. Dev. Comp. Immunol. 2013, 40:132-141.
129. Yoo S.K., Huttenlocher A. Spatiotemporal photolabeling of neutrophil trafficking during inflammation in live zebrafish. J. Leukoc. Biol. 2011, 89:661-667.
130. Yu J.E., Cho M.Y., Kim J.W., Kang H.Y. Large antibiotic-resistance plasmid of Edwardsiella tarda contributes to virulence in fish. Microb. Pathog. 2012, 52:259-266.
131. Zlotkin A., Hershko H., Eldar A. Possible transmission of Streptococcus iniae from wild fish to cultured marine fish. Appl. Environ. Microbiol. 1998, 64:4065-4067.