Advertisement

Innate Immune System of the Zebrafish, Danio rerio

  • Con Sullivan
  • Carol H. Kim
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 21)

There has been a revolution in immunology in recent years that has transformed the paradigmatic underpinnings of vertebrate immunology to include the innate immune response. The utilization of basally diverging model systems, like the zebrafish, provides particular insight into the origins and evolution of vertebrate immunity. Investigations aimed at exposing the breadth and complexity of innate immunity using the zebrafish model system have uncovered a broad spectrum of mechanisms, both novel and conserved, that add depth to our understanding of how the immune system functions. Of particular significance is the fact that, during the first 4–6 weeks of development, the zebrafish relies upon innate immunity as its sole mechanism of defense. This unique characteristic, combined with the zebrafish model's inherent advantages including high fecundity, external development, and optical transparency during early development, make the zebrafish a particularly attractive model of study. The establishment of bacterial and viral infectious disease models such as Edwardsiella tarda and snakehead rhabdovirus, respectively, as well as the addition of a wide range of reagents and techniques, including robust forward and reverse genetics approaches, have facilitated the zebrafish model's usage to study of a variety of innate immunity questions. Close examination of the zebrafish's innate immune system reveals a strong degree of sequence conservation in many of areas of study, including but not limited to pattern recognition receptors like the Toll-like receptors, their pathway components, and a variety of cytokines. Studies are currently underway to determine whether such sequence homology equates to functional homology. In addition, a variety of zebrafish genes encoding proteins of unique function are currently under study, including assorted lectins and novel immune type receptors. Close examination of these genes may provide needed insight into the evolutionary history of immunity in vertebrates.

Keywords

Natural Killer Cell Danio Rerio Infectious Hematopoietic Necrosis Virus Morpholino Oligo Infectious Pancreatic Necrosis Virus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agrawal A, Eastman QM, Schatz DG (1998) Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394:744–751PubMedGoogle Scholar
  2. Ahmed H, Du SJ, O’Leary N, Vasta GR (2004) Biochemical and molecular characterization of galectins from zebrafish (Danio rerio): notochord-specific expression of a prototype galectin during early embryogenesis. Glycobiology 14:219–232PubMedGoogle Scholar
  3. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511PubMedGoogle Scholar
  4. Akira S, Takeda K, Kaisho T (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2:675–680PubMedGoogle Scholar
  5. Akira S, Yamamoto M, Takeda K (2003) Role of adapters in Toll-like receptor signalling. Biochem Soc Trans 31:637–642PubMedGoogle Scholar
  6. Alder MN, Rogozin IB, Iyer LM, Glazko GV, Cooper MD, Pancer Z (2005) Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 310:1970–1973PubMedGoogle Scholar
  7. Altmann SM, Mellon MT, Distel DL, Kim CH (2003) Molecular and functional analysis of an interferon gene from the zebrafish, Danio rerio. J Virol 77:1992–2002PubMedGoogle Scholar
  8. Anderson KV, Nusslein-Volhard C (1984a) Genetic analysis of dorsal–ventral embryonic pattern in Drosophila. In: Malacinski GM, Bryant SV (eds) Pattern formation: a primer in developmental biology. Macmillan, New York, pp 269–289Google Scholar
  9. Anderson KV, Nusslein-Volhard C (1984b) Information for the dorsal–ventral pattern of the Drosophila embryo is stored as maternal mRNA. Nature 311:223–227PubMedGoogle Scholar
  10. Anderson KV, Bokla L, Nusslein-Volhard C (1985a) Establishment of dorsal–ventral polarity in the Drosophila embryo: the induction of polarity by the Toll gene product. Cell 42:791–798PubMedGoogle Scholar
  11. Anderson KV, Jurgens G, Nusslein-Volhard C (1985b) Establishment of dorsal–ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 42:779–789PubMedGoogle Scholar
  12. Baoprasertkul P, He C, Peatman E, Zhang S, Li P, Liu Z (2005) Constitutive expression of three novel catfish CXC chemokines: homeostatic chemokines in teleost fish. Mol Immunol 42:1355–1366PubMedGoogle Scholar
  13. Barbazuk WB, Korf I, Kadavi C, Heyen J, Tate S, Wun E, Bedell JA, McPherson JD, Johnson SL (2000) The syntenic relationship of the zebrafish and human genomes. Genome Res 10:1351–1358PubMedGoogle Scholar
  14. Barondes SH, Cooper DN, Gitt MA, Leffler H (1994) Galectins. Structure and function of a large family of animal lectins. J Biol Chem 269:20807–20810PubMedGoogle Scholar
  15. Bei JX, Suetake H, Araki K, Kikuchi K, Yoshiura Y, Lin HR, Suzuki Y (2006) Two interleukin (IL)-15 homologues in fish from two distinct origins. Mol Immunol 43:860–869PubMedGoogle Scholar
  16. Bennett CM, Kanki JP, Rhodes J, Liu TX, Paw BH, Kieran MW, Langenau DM, Delahaye-Brown A, Zon LI, Fleming MD, Look AT (2001) Myelopoiesis in the zebrafish, Danio rerio. Blood 98:643–651PubMedGoogle Scholar
  17. Beutler B (2004) Inferences, questions and possibilities in Toll-like receptor signalling. Nature 430:257–263PubMedGoogle Scholar
  18. Bin LH, Xu LG, Shu HB (2003) TIRP, a novel Toll/interleukin-1 receptor (TIR) domain-containing adapter protein involved in TIR signaling. J Biol Chem 278:24526–24532PubMedGoogle Scholar
  19. Burnet FM (1959) The clonal selection theory of acquired immunity. Vanderbilt University Press, NashvilleGoogle Scholar
  20. Carlson RL, Evans DL, Graves SS (1985) Nonspecific cytotoxic cells in fish (Ictalurus punctatus). V. Metabolic requirements of lysis. Dev Comp Immunol 9:271–280PubMedGoogle Scholar
  21. Couillault C, Pujol N, Reboul J, Sabatier L, Guichou JF, Kohara Y, Ewbank JJ (2004) TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat Immunol 5:488–494PubMedGoogle Scholar
  22. Danilova N, Steiner LA (2002) B cells develop in the zebrafish pancreas. Proc Natl Acad Sci USA 99:13711–13716PubMedGoogle Scholar
  23. Danilova N, Hohman VS, Sacher F, Ota T, Willett CE, Steiner LA (2004) T cells and the thymus in developing zebrafish. Dev Comp Immunol 28:755–767PubMedGoogle Scholar
  24. Davis DM (2002) Assembly of the immunological synapse for T cells and NK cells. Trends Immunol 23:356–363PubMedGoogle Scholar
  25. Davis JM, Clay H, Lewis JL, Ghori N, Herbomel P, Ramakrishnan L (2002) Real-time visualization of mycobacterium–macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity 17:693–702PubMedGoogle Scholar
  26. Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3:e314PubMedGoogle Scholar
  27. deKruif P (1926) Microbe hunters. Harcourt Brace, OrlandoGoogle Scholar
  28. Deng L, Wang C, Spencer E, Yang L, Braun A, You J, Slaughter C, Pickart C, Chen ZJ (2000) Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103:351–361PubMedGoogle Scholar
  29. Draper BW, Stock DW, Kimmel CB (2003) Zebrafish fgf24 functions with fgf8 to promote posterior mesodermal development. Development 130:4639–4654PubMedGoogle Scholar
  30. Evans DL, Carlson RL, Graves SS, Hogan KT (1984a) Nonspecific cytotoxic cells in fish (Ictalurus punctatus). IV. Target cell binding and recycling capacity. Dev Comp Immunol 8:823–833PubMedGoogle Scholar
  31. Evans DL, Graves SS, Cobb D, Dawe DL (1984b) Nonspecific cytotoxic cells in fish (Ictalurus punctatus). II. Parameters of target cell lysis and specificity. Dev Comp Immunol 8:303–312PubMedGoogle Scholar
  32. Evans DL, Hogan KT, Graves SS, Carlson RL Jr, Floyd E, Dawe DL (1984c) Nonspecific cytotoxic cells in fish (Ictalurus punctatus). III. Biophysical and biochemical properties affecting cytolysis. Dev Comp Immunol 8:599–610PubMedGoogle Scholar
  33. Evans DL, Smith EE Jr, Brown FE (1987) Nonspecific cytotoxic cells in fish (Ictalurus punctatus). VI. Flow cytometric analysis. Dev Comp Immunol 11:95–104PubMedGoogle Scholar
  34. Evans DL, Jaso-Friedmann L, Smith EE Jr, St John A, Koren HS, Harris DT (1988) Identification of a putative antigen receptor on fish nonspecific cytotoxic cells with monoclonal antibodies. J Immunol 141:324–332PubMedGoogle Scholar
  35. Evans DL, Leary JH 3rd, Jaso-Friedmann L (2001) Nonspecific cytotoxic cells and innate immunity: regulation by programmed cell death. Dev Comp Immunol 25:791–805PubMedGoogle Scholar
  36. Fishman MC (2001) Genomics. Zebrafish–the canonical vertebrate. Science 294:1290–1291PubMedGoogle Scholar
  37. Fitzgerald KA, Palsson-McDermott EM, Bowie AG, Jefferies CA, Mansell AS, Brady G, Brint E, Dunne A, Gray P, Harte MT, McMurray D, Smith DE, Sims JE, Bird TA, O’Neill LA (2001) Mal (MyD88-adapter-like) is required for Toll-like receptor-4 signal transduction. Nature 413:78–83PubMedGoogle Scholar
  38. Fitzgerald KA, Rowe DC, Barnes BJ, Caffrey DR, Visintin A, Latz E, Monks B, Pitha PM, Golenbock DT (2003) LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J Exp Med 198:1043–1055PubMedGoogle Scholar
  39. Geijtenbeek TB, Van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CM, Appelmelk B, Van Kooyk Y (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 197:7–17PubMedGoogle Scholar
  40. Graves SS, Evans DL, Cobb D, Dawe DL (1984) Nonspecific cytotoxic cells in fish (Ictalurus punctatus). I. Optimum requirements for target cell lysis. Dev Comp Immunol 8:293–302PubMedGoogle Scholar
  41. Harris DT, Jaso-Friedmann L, Devlin RB, Koren HS, Evans DL (1991) Identification of an evolutionarily conserved, function-associated molecule on human natural killer cells. Proc Natl Acad Sci USA 88:3009–3013PubMedGoogle Scholar
  42. Hawke NA, Yoder JA, Haire RN, Mueller MG, Litman RT, Miracle AL, Stuge T, Shen L, Miller N, Litman GW (2001) Extraordinary variation in a diversified family of immune-type receptor genes. Proc Natl Acad Sci USA 98:13832–13837PubMedGoogle Scholar
  43. Heguy A, Baldari CT, Macchia G, Telford JL, Melli M (1992) Amino acids conserved in interleukin-1 receptors (IL-1Rs) and the Drosophila toll protein are essential for IL-1R signal transduction. J Biol Chem 267:2605–2609PubMedGoogle Scholar
  44. Henneke P, Golenbock DT (2001) TIRAP: how Toll receptors fraternize. Nat Immunol 2:828–830PubMedGoogle Scholar
  45. Hermann AC, Millard PJ, Blake SL, Kim CH (2004) Development of a respiratory burst assay using zebrafish kidneys and embryos. J Immunol Methods 292:119–129PubMedGoogle Scholar
  46. Horng T, Barton GM, Medzhitov R (2001) TIRAP: an adapter molecule in the Toll signaling pathway. Nat Immunol 2:835–841PubMedGoogle Scholar
  47. Horng T, Barton GM, Flavell RA, Medzhitov R (2002) The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 420:329–333PubMedGoogle Scholar
  48. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S (1999) Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162:3749–3752PubMedGoogle Scholar
  49. Huising MO, Stet RJ, Savelkoul HF, Verburg-van Kemenade BM (2004) The molecular evolution of the interleukin-1 family of cytokines; IL-18 in teleost fish. Dev Comp Immunol 28:395–413PubMedGoogle Scholar
  50. Huising MO, Kruiswijk CP, Schijndel JE van, Savelkoul HF, Flik G, Verburg-van Kemenade BM (2005) Multiple and highly divergent IL-11 genes in teleost fish. Immunogenetics 57:432–443PubMedGoogle Scholar
  51. Igawa D, Sakai M, Savan R (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 43:999–1009PubMedGoogle Scholar
  52. Iliev DB, Roach JC, Mackenzie S, Planas JV, Goetz FW (2005) Endotoxin recognition: in fish or not in fish? FEBS Lett 579:6519–6528PubMedGoogle Scholar
  53. Janeway CA Jr (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54:1–13PubMedGoogle Scholar
  54. Jaso-Friedmann L, Leary JH 3rd, Evans DL (1993) Role of function-associated molecules in target cell lysis: analysis of rat adherent lymphokine-activated killer cells. Nat Immun 12:316–325PubMedGoogle Scholar
  55. Jaso-Friedmann L, Leary JH 3rd, Evans DL (1997) NCCRP-1: a novel receptor protein sequenced from teleost nonspecific cytotoxic cells. Mol Immunol 34:955–965PubMedGoogle Scholar
  56. Jaso-Friedmann L, Leary JH 3rd, Evans DL (2001) The non-specific cytotoxic cell receptor (NCCRP-1): molecular organization and signaling properties. Dev Comp Immunol 25:701–711PubMedGoogle Scholar
  57. Jault C, Pichon L, Chluba J (2004) Toll-like receptor gene family and TIR-domain adapters in Danio rerio. Mol Immunol 40:759–771PubMedGoogle Scholar
  58. Jong JL de, Zon LI (2005) Use of the zebrafish system to study primitive and definitive hematopoiesis. Annu Rev Genet 39:481–501PubMedGoogle Scholar
  59. Kanayama A, Seth RB, Sun L, Ea CK, Hong M, Shaito A, Chiu YH, Deng L, Chen ZJ (2004) TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol Cell 15:535–548PubMedGoogle Scholar
  60. Kono T, Zou J, Bird S, Savan R, Sakai M, Secombes CJ (2006) Identification and expression analysis of lymphotoxin-beta like homologues in rainbow trout Oncorhynchus mykiss. Mol Immunol 43:1390–1401PubMedGoogle Scholar
  61. Kopp E, Medzhitov R (2003) Recognition of microbial infection by Toll-like receptors. Curr Opin Immunol 15:396–401PubMedGoogle Scholar
  62. Lam SH, Chua HL, Gong Z, Lam TJ, Sin YM (2004) Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Dev Comp Immunol 28:9–28PubMedGoogle Scholar
  63. Lanier LL (2005) NK cell recognition. Annu Rev Immunol 23:225–274PubMedGoogle Scholar
  64. LaPatra SE, Barone L, Jones GR, Zon LI (2000) Effects of infectious hematopoietic necrosis virus and infectious pancreatic necrosis virus infection on hematopoietic precursors of the zebrafish. Blood Cells Mol Dis 26:445–452PubMedGoogle Scholar
  65. Leippe M (1995) Ancient weapons: NK-lysin, is a mammalian homolog to pore-forming peptides of a protozoan parasite. Cell 83:17–18PubMedGoogle Scholar
  66. Lemaitre B (2004) The road to Toll. Nat Rev Immunol 4:521–527PubMedGoogle Scholar
  67. Lemaitre B, Kromer-Metzger E, Michaut L, Nicolas E, Meister M, Georgel P, Reichhart JM, Hoffmann JA (1995) A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc Natl Acad Sci USA 92:9465–9469PubMedGoogle Scholar
  68. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973–983PubMedGoogle Scholar
  69. Lemaitre B, Reichhart JM, Hoffmann JA (1997) Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci USA 94:14614–14619PubMedGoogle Scholar
  70. Lieberman J (2003) The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat Rev Immunol 3:361–370PubMedGoogle Scholar
  71. Liu WY, Wang Y, Sun YH, Wang YP, Chen SP, Zhu ZY (2005) Efficient RNA interference in zebrafish embryos using siRNA synthesized with SP6 RNA polymerase. Dev Growth Differ 47:323–331PubMedGoogle Scholar
  72. McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeted screening for induced mutations. Nat Biotechnol 18:455–457PubMedGoogle Scholar
  73. McCann FE, Suhling K, Carlin LM, Eleme K, Taner SB, Yanagi K, Vanherberghen B, French PM, Davis DM (2002) Imaging immune surveillance by T cells and NK cells. Immunol Rev 189:179–192PubMedGoogle Scholar
  74. Medzhitov R, Preston-Hurlburt P, Janeway CA Jr (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394–397PubMedGoogle Scholar
  75. Medzhitov R, Preston-Hurlburt P, Kopp E, Stadlen A, Chen C, Ghosh S, Janeway CA Jr (1998) MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell 2:253–258PubMedGoogle Scholar
  76. Meijer AH, Gabby Krens SF, Medina Rodriguez IA, He S, Bitter W, Ewa Snaar-Jagalska B, Spaink HP (2004) Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish. Mol Immunol 40:773–783PubMedGoogle Scholar
  77. Menudier A, Rougier FP, Bosgiraud C (1996) Comparative virulence between different strains of Listeria in zebrafish (Brachydanio rerio) and mice. Pathol Biol (Paris) 44:783–789Google Scholar
  78. Meyer-Wentrup F, Cambi A, Adema GJ, Figdor CG (2005) “Sweet talk”: closing in on C type lectin signaling. Immunity 22:399–400PubMedGoogle Scholar
  79. Nasevicius A, Ekker SC (2000) Effective targeted gene ‘knockdown’ in zebrafish. Nat Genet 26:216–220PubMedGoogle Scholar
  80. Neely MN, Pfeifer JD, Caparon M (2002) Streptococcus–zebrafish model of bacterial pathogenesis. Infect Immun 70:3904–3914PubMedGoogle Scholar
  81. Oates AC, Bruce AE, Ho RK (2000) Too much interference: injection of double-stranded RNA has nonspecific effects in the zebrafish embryo. Dev Biol 224:20–28PubMedGoogle Scholar
  82. Odom EW, Vasta GR (2006) Characterization of a binary tandem domain F-type lectin from striped bass (Morone saxatilis). J Biol Chem 281:1698–1713PubMedGoogle Scholar
  83. Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T (2003a) TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol 4:161–167PubMedGoogle Scholar
  84. Oshiumi H, Sasai M, Shida K, Fujita T, Matsumoto M, Seya T (2003b) TIR-containing adapter molecule (TICAM)-2, a bridging adapter recruiting to toll-like receptor 4 TICAM-1 that induces interferon-beta. J Biol Chem 278:49751–49762PubMedGoogle Scholar
  85. Panagos PG, Dobrinski KP, Chen X, Grant AW, Traver D, Djeu JY, Wei S, Yoder JA (2006) Immune-related, lectin-like receptors are differentially expressed in the myeloid and lymphoid lineages of zebrafish. Immunogenetics 58:31–40PubMedGoogle Scholar
  86. Peatman E, Liu Z (2006) CC chemokines in zebrafish: evidence for extensive intrachromosomal gene duplications. Genomics 88:381–385PubMedGoogle Scholar
  87. Phelan PE, Mellon MT, Kim CH (2005a) Functional characterization of full-length TLR3, IRAK-4, and TRAF6 in zebrafish (Danio rerio). Mol Immunol 42:1057–1071PubMedGoogle Scholar
  88. Phelan PE, Pressley ME, Witten PE, Mellon MT, Blake S, Kim CH (2005b) Characterization of snakehead rhabdovirus infection in zebrafish (Danio rerio). J Virol 79:1842–1852PubMedGoogle Scholar
  89. Phelan PE III, Mellon MT, Kim CH (2005c) Functional characterization of full-length TLR3, IRAK-4, and TRAF6 in zebrafish (Danio rerio). Mol Immunol 42:1057–1071PubMedGoogle Scholar
  90. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085–2088PubMedGoogle Scholar
  91. Praveen K, Evans DL, Jaso-Friedmann L (2004) Evidence for the existence of granzyme-like serine proteases in teleost cytotoxic cells. J Mol Evol 58:449–459PubMedGoogle Scholar
  92. Praveen K, Evans DL, Jaso-Friedmann L (2006a) Constitutive expression of tumor necrosis factor-alpha in cytotoxic cells of teleosts and its role in regulation of cell-mediated cytotoxicity. Mol Immunol 43:279–291PubMedGoogle Scholar
  93. Praveen K, Leary JH 3rd, Evans DL, Jaso-Friedmann L (2006b) Nonspecific cytotoxic cells of teleosts are armed with multiple granzymes and other components of the granule exocytosis pathway. Mol Immunol 43:1152–1162PubMedGoogle Scholar
  94. Pressley ME, Phelan PE 3rd, Witten PE, Mellon MT, Kim CH (2005) Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Dev Comp Immunol 29:501–513PubMedGoogle Scholar
  95. Prouty MG, Correa NE, Barker LP, Jagadeeswaran P, Klose KE (2003) Zebrafish–Mycobacterium marinum model for mycobacterial pathogenesis. FEMS Microbiol Lett 225:177–182PubMedGoogle Scholar
  96. Rabinovich GA, Rubinstein N, Toscano MA (2002) Role of galectins in inflammatory and immunomodulatory processes. Biochim Biophys Acta 1572:274–284PubMedGoogle Scholar
  97. Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK, Smith KD, Hood LE, Aderem A (2005) The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci USA 102:9577–9582PubMedGoogle Scholar
  98. Robertsen B (2006) The interferon system of teleost fish. Fish Shellfish Immunol 20:172–191PubMedGoogle Scholar
  99. Rogers NC, Slack EC, Edwards AD, Nolte MA, Schulz O, Schweighoffer E, Williams DL, Gordon S, Tybulewicz VL, Brown GD, Reis e Sousa C (2005) Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22:507–517PubMedGoogle Scholar
  100. Sanders GE, Batts WN, Winton JR (2003) Susceptibility of zebrafish (Danio rerio) to a model pathogen, spring viremia of carp virus. Comp Med 53:514–521PubMedGoogle Scholar
  101. Santos MD, Yasuike M, Hirono I, Aoki T (2006) The granulocyte colony-stimulating factors (CSF3s) of fish and chicken. Immunogenetics 58:422–432PubMedGoogle Scholar
  102. Sar AM van der, Musters RJ, van Eeden FJ, Appelmelk BJ, Vandenbroucke-Grauls CM, Bitter W (2003) Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections. Cell Microbiol 5:601–611PubMedGoogle Scholar
  103. Sar AM van der, Stockhammer OW, van der Laan C, Spaink HP, Bitter W, Meijer AH (2006) MyD88 innate immune function in a Zebrafish embryo infection model. Infect Immun 74:2436–2441PubMedGoogle Scholar
  104. Schilling D, Thomas K, Nixdorff K, Vogel SN, Fenton MJ (2002) Toll-like receptor 4 and Toll-IL-1 receptor domain-containing adapter protein (TIRAP)/myeloid differentiation protein 88 adapter-like (Mal) contribute to maximal IL-6 expression in macrophages. J Immunol 169:5874–5880PubMedGoogle Scholar
  105. Schneider DS, Hudson KL, Lin TY, Anderson KV (1991) Dominant and recessive mutations define functional domains of Toll, a transmembrane protein required for dorsal-ventral polarity in the Drosophila embryo. Genes Dev 5:797–807PubMedGoogle Scholar
  106. Shen L, Stuge TB, Zhou H, Khayat M, Barker KS, Quiniou SM, Wilson M, Bengten E, Chinchar VG, Clem LW, Miller NW (2002) Channel catfish cytotoxic cells: a mini-review. Dev Comp Immunol 26:141–149PubMedGoogle Scholar
  107. Shinobu N, Iwamura T, Yoneyama M, Yamaguchi K, Suhara W, Fukuhara Y, Amano F, Fujita T (2002) Involvement of TIRAP/MAL in signaling for the activation of interferon regulatory factor 3 by lipopolysaccharide. FEBS Lett 517:251–256PubMedGoogle Scholar
  108. Silverstein AM (1989) A history of immunology. Academic, San DiegoGoogle Scholar
  109. Silverstein AM (2002) Paul Ehrlich’s receptor immunology: the magnificent obsession. Academic, San DiegoGoogle Scholar
  110. Steward R (1987) Dorsal, an embryonic polarity gene in Drosophila, is homologous to the vertebrate proto-oncogene, c-rel. Science 238:692–694PubMedGoogle Scholar
  111. Strong SJ, Mueller MG, Litman RT, Hawke NA, Haire RN, Miracle AL, Rast JP, Amemiya CT, Litman GW (1999) A novel multigene family encodes diversified variable regions. Proc Natl Acad Sci USA 96:15080–15085PubMedGoogle Scholar
  112. Stuge TB, Wilson MR, Zhou H, Barker KS, Bengten E, Chinchar G, Miller NW, Clem LW (2000) Development and analysis of various clonal alloantigen-dependent cytotoxic cell lines from channel catfish. J Immunol 164:2971–2977PubMedGoogle Scholar
  113. Takeda K, Akira S (2004) TLR signaling pathways. Semin Immunol 16:3–9PubMedGoogle Scholar
  114. Tauber AI, Chernyak L (1991) Metchnikoff and the origins of immunology: from metaphor to theory. Oxford University Press, New YorkGoogle Scholar
  115. Thisse C, Zon LI (2002) Organogenesis–heart and blood formation from the zebrafish point of view. Science 295:457–462PubMedGoogle Scholar
  116. Traver D, Herbomel P, Patton EE, Murphey RD, Yoder JA, Litman GW, Catic A, Amemiya CT, Zon LI, Trede NS (2003) The zebrafish as a model organism to study development of the immune system. Adv Immunol 81:253–330PubMedGoogle Scholar
  117. Trede NS, Langenau DM, Traver D, Look AT, Zon LI (2004) The use of zebrafish to understand immunity. Immunity 20:367–379PubMedGoogle Scholar
  118. Ulevitch RJ (2004) Therapeutics targeting the innate immune system. Nat Rev Immunol 4:512–520PubMedGoogle Scholar
  119. Vasta GR, Ahmed H, Du S, Henrikson D (2004) Galectins in teleost fish: zebrafish (Danio rerio) as a model species to address their biological roles in development and innate immunity. Glycoconj J 21:503–521PubMedGoogle Scholar
  120. Vitved L, Holmskov U, Koch C, Teisner B, Hansen S, Salomonsen J, Skjodt K (2000) The homologue of mannose-binding lectin in the carp family Cyprinidae is expressed at high level in spleen, and the deduced primary structure predicts affinity for galactose. Immunogenetics 51:955–964PubMedGoogle Scholar
  121. Vogel SN, Fenton M (2003) Toll-like receptor 4 signalling: new perspectives on a complex signal-transduction problem. Biochem Soc Trans 31:664–668PubMedGoogle Scholar
  122. Walsh CM, Matloubian M, Liu CC, Ueda R, Kurahara CG, Christensen JL, Huang MT, Young JD, Ahmed R, Clark WR (1994) Immune function in mice lacking the perforin gene. Proc Natl Acad Sci USA 91:10854–10858PubMedGoogle Scholar
  123. Wienholds E, Eeden F van, Kosters M, Mudde J, Plasterk RH, Cuppen E (2003) Efficient target-selected mutagenesis in zebrafish. Genome Res 13:2700–2707PubMedGoogle Scholar
  124. Willett CE, Cherry JJ, Steiner LA (1997) Characterization and expression of the recombination activating genes (rag1 and rag2) of zebrafish. Immunogenetics 45:394–404PubMedGoogle Scholar
  125. Xie Y, Chen X, Wagner TE (1997) A ribozyme-mediated, gene “knockdown” strategy for the identification of gene function in zebrafish. Proc Natl Acad Sci USA 94:13777–13781PubMedGoogle Scholar
  126. Yamamoto M, Sato S, Hemmi H, Sanjo H, Uematsu S, Kaisho T, Hoshino K, Takeuchi O, Kobayashi M, Fujita T, Takeda K, Akira S (2002a) Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 420:324–329PubMedGoogle Scholar
  127. Yamamoto M, Sato S, Mori K, Hoshino K, Takeuchi O, Takeda K, Akira S (2002b) Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J Immunol 169:6668–6672PubMedGoogle Scholar
  128. Yamamoto M, Sato S, Hemmi H, Uematsu S, Hoshino K, Kaisho T, Takeuchi O, Takeda K, Akira S (2003) TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat Immunol 4:1144–1150PubMedGoogle Scholar
  129. Yan YL, Miller CT, Nissen RM, Singer A, Liu D, Kirn A, Draper B, Willoughby J, Morcos PA, Amsterdam A, Chung BC, Westerfield M, Haffter P, Hopkins N, Kimmel C, Postlethwait JH (2002) A zebrafish sox9 gene required for cartilage morphogenesis. Development 129:5065–5079PubMedGoogle Scholar
  130. Yoder JA, Litman GW (2000) Immune-type diversity in the absence of somatic rearrangement. Curr Top Microbiol Immunol 248:271–282PubMedGoogle Scholar
  131. Yoder JA, Mueller MG, Wei S, Corliss BC, Prather DM, Willis T, Litman RT, Djeu JY, Litman GW (2001) Immune-type receptor genes in zebrafish share genetic and functional properties with genes encoded by the mammalian leukocyte receptor cluster. Proc Natl Acad Sci USA 98:6771–6776PubMedGoogle Scholar
  132. Yoder JA, Litman RT, Mueller MG, Desai S, Dobrinski KP, Montgomery JS, Buzzeo MP, Ota T, Amemiya CT, Trede NS, Wei S, Djeu JY, Humphray S, Jekosch K, Hernandez Prada JA, Ostrov DA, Litman GW (2004) Resolution of the novel immune-type receptor gene cluster in zebrafish. Proc Natl Acad Sci USA 101:15706–15711PubMedGoogle Scholar
  133. Zhang DC, Shao YQ, Huang YQ, Jiang SG (2005) Cloning, characterization and expression analysis of interleukin-10 from the zebrafish (Danio rerion). J Biochem Mol Biol 38:571–576PubMedGoogle Scholar
  134. Zhao Z, Cao Y, Li M, Meng A (2001) Double-stranded RNA injection produces nonspecific defects in zebrafish. Dev Biol 229:215–223PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Con Sullivan
    • 1
  • Carol H. Kim
    • 1
  1. 1.Department of Biochemistry, Microbiology, and Molecular BiologyUniversity of MaineOronoUSA

Personalised recommendations