Source: http://www.asmscience.org/content/book/10.1128/9781555816650.ch34
Timestamp: 2019-04-18 22:32:55+00:00

Document:
The zebrafish as a model for host-pathogen interactions has now matured to the point that we can reflect on what it truly has to offer, where it is helpful, and how it complements other models. The genetic advantages of zebrafish are often considered the strongest. Forward genetic screens are relatively easy, again because of the large number of progeny derived and the speed with which they can be assessed. Morpholino technology makes for a rapid and relatively inexpensive tool for the study of gene function for up to 7 to 10 days of life. Macrophages are the first phagocytes, and indeed the first immune cells, to appear in zebrafish development (although the precise timing of neutrophil development is not certain). Although the kidney is the site of hematopoiesis in the adult fish, the predecessors of the stem cells responsible for definitive hematopoiesis first appear in a region of the trunk called the aorta-gonad-mesonephros (AGM) at about 24 hpf, whence they move to another temporary hematopoietic site in the ventral tail called the caudal hematopoietic tissue. Some studies of embryonic macrophages have taken advantage of neutral red accumulation in macrophages, but this dye is toxic within hours of administration. Melanomacrophages are a subset of macrophages found in fish, amphibians, and reptiles. They are most commonly found as a part of melanomacrophage centers (MMCs) in the spleen, liver, and sometimes kidney, but are also seen singly. The chapter highlights the work done thus far with the various pathogen species.
General anatomy and location of myelopoiesis during progressive stages of development. (A–D) Line drawings based on sketches from Kimmel et al. (1995) . Path of hematopoietic cells as reported in Herbomel et al. (1999) and Murayama et al. (2006) . (A) Path of embryonic macrophages from lateral mesoderm to anterior yolk. (B) Before the onset of circulation, embryonic macrophages have spread over the yolk and begun to infiltrate the brain. (C) Definitive hematopoiesis begins in the aorta-gonad-mesonephros (AGM), but hematopoietic precursors soon migrate to the caudal hematopoietic tissue (CHT). (D) By 4 days postfertilization, hematopoiesis is taking place in the CHT, but hematopoietic cells are also transferring to the thymus and kidney. (E) Location of organs important to hematopoiesis and infection in the adult.
Examples of macrophages and neutrophils visible with DIC microscopy during embryonic and larval development. (A–C) Embryonic macrophages located near caudal vein (ventral is up), with muscle tissue nearby. (A) Early embryonic macrophage at yolk surface, ~30 hpf, just before the onset of circulation. (Scale bar, 20 μm; all panels, same scale.) (B) More mature embryonic macrophage in yolk circulation valley at ~48 hpf. (C) Two embryonic macrophages in yolk circulation valley, with many cellular processes and connected by a “tether.” (D–F) Neutrophils located just superficial to caudal hematopoietic tissue. Note the more slender proportions and plentiful cytoplasmic granules.
1. Agius, C.,, and R. J. Roberts. 2003. Melano-macrophage centres and their role in fish pathology. J. Fish Dis. 26: 499– 509.
2. Alliot, F.,, E. Lecain,, B. Grima, and, B. Pessac. 1991. Microglial progenitors with a high proliferative potential in the embryonic and adult mouse brain. Proc. Natl. Acad. Sci. USA 88: 1541– 1545.
3. Amores, A.,, A. Force,, Y. L. Yan,, L. Joly,, C. Amemiya,, A. Fritz,, R. K. Ho,, J. Langeland,, V. Prince,, Y. L. Wang,, M. Westerfield,, M. Ekker, and, J. H. Postlethwait. 1998. Zebrafish hox clusters and vertebrate genome evolution. Science 282: 1711– 1714.
4. Barreda, D. R.,, N. F. Neumann, and, M. Belosevic. 2000. Flow cytometric analysis of PKH26-labeled goldfish kidney-derived macrophages. Dev. Comp. Immunol. 24: 395– 406.
5. Bates, C. S.,, C. Toukoki,, M. N. Neely, and, Z. Eichenbaum. 2005. Characterization of MtsR, a new metal regulator in group A streptococcus, involved in iron acquisition and virulence. Infect. Immun. 73: 5743– 5753.
6. Belcourt, D. R.,, C. Lazure, and, H. P. Bennett. 1993. Isolation and primary structure of the three major forms of granulin-like peptides from hematopoietic tissues of a teleost fish (Cyprinus carpio). J. Biol. Chem. 268: 9230– 9237.
7. Bennett, C. M.,, J. P. Kanki,, J. Rhodes,, T. X. Liu,, B. H. Paw,, M. W. Kieran,, D. M. Langenau,, A. Delahaye-Brown,, L. I. Zon,, M. D. Fleming, and, A. T. Look. 2001. Myelopoiesis in the zebrafish, Danio rerio. Blood 98: 643– 651.
8. Berthet, F. X.,, M. Lagranderie,, P. Gounon,, C. Laurent-Winter,, D. Ensergueix,, P. Chavarot,, F. Thouron,, E. Maranghi,, V. Pelicic,, D. Portnoi,, G. Marchal, and, B. Gicquel. 1998. Attenuation of virulence by disruption of the Myco-bacterium tuberculosis erp gene. Science 282: 759– 762.
9. Blaser, H.,, M. Reichman-Fried,, I. Castanon,, K. Dumstrei,, F. L. Marlow,, K. Kawakami,, L. Solnica-Krezel,, C. P. Heisenberg, and, E. Raz. 2006. Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow. Dev. Cell 11: 613– 627.
10. Brannon, M. K.,, J. M. Davis,, J. R. Mathias,, C. J. Hall,, J. C. Emerson,, P. S. Crosier,, A. Huttenlocher,, L. Ramakrishnan, and, S. M. Moskowitz. 2009. Pseudomonas aeruginosa type III secretion system interacts with phagocytes to modulate systemic infection of zebrafish embryos. Cell. Microbiol. 11: 755– 768.
11. Brenot, A.,, K. Y. King,, B. Janowiak,, O. Griffith, and, M. G. Caparon. 2004. Contribution of glutathione peroxidase to the virulence of Streptococcus pyogenes. Infect. Immun. 72: 408– 413.
12. Broussard, G. W.,, and D. G. Ennis. 2007. Mycobacterium marinum produces long-term chronic infections in medaka: a new animal model for studying human tuberculosis. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 145: 45– 54.
13. Brown, S. B.,, C. S. Tucker,, C. Ford,, Y. Lee,, D. R. Dunbar, and, J. J. Mullins. 2007. Class III antiarrhythmic methane-sulfonanilides inhibit leukocyte recruitment in zebrafish. J. Leukoc. Biol. 82: 79– 84.
14. Cadieux, B.,, B. P. Chitramuthu,, D. Baranowski, and, H. P. Bennett. 2005. The zebrafish progranulin gene family and antisense transcripts. BMC Genomics 6: 156.
15. Chen, S. C.,, A. Adams,, K. D. Thompson, and, R. H. Richards. 1998. Electron microscope studies of the in vitro phagocytosis of Mycobacterium spp. by rainbow trout Oncorhynchus mykiss head kidney macrophages. Dis. Aquat. Organ. 32: 99– 110.
16. Chiang, C. Y.,, and L. W. Riley. 2005. Exogenous reinfection in tuberculosis. Lancet Infect. Dis. 5: 629– 636.
17. Chong, S. W.,, L. M. Nguyet,, Y. J. Jiang, and, V. Korzh. 2007. The chemokine, Sdf-1, and its receptor, Cxcr4, are required for formation of muscle in zebrafish. BMC Dev. Biol. 7: 54.
18. Clay, H.,, J. M. Davis,, D. Beery,, A. Huttenlocher,, S. E. Lyons, and, L. Ramakrishnan. 2007. Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host Microbe 2: 29– 39.
19. Cooper, A. M.,, D. K. Dalton,, T. A. Stewart,, J. P. Griffin,, D. G. Russell, and, I. M. Orme. 1993. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med. 178: 2243– 2247.
20. Cooper, M. S.,, D. P. Szeto,, G. Sommers-Herivel,, J. Topczewski,, L. Solnica-Krezel,, H. C. Kang,, I. Johnson, and, D. Kimelman. 2005. Visualizing morphogenesis in transgenic zebrafish embryos using BODIPY TR methyl ester dye as a vital counterstain for GFP. Dev. Dyn. 232: 359– 368.
21. Cosma, C. L.,, O. Humbert, and, L. Ramakrishnan. 2004. Superinfecting mycobacteria home to established tuberculous granulomas. Nat. Immunol. 5: 828– 835.
22. Cosma, C. L.,, K. Klein,, R. Kim,, D. Beery, and, L. Ramakrishnan. 2006. Mycobacterium marinum Erp is a virulence determinant required for cell wall integrity and intracellular survival. Infect. Immun. 74: 3125– 3133.
23. Cosma, C. L.,, D. R. Sherman, and, L. Ramakrishnan. 2003. The secret lives of the pathogenic mycobacteria. Annu. Rev. Microbiol. 57: 641– 676.
24. Crosnier, C.,, N. Vargesson,, S. Gschmeissner,, L. Ariza-McNaughton,, A. Morrison, and, J. Lewis. 2005. Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 132: 1093– 1104.
25. Dai, X. M.,, G. R. Ryan,, A. J. Hapel,, M. G. Dominguez,, R. G. Russell,, S. Kapp,, V. Sylvestre, and, E. R. Stanley. 2002. Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99: 111– 120.
26. Dakic, A.,, Q. X. Shao,, A. D’Amico,, M. O’Keeffe,, W. F. Chen,, K. Shortman, and, L. Wu. 2004. Development of the dendritic cell system during mouse ontogeny. J. Immunol. 172: 1018– 1027.
27. Dambly-Chaudiere, C.,, N. Cubedo, and, A. Ghysen. 2007. Control of cell migration in the development of the posterior lateral line: antagonistic interactions between the chemokine receptors CXCR4 and CXCR7/RDC1. BMC Dev. Biol. 7: 23.
28. Danilova, N.,, J. Bussmann,, K. Jekosch, and, L. A. Steiner. 2005. The immunoglobulin heavy-chain locus in zebrafish: identification and expression of a previously unknown iso-type, immunoglobulin Z. Nat. Immunol. 6: 295– 302.
29. Dannenberg, A. M., Jr. 1993. Immunopathogenesis of pulmonary tuberculosis. Hosp. Pract. 28: 51– 58.
30. Davis, J. M.,, H. Clay,, J. L. Lewis,, N. Ghori,, P. Herbomel, and, L. Ramakrishnan. 2002. Real-time visualization of Mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity 17: 693– 702.
31. Davis, J. M.,, and L. Ramakrishnan. 2009. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136: 37– 49.
32. Ellis, A. E.,, and M. De Sousa. 1974. Phylogeny of the lymphoid system. I. A study of the fate of circulating lymphocytes in plaice. Eur. J. Immunol. 4: 338– 343.
33. Ellis, A. E.,, A. L. S. Munro, and, R. J. Roberts. 1976. Defence mechanisms in fish: fate of intraperitoneally introduced carbon in the plaice (Pleuronectes platessa). J. Fish Biol. 8: 67– 78.
34. Flynn, J. L.,, M. M. Goldstein,, J. Chan,, K. J. Triebold,, K. Pfeffer,, C. J. Lowenstein,, R. Schreiber,, T. W. Mak, and, B. R. Bloom. 1995. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2: 561– 572.
35. Hall, C.,, M. V. Flores,, T. Storm,, K. Crosier, and, P. Crosier. 2007. The zebrafish lysozyme C promoter drives myeloidspecific expression in transgenic fish. BMC Dev. Biol. 7: 42.
36. Hamm, E. E.,, D. E. Voth, and, J. D. Ballard. 2006. Identification of Clostridium difficile toxin B cardiotoxicity using a zebrafish embryo model of intoxication. Proc. Natl. Acad. Sci. USA 103: 14176– 14181.
37. Hammerschmidt, M.,, and A. P. McMahon. 1998. The effect of pertussis toxin on zebrafish development: a possible role for inhibitory G-proteins in hedgehog signaling. Dev. Biol. 194: 166– 171.
38. Hanington, P. C.,, D. R. Barreda, and, M. Belosevic. 2006. A novel hematopoietic granulin induces proliferation of gold-fish ( Carassius auratus L.) macrophages. J. Biol. Chem. 281: 9963– 9970.
39. Haugarvoll, E.,, J. Thorsen,, M. Laane,, Q. Huang, and, E. O. Koppang. 2006. Melanogenesis and evidence for melanosome transport to the plasma membrane in a CD83 teleost leukocyte cell line. Pigment Cell Res. 19: 214– 225.
40. Herbomel, P.,, B. Thisse, and, C. Thisse. 1999. Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126: 3735– 3745.
41. Herbomel, P.,, B. Thisse, and, C. Thisse. 2001. Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev. Biol. 238: 274– 288.
42. Herraez, M. P.,, and A. G. Zapata. 1991. Structural characterization of the melano-macrophage centres (MMC) of gold-fish Carassius auratus. Eur. J. Morphol. 29: 89– 102.
43. Honer zu Bentrup, K.,, and D. G. Russell. 2001. Mycobacterial persistence: adaptation to a changing environment. Trends Microbiol. 9: 597– 605.
44. Hsu, K.,, D. Traver,, J. L. Kutok,, A. Hagen,, T. X. Liu,, B. H. Paw,, J. Rhodes,, J. N. Berman,, L. I. Zon,, J. P. Kanki, and, A. T. Look. 2004. The pu.1 promoter drives myeloid gene expression in zebrafish. Blood 104: 1291– 1297.
45. Hung, D. T.,, E. A. Shakhnovich,, E. Pierson, and, J. J. Mekalanos. 2005. Small-molecule inhibitor of Vibrio cholerae virulence and intestinal colonization. Science 310: 670– 674.
46. Igawa, D.,, M. Sakai, and, R. Savan. 2006. An unexpected discovery of two interferon gamma-like genes along with interleukin (IL)-22 and -26 from teleost: IL-22 and -26 genes have been described for the first time outside mammals. Mol. Immunol. 43: 999– 1009.
47. Isogai, S.,, M. Horiguchi, and, B. M. Weinstein. 2001. The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev. Biol. 230: 278– 301.
48. Jault, C.,, L. Pichon, and, J. Chluba. 2004. Toll-like receptor gene family and TIR-domain adapters in Danio rerio. Mol. Immunol. 40: 759– 771.
49. Jozefowicz, C.,, J. McClintock, and, V. Prince. 2003. The fates of zebrafish Hox gene duplicates. J. Struct. Funct. Genomics 3: 185– 194.
50. Kemenade, B.,, A. Groeneveld,, B. Rens, and, J. Rombout. 1994. Characterization of macrophages and neutrophilic granulocytes from the pronephros of carp (Cyprinus carpio). J. Exp. Biol. 187: 143– 158.
51. Kimmel, C. B.,, W. W. Ballard,, S. R. Kimmel,, B. Ullmann, and, T. F. Schilling. 1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203: 253– 310.
52. Knaut, H.,, C. Werz,, R. Geisler, and, C. Nusslein-Volhard. 2003. A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature 421: 279– 282.
53. Kuchler, A. M.,, E. Gjini,, J. Peterson-Maduro,, B. Cancilla,, H. Wolburg, and, S. Schulte-Merker. 2006. Development of the zebrafish lymphatic system requires VEGFC signaling. Curr. Biol. 16: 1244– 1248.
54. Langenau, D. M.,, A. A. Ferrando,, D. Traver,, J. L. Kutok,, J. P. Hezel,, J. P. Kanki,, L. I. Zon,, A. T. Look, and, N. S. Trede. 2004. In vivo tracking of T cell development, ablation, and engraftment in transgenic zebrafish. Proc. Natl. Acad. Sci. USA 101: 7369– 7374.
55. Langenau, D. M.,, D. Traver,, A. A. Ferrando,, J. L. Kutok,, J. C. Aster,, J. P. Kanki,, S. Lin,, E. Prochownik,, N. S. Trede,, L. I. Zon, and, A. T. Look. 2003. Myc-induced T cell leukemia in transgenic zebrafish. Science 299: 887– 890.
56. Lawson, N. D.,, and B. M. Weinstein. 2002. In vivo imaging of embryonic vascular development using transgenic zebra-fish. Dev. Biol. 248: 307– 318.
57. Le Guyader, D.,, M. J. Redd,, E. Colucci-Guyon,, E. Murayama,, K. Kissa,, V. Briolat,, E. Mordelet,, A. Zapata,, H. Shinomiya, and, P. Herbomel. 2008. Origins and unconventional behavior of neutrophils in developing zebrafish. Blood 111: 132– 141.
58. Li, J.,, D. R. Barreda,, Y. A. Zhang,, H. Boshra,, A. E. Gelman,, S. Lapatra,, L. Tort, and, J. O. Sunyer. 2006. B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat. Immunol. 7: 1116– 1124.
59. Lin, B.,, S. Chen,, Z. Cao,, Y. Lin,, D. Mo,, H. Zhang,, J. Gu,, M. Dong,, Z. Liu, and, A. Xu. 2007. Acute phase response in zebrafish upon Aeromonas salmonicida and Staphylococcus aureus infection: striking similarities and obvious differences with mammals. Mol. Immunol. 44: 295– 301.
60. Linehan, S. A.,, and D. W. Holden. 2003. The interplay between Salmonella typhimurium and its macrophage host—what can it teach us about innate immunity? Immunol. Lett. 85: 183– 192.
61. Lowe, B. A.,, J. D. Miller, and, M. N. Neely. 2007. Analysis of the polysaccharide capsule of the systemic pathogen Streptococcus iniae and its implications in virulence. Infect. Immun. 75: 1255– 1264.
62. Mathias, J. R.,, M. E. Dodd,, K. B. Walters,, J. Rhodes,, J. P. Kanki,, A. T. Look, and, A. Huttenlocher. 2007. Live imaging of chronic inflammation caused by mutation of zebra-fish Hai1. J. Cell Sci. 120: 3372– 3383.
63. Mathias, J. R.,, B. J. Perrin,, T. X. Liu,, J. Kanki,, A. T. Look, and, A. Huttenlocher. 2006. Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J. Leukoc. Biol. 80: 1281– 1288.
64. Meijer, A. H.,, S. F. Gabby Krens,, I. A. Medina Rodriguez,, S. He,, W. Bitter,, B. Ewa Snaar-Jagalska, and, H. P. Spaink. 2004. Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish. Mol. Immunol. 40: 773– 783.
65. Meijer, A. H.,, A. M. van der Sar,, C. Cunha,, G. E. Lamers,, M. A. Laplante,, H. Kikuta,, W. Bitter,, T. S. Becker, and, H. P. Spaink. 2008. Identification and real-time imaging of a myc-expressing neutrophil population involved in inflammation and mycobacterial granuloma formation in zebrafish. Dev. Comp. Immunol. 32: 36– 49.
66. Miller, J. D.,, and M. N. Neely. 2005. Large-scale screen highlights the importance of capsule for virulence in the zoonotic pathogen Streptococcus iniae. Infect. Immun. 73: 921– 934.
67. Miller, J. D.,, and M. N. Neely. 2004. Zebrafish as a model host for streptococcal pathogenesis. Acta Trop. 91: 53– 68.
68. Miyasaka, N.,, H. Knaut, and, Y. Yoshihara. 2007. Cxcl12/Cxcr4 chemokine signaling is required for placode assembly and sensory axon pathfinding in the zebrafish olfactory system. Development 134: 2459– 2468.
69. Montanez, G. E.,, M. N. Neely, and, Z. Eichenbaum. 2005. The streptococcal iron uptake (Siu) transporter is required for iron uptake and virulence in a zebrafish infection model. Microbiology 151: 3749– 3757.
70. Murayama, E.,, K. Kissa,, A. Zapata,, E. Mordelet,, V. Briolat,, H. F. Lin,, R. I. Handin, and, P. Herbomel. 2006. Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 25: 963– 975.
71. Nasevicius, A.,, and S. C. Ekker. 2000. Effective targeted gene “knockdown” in zebrafish. Nat. Genet. 26: 216– 220.
72. Nayak, A. S.,, C. R. Lage, and, C. H. Kim. 2007. Effects of low concentrations of arsenic on the innate immune system of the zebrafish (Danio rerio). Toxicol. Sci. 98: 118– 124.
73. Neely, M. N.,, J. D. Pfeifer, and, M. Caparon. 2002. Streptococcus-zebrafish model of bacterial pathogenesis. Infect. Immun. 70: 3904– 3914.
74. Neumann, N. F.,, D. R. Barreda, and, M. Belosevic. 2000. Generation and functional analysis of distinct macrophage sub-populations from goldfish ( Carassius auratus L.) kidney leukocyte cultures. Fish Shellfish Immunol. 10: 1– 20.
75. Neumann, N. F.,, J. L. Stafford,, D. Barreda,, A. J. Ainsworth, and, M. Belosevic. 2001. Antimicrobial mechanisms of fish phagocytes and their role in host defense. Dev. Comp. Immunol. 25: 807– 825.
76. Novoa, B.,, A. Romero,, V. Mulero,, I. Rodriguez,, I. Fernandez, and, A. Figueras. 2006. Zebrafish (Danio rerio) as a model for the study of vaccination against viral haemorrhagic septicemia virus (VHSV). Vaccine 24: 5806– 5816.
77. Ogura, Y.,, L. Saab,, F. F. Chen,, A. Benito,, N. Inohara, and, G. Nunez. 2003. Genetic variation and activity of mouse Nod2, a susceptibility gene for Crohn’s disease. Genomics 81: 369– 377.
78. Ohta, Y.,, E. Landis,, T. Boulay,, R. B. Phillips,, B. Collet,, C. J. Secombes,, M. F. Flajnik, and, J. D. Hansen. 2004. Homologs of CD83 from elasmobranch and teleost fish. J. Immunol. 173: 4553– 4560.
79. Palic, D.,, C. B. Andreasen,, J. Ostojic,, R. M. Tell, and, J. A. Roth. 2007. Zebrafish (Danio rerio) whole kidney assays to measure neutrophil extracellular trap release and degranulation of primary granules. J. Immunol. Methods 319: 87– 97.
80. Palic, D.,, J. Ostojic,, C. B. Andreasen, and, J. A. Roth. 2007. Fish cast NETs: neutrophil extracellular traps are released from fish neutrophils. Dev. Comp. Immunol. 31: 805– 816.
81. Parichy, D. M.,, and J. M. Turner. 2003. Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development 130: 817– 833.
82. Patton, E. E.,, and L. I. Zon. 2001. The art and design of genetic screens: zebrafish. Nat. Rev. Genet. 2: 956– 966.
83. Peatman, E.,, B. Bao,, P. Baoprasertkul, and, Z. Liu. 2005. In silico identification and expression analysis of 12 novel CC chemokines in catfish. Immunogenetics 57: 409– 419.
84. Peatman, E.,, B. Bao,, X. Peng,, P. Baoprasertkul,, Y. Brady, and, Z. Liu. 2006. Catfish CC chemokines: genomic clustering, duplications, and expression after bacterial infection with Edwardsiella ictaluri. Mol. Genet. Genomics 275: 297– 309.
85. Peatman, E.,, and Z. Liu. 2006. CC chemokines in zebrafish: evidence for extensive intrachromosomal gene duplications. Genomics 88: 381– 385.
86. Peterson, R. T.,, S. Y. Shaw,, T. A. Peterson,, D. J. Milan,, T. P. Zhong,, S. L. Schreiber,, C. A. MacRae, and, M. C. Fishman. 2004. Chemical suppression of a genetic mutation in a zebrafish model of aortic coarctation. Nat. Biotechnol. 22: 595– 599.
87. Phelan, P. E.,, M. T. Mellon, and, C. H. Kim. 2005. Functional characterization of full-length TLR3, IRAK-4, and TRAF6 in zebrafish (Danio rerio). Mol. Immunol. 42: 1057– 1071.
88. Phelan, P. E.,, M. E. Pressley,, P. E. Witten,, M. T. Mellon,, S. Blake, and, C. H. Kim. 2005. Characterization of snake-head rhabdovirus infection in zebrafish (Danio rerio). J. Virol. 79: 1842– 1852.
89. Phelps, H. A.,, and M. N. Neely. 2007. SalY of Streptococcus pyogenes lantibiotic locus is required for full virulence and intracellular survival in macrophages. Infect. Immun. 75: 4541– 4551.
90. Pressley, M. E.,, P. E. Phelan III,, P. E. Witten,, M. T. Mellon, and, C. H. Kim. 2005. Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Dev. Comp. Immunol. 29: 501– 513.
91. Redd, M. J.,, G. Kelly,, G. Dunn,, M. Way, and, P. Martin. 2006. Imaging macrophage chemotaxis in vivo: studies of microtubule function in zebrafish wound inflammation. Cell. Motil. Cytoskelet. 63: 415– 422.
92. Renshaw, S. A.,, C. A. Loynes,, D. M. Trushell,, S. Elworthy,, P. W. Ingham, and, M. K. Whyte. 2006. A transgenic zebrafish model of neutrophilic inflammation. Blood 108: 3976– 3978.
93. Rodriguez, A.,, M. A. Esteban, and, J. Meseguer. 2003. A mannose-receptor is possibly involved in the phagocytosis of Saccharomyces cerevisiae by seabream ( Sparus aurata L.) leucocytes. Fish Shellfish Immunol. 14: 375– 388.
94. Sanders, G. E.,, W. N. Batts, and, J. R. Winton. 2003. Susceptibility of zebrafish (Danio rerio) to a model pathogen, spring viremia of carp virus. Comp. Med. 53: 514– 521.
95. Santos, F.,, G. MacDonald,, E. W. Rubel, and, D. W. Raible. 2006. Lateral line hair cell maturation is a determinant of aminoglycoside susceptibility in zebrafish (Danio rerio). Hear. Res. 213: 25– 33.
96. Schraml, B.,, M. A. Baker, and, B. D. Reilly. 2006. A complement receptor for opsonized immune complexes on erythrocytes from Oncorhynchus mykiss but not Ictalarus punctatus. Mol. Immunol. 43: 1595– 1603.
97. Sichel, G.,, M. Scalia,, F. Mondio, and, C. Corsaro. 1997. The amphibian Kupffer cells build and demolish melanosomes: an ultrastructural point of view. Pigment Cell Res. 10: 271– 287.
98. Skromne, I.,, and V. E. Prince. 2008. Current perspectives in zebrafish reverse genetics: moving forward. Dev. Dyn. 237: 861– 882.
99. Soanes, K. H.,, K. Figuereido,, R. C. Richards,, N. R. Mattatall, and, K. V. Ewart. 2004. Sequence and expression of C-type lectin receptors in Atlantic salmon (Salmo salar). Immunogenetics 56: 572– 584.
100. Sorensen, K. K.,, O. K. Tollersrud,, G. Evjen, and, B. Smedsrod. 2001. Mannose-receptor-mediated clearance of lysosomal alpha-mannosidase in scavenger endothelium of cod endocardium. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 129: 615– 630.
101. Sorokin, S. P.,, and R. F. Hoyt, Jr. 1987. Pure population of nonmonocyte derived macrophages arising in organ cultures of embryonic rat lungs. Anat. Rec. 217: 35– 52.
102. Stafford, J.,, N. F. Neumann, and, M. Belosevic. 1999. Inhibition of macrophage activity by mitogen-induced goldfish leukocyte deactivating factor. Dev. Comp. Immunol. 23: 585– 596.
103. Stafford, J. L.,, and M. Belosevic. 2003. Transferrin and the innate immune response of fish: identification of a novel mechanism of macrophage activation. Dev. Comp. Immunol. 27: 539– 554.
104. Stafford, J. L.,, N. F. Neumann, and, M. Belosevic. 2001. Products of proteolytic cleavage of transferrin induce nitric oxide response of goldfish macrophages. Dev. Comp. Immunol. 25: 101– 115.
105. Stamm, L. M.,, J. H. Morisaki,, L. Y. Gao,, R. L. Jeng,, K. L. McDonald,, R. Roth,, S. Takeshita,, J. Heuser,, M. D. Welch, and, E. J. Brown. 2003. Mycobacterium marinum escapes from phagosomes and is propelled by actin-based motility. J. Exp. Med. 198: 1361– 1368.
106. Swaim, L. E.,, L. E. Connolly,, H. E. Volkman,, O. Humbert,, D. E. Born, and, L. Ramakrishnan. 2006. Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infect. Immun. 74: 6108– 6117.
107. Traver, D.,, P. Herbomel,, E. E. Patton,, R. D. Murphey,, J. A. Yoder,, G. W. Litman,, A. Catic,, C. T. Amemiya,, L. I. Zon, and, N. S. Trede. 2003. The zebrafish as a model organism to study development of the immune system. Adv. Immunol. 81: 253– 330.
108. Trede, N. S.,, D. M. Langenau,, D. Traver,, A. T. Look, and, L. I. Zon. 2004. The use of zebrafish to understand immunity. Immunity 20: 367– 379.
109. van der Sar, A. M.,, R. J. Musters,, F. J. van Eeden,, B. J. Appelmelk,, C. M. Vandenbroucke-Grauls, and, W. Bitter. 2003. Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections. Cell. Microbiol. 5: 601– 611.
110. van der Sar, A. M.,, O. W. Stockhammer,, C. van der Laan,, H. P. Spaink,, W. Bitter, and, A. H. Meijer. 2006. MyD88 innate immune function in a zebrafish embryo infection model. Infect. Immun. 74: 2436– 2441.
111. van der Wel, N.,, D. Hava,, D. Houben,, D. Fluitsma,, M. van Zon,, J. Pierson,, M. Brenner, and, P. J. Peters. 2007. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129: 1287– 1298.
112. Vigliano, F. A.,, R. Bermudez,, M. I. Quiroga, and, J. M. Nieto. 2006. Evidence for melano-macrophage centres of teleost as evolutionary precursors of germinal centres of higher vertebrates: an immunohistochemical study. Fish Shellfish Immunol. 21: 467– 471.
113. Volkman, H. E.,, H. Clay,, D. Beery,, J. C. Chang,, D. R. Sherman, and, L. Ramakrishnan. 2004. Tuberculous granuloma formation is enhanced by a mycobacterium virulence determinant. PLoS Biol. 2: 1946– 1956.
114. Voth, D. E.,, E. E. Hamm,, L. G. Nguyen,, A. E. Tucker,, I. I. Salles,, W. Ortiz-Leduc, and, J. D. Ballard. 2005. Bacillus anthracis oedema toxin as a cause of tissue necrosis and cell type-specific cytotoxicity. Cell. Microbiol. 7: 1139– 1149.
115. Wakae, K.,, B. G. Magor,, H. Saunders,, H. Nagaoka,, A. Kawamura,, K. Kinoshita,, T. Honjo, and, M. Muramatsu. 2006. Evolution of class switch recombination function in fish activation-induced cytidine deaminase, AID. Int. Immunol. 18: 41– 47.
116. Wakamatsu, Y.,, S. Pristyazhnyuk,, M. Kinoshita,, M. Tanaka, and, K. Ozato. 2001. The see-through medaka: a fish model that is transparent throughout life. Proc. Natl. Acad. Sci. USA 98: 10046– 10050.
117. Weinholds, E.,, F. van Eeden,, M. Kosters,, J. Mudde,, R. H. A. Plasterk, and, E. Cuppen. 2003. Efficient target-selected mutagenesis in zebrafish. Genome Res. 13: 2700– 2707.
118. Westerfield, M. 2000. The Zebrafish Book. A Guide for the Use of Zebrafish (Danio rerio). University of Oregon Press, Eugene, OR.
119. White, R. M.,, A. Sessa,, C. Burke,, T. Bowman,, J. LeBlanc,, C. Ceol,, C. Bourque,, M. Dovey,, W. Goessling,, C. E. Burns, and, L. I. Zon. 2008. Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2: 183– 189.
120. Willett, C. E.,, A. Cortes,, A. Zuasti, and, A. G. Zapata. 1999. Early hematopoiesis and developing lymphoid organs in the zebrafish. Dev. Dyn. 214: 323– 336.
121. Yaniv, K.,, S. Isogai,, D. Castranova,, L. Dye,, J. Hitomi, and, B. M. Weinstein. 2006. Live imaging of lymphatic development in the zebrafish. Nat. Med. 12: 711– 716.
122. Zuasti, A.,, J. R. Jara,, C. Ferrer, and, F. Solano. 1989. Occurrence of melanin granules and melanosynthesis in the kidney of Sparus auratus. Pigment Cell Res. 2: 93– 99.

References: V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V.