Table of Contents Author Guidelines Submit a Manuscript
Advances in Hematology
Volume 2012, Article ID 159807, 19 pages
http://dx.doi.org/10.1155/2012/159807
Review Article

Pathogen Recognition and Activation of the Innate Immune Response in Zebrafish

Institute of Biology, Leiden University, Einsteinweg 55, 2333 CC Leiden, The Netherlands

Received 3 February 2012; Accepted 22 April 2012

Academic Editor: Christopher Hall

Copyright © 2012 Michiel van der Vaart et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. M. Tobin, J. C. Vary, J. P. Ray et al., “The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans,” Cell, vol. 140, no. 5, pp. 717–730, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. H. E. Volkman, T. C. Pozos, J. Zheng, J. M. Davis, J. F. Rawls, and L. Ramakrishnan, “Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium,” Science, vol. 327, no. 5964, pp. 466–469, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Ludwig, N. Palha, C. Torhy et al., “Whole-body analysis of a viral infection: vascular endothelium is a primary target of Infectious hematopoietic necrosis virus in zebrafish larvae,” PLoS Pathogens, vol. 7, no. 2, Article ID e1001269, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. A. H. Meijer and H. P. Spaink, “Host-Pathogen interactions made transparent with the zebrafish model,” Current Drug Targets, vol. 12, no. 7, pp. 1000–1017, 2011. View at Google Scholar · View at Scopus
  5. C. Sullivan and C. H. Kim, “Zebrafish as a model for infectious disease and immune function,” Fish and Shellfish Immunology, vol. 25, no. 4, pp. 341–350, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. J. P. Allen and M. N. Neely, “Trolling for the ideal model host: zebrafish take the bait,” Future Microbiology, vol. 5, no. 4, pp. 563–569, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. J. R. Mathias, K. B. Walters, and A. Huttenlocher, “Neutrophil motility in vivo using zebrafish.,” Methods in Molecular Biology, vol. 571, pp. 151–166, 2009. View at Google Scholar · View at Scopus
  8. S. A. Renshaw, C. A. Loynes, D. M. I. Trushell, S. Elworthy, P. W. Ingham, and M. K. B. Whyte, “Atransgenic zebrafish model of neutrophilic inflammation,” Blood, vol. 108, no. 13, pp. 3976–3978, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Hall, M. Flores, T. Storm, K. Crosier, and P. Crosier, “The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish,” BMC Developmental Biology, vol. 7, article no. 42, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Gray, C. A. Loynes, M. K. B. Whyte, D. C. Crossman, S. A. Renshaw, and T. J. A. Chico, “Simultaneous intravital imaging of macrophage and neutrophil behaviour during inflammation using a novel transgenic zebrafish,” Thrombosis and Haemostasis, vol. 105, no. 5, pp. 811–819, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. F. Ellett, L. Pase, J. W. Hayman, A. Andrianopoulos, and G. J. Lieschke, “mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish,” Blood, vol. 117, no. 4, pp. e49–e56, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Herbomel, B. Thisse, and C. Thisse, “Ontogeny and behaviour of early macrophages in the zebrafish embryo,” Development, vol. 126, no. 17, pp. 3735–3745, 1999. View at Google Scholar · View at Scopus
  13. O. W. Stockhammer, A. Zakrzewska, Z. Hegedûs, H. P. Spaink, and A. H. Meijer, “Transcriptome profiling and functional analyses of the zebrafish embryonic innate immune response to Salmonella infection,” Journal of Immunology, vol. 182, no. 9, pp. 5641–5653, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. S. H. Lam, H. L. Chua, Z. Gong, T. J. Lam, and Y. M. Sin, “Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study,” Developmental and Comparative Immunology, vol. 28, no. 1, pp. 9–28, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Medzhitov and C. Janeway Jr., “Innate immune recognition: mechanisms and pathways,” Immunological Reviews, vol. 173, pp. 89–97, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. A. A. Beg, “Endogenous ligands of Toll-like receptors: implications for regulating inflammatory and immune responses,” Trends in Immunology, vol. 23, no. 11, pp. 509–512, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Matzinger, “An innate sense of danger,” Annals of the New York Academy of Sciences, vol. 961, pp. 341–342, 2002. View at Google Scholar · View at Scopus
  18. T. H. Mogensen, “Pathogen recognition and inflammatory signaling in innate immune defenses,” Clinical Microbiology Reviews, vol. 22, no. 2, pp. 240–273, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Akira and K. Takeda, “Toll-like receptor signalling,” Nature Reviews Immunology, vol. 4, no. 7, pp. 499–511, 2004. View at Google Scholar · View at Scopus
  20. S. Akira, S. Uematsu, and O. Takeuchi, “Pathogen recognition and innate immunity,” Cell, vol. 124, no. 4, pp. 783–801, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Forlenza, J. P. Scharsack, N. M. Kachamakova, A. J. Taverne-Thiele, J. H. W. M. Rombout, and G. F. Wiegertjes, “Differential contribution of neutrophilic granulocytes and macrophages to nitrosative stress in a host-parasite animal model,” Molecular Immunology, vol. 45, no. 11, pp. 3178–3189, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. A. M. van der Sar, H. P. Spaink, A. Zakrzewska, W. Bitter, and A. H. Meijer, “Specificity of the zebrafish host transcriptome response to acute and chronic mycobacterial infection and the role of innate and adaptive immune components,” Molecular Immunology, vol. 46, no. 11-12, pp. 2317–2332, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Lemaitre, E. Nicolas, L. Michaut, J. M. Reichhart, and J. A. Hoffmann, “The dorsoventral regulatory gene cassette spatzle/Toll/Cactus controls the potent antifungal response in Drosophila adults,” Cell, vol. 86, no. 6, pp. 973–983, 1996. View at Publisher · View at Google Scholar · View at Scopus
  24. L. A. J. O'Neill and A. G. Bowie, “The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling,” Nature Reviews Immunology, vol. 7, no. 5, pp. 353–364, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Miettinen, T. Sareneva, I. Julkunen, and S. Matikainen, “IFNs activate toll-like receptor gene expression in viral infections,” Genes and Immunity, vol. 2, no. 6, pp. 349–355, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Takeda and S. Akira, “Microbial recognition by Toll-like receptors,” Journal of Dermatological Science, vol. 34, no. 2, pp. 73–82, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Jault, L. Pichon, and J. Chluba, “Toll-like receptor gene family and TIR-domain adapters in Danio rerio,” Molecular Immunology, vol. 40, no. 11, pp. 759–771, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. A. H. Meijer, S. F. Gabby Krens, I. A. Medina Rodriguez et al., “Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish,” Molecular Immunology, vol. 40, no. 11, pp. 773–783, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Palti, “Toll-like receptors in bony fish: from genomics to function,” Developmental and Comparative Immunology, vol. 35, no. 12, pp. 1263–1272, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. C. M. S. Ribeiro, T. Hermsen, A. J. Taverne-Thiele, H. F. J. Savelkoul, and G. F. Wiegertjes, “Evolution of recognition of ligands from gram-positive bacteria: similarities and differences in the TLR2-mediated response between mammalian vertebrates and teleost fish,” Journal of Immunology, vol. 184, no. 5, pp. 2355–2368, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Matsuo, H. Oshiumi, T. Tsujita et al., “Teleost TLR22 recognizes RNA duplex to induce IFN and protect cells from birnaviruses,” Journal of Immunology, vol. 181, no. 5, pp. 3474–3485, 2008. View at Google Scholar · View at Scopus
  32. M. P. Sepulcre, F. Alcaraz-Pérez, A. López-Muñoz et al., “Evolution of lipopolysaccharide (LPS) recognition and signaling: fish TLR4 does not recognize LPS and negatively regulates NF-κB activation,” Journal of Immunology, vol. 182, no. 4, pp. 1836–1845, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Sullivan, J. Charette, J. Catchen et al., “The gene history of zebrafish tlr4a and tlr4b is predictive of their divergent functions,” Journal of Immunology, vol. 183, no. 9, pp. 5896–5908, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Stein, M. Caccamo, G. Laird, and M. Leptin, “Conservation and divergence of gene families encoding components of innate immune response systems in zebrafish,” Genome Biology, vol. 8, no. 11, article no. R251, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. J. M. Bates, J. Akerlund, E. Mittge, and K. Guillemin, “Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota,” Cell Host and Microbe, vol. 2, no. 6, pp. 371–382, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. A. M. Van Der Sar, O. W. Stockhammer, C. Van Der Laan, H. P. Spaink, W. Bitter, and A. H. Meijer, “MyD88 innate immune function in a zebrafish embryo infection model,” Infection and Immunity, vol. 74, no. 4, pp. 2436–2441, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. O. W. Stockhammer, H. Rauwerda, F. R. Wittink, T. M. Breit, A. H. Meijer, and H. P. Spaink, “Transcriptome analysis of Traf6 function in the innate immune response of zebrafish embryos,” Molecular Immunology, vol. 48, no. 1-3, pp. 179–190, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Ordas, Z. Hegedus, C. V. Henkel et al., “Deep sequencing of the innate immune transcriptomic response of zebrafish embryos to Salmonella infection,” Fish and Shellfish Immunology, vol. 31, no. 5, pp. 716–724, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Kersse, M. J. M. Bertrand, M. Lamkanfi, and P. Vandenabeele, “NOD-like receptors and the innate immune system: coping with danger, damage and death,” Cytokine and Growth Factor Reviews, vol. 22, no. 5-6, pp. 257–276, 2011. View at Publisher · View at Google Scholar
  40. T. D. Kanneganti, M. Lamkanfi, and G. Núñez, “Intracellular NOD-like receptors in host defense and disease,” Immunity, vol. 27, no. 4, pp. 549–559, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. S. E. Girardin, I. G. Boneca, L. A. M. Carneiro et al., “Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan,” Science, vol. 300, no. 5625, pp. 1584–1587, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. S. E. Girardin, J. P. Hugot, and P. J. Sansonetti, “Lessons from Nod2 studies: towards a link between Crohn's disease and bacterial sensing,” Trends in Immunology, vol. 24, no. 12, pp. 652–658, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. G. K. Silva, F. R. S. Gutierrez, P. M. M. Guedes et al., “Cutting edge: nucleotide-binding oligomerization domain 1-dependent responses account for murine resistance against Trypanosoma cruzi infection,” Journal of Immunology, vol. 184, no. 3, pp. 1148–1152, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. M. H. Shaw, T. Reimer, C. Sánchez-Valdepeñas et al., “T cell-intrinsic role of Nod2 in promoting type 1 immunity to Toxoplasma gondii,” Nature Immunology, vol. 10, no. 12, pp. 1267–1274, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. N. Inohara, T. Koseki, J. Lin et al., “An induced proximity model for NF-κB activation in the Nod1/RICK and RIP signaling pathways,” Journal of Biological Chemistry, vol. 275, no. 36, pp. 27823–27831, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. K. Kobayashi, N. Inohara, L. D. Hernandez et al., “RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems,” Nature, vol. 416, no. 6877, pp. 194–199, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. J. H. Park, Y. G. Kim, M. Shaw et al., “Nod1/RICK and TLR signaling regulate chemokine and antimicrobial innate immune responses in mesothelial cells,” Journal of Immunology, vol. 179, no. 1, pp. 514–521, 2007. View at Google Scholar · View at Scopus
  48. E. Voss, J. Wehkamp, K. Wehkamp, E. F. Stange, J. M. Schröder, and J. Harder, “NOD2/CARD15 mediates induction of the antimicrobial peptide human beta-defensin-2,” Journal of Biological Chemistry, vol. 281, no. 4, pp. 2005–2011, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. E. Noguchi, Y. Homma, X. Kang, M. G. Netea, and X. Ma, “A Crohn's disease-associated NOD2 mutation suppresses transcription of human IL10 by inhibiting activity of the nuclear ribonucleoprotein hnRNP-A1,” Nature Immunology, vol. 10, no. 5, pp. 471–479, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. F. Martinon, K. Burns, and J. Tschopp, “The Inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-β,” Molecular Cell, vol. 10, no. 2, pp. 417–426, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. K. Tsuchiya, H. Hara, I. Kawamura et al., “Involvement of absent in melanoma 2 in inflammasome activation in macrophages infected with Listeria monocytogenes,” Journal of Immunology, vol. 185, no. 2, pp. 1186–1195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. D. L. Kastner, I. Aksentijevich, and R. Goldbach-Mansky, “Autoinflammatory disease reloaded: a clinical perspective,” Cell, vol. 140, no. 6, pp. 784–790, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. S. C. Eisenbarth, O. R. Colegio, W. O'Connor, F. S. Sutterwala, and R. A. Flavell, “Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants,” Nature, vol. 453, no. 7198, pp. 1122–1126, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Chamaillard, S. E. Girardin, J. Viala, and D. J. Philpott, “Nods, nalps and naip: intracellular regulators of bacterial-induced inflammation,” Cellular Microbiology, vol. 5, no. 9, pp. 581–592, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Henry, A. Brotcke, D. S. Weiss, L. J. Thompson, and D. M. Monack, “Type I interferon signaling is required for activation of the inflammasome during Francisella infection,” Journal of Experimental Medicine, vol. 204, no. 5, pp. 987–994, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. K. J. Laing, M. K. Purcell, J. R. Winton, and J. D. Hansen, “A genomic view of the NOD-like receptor family in teleost fish: identification of a novel NLR subfamily in zebrafish,” BMC Evolutionary Biology, vol. 8, no. 1, article no. 42, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. S. H. Oehlers, M. V. Flores, C. J. Hall, S. Swift, K. E. Crosier, and P. S. Crosier, “The inflammatory bowel disease (IBD) susceptibility genes NOD1 and NOD2 have conserved anti-bacterial roles in zebrafish,” Disease Models and Mechanisms, vol. 4, no. 6, pp. 832–841, 2011. View at Publisher · View at Google Scholar
  58. Y. M. Loo and M. Gale, “Immune signaling by RIG-I-like receptors,” Immunity, vol. 34, no. 5, pp. 680–692, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. D. C. Kang, R. V. Gopalkrishnan, L. Lin et al., “Expression analysis and genomic characterization of human melanoma differentiation associated gene-5, mda-5: a novel type I interferon-responsive apoptosis-inducing gene,” Oncogene, vol. 23, no. 9, pp. 1789–1800, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Yoneyama, M. Kikuchi, T. Natsukawa et al., “The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses,” Nature Immunology, vol. 5, no. 7, pp. 730–737, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. T. Saito, R. Hirai, Y. M. Loo et al., “Regulation of innate antiviral defenses through a shared repressor domain in RIG-1 and LGP2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 2, pp. 582–587, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Yoneyama, M. Kikuchi, K. Matsumoto et al., “Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity,” Journal of Immunology, vol. 175, no. 5, pp. 2851–2858, 2005. View at Google Scholar · View at Scopus
  63. I. Scott, “The role of mitochondria in the mammalian antiviral defense system,” Mitochondrion, vol. 10, no. 4, pp. 316–320, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Paz, Q. Sun, P. Nakhaei et al., “Induction of IRF-3 and IRF-7 phosphorylation following activation of the RIG-I pathway,” Cellular and Molecular Biology, vol. 52, no. 1, pp. 17–28, 2006. View at Google Scholar · View at Scopus
  65. Y. M. Loo, J. Fornek, N. Crochet et al., “Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity,” Journal of Virology, vol. 82, no. 1, pp. 335–345, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. J. Zou, M. Chang, P. Nie, and C. J. Secombes, “Origin and evolution of the RIG-I like RNA helicase gene family,” BMC Evolutionary Biology, vol. 9, no. 1, article no. 85, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. D. Aggad, M. Mazel, P. Boudinot et al., “The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains,” Journal of Immunology, vol. 183, no. 6, pp. 3924–3931, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Biacchesi, M. LeBerre, A. Lamoureux et al., “Mitochondrial antiviral signaling protein plays a major role in induction of the fish innate immune response against RNA and DNA viruses,” Journal of Virology, vol. 83, no. 16, pp. 7815–7827, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. F. Sun, Y.-B. Zhang, T.-K. Liu, J. Shi, B. Wang, and J.-F. Gui, “Fish MITA serves as a mediator for distinct fish IFN gene activation dependent on IRF3 or IRF7,” Journal of Immunology, vol. 187, no. 5, pp. 2531–2539, 2011. View at Publisher · View at Google Scholar
  70. N. Medic, F. Vita, R. Abbate et al., “Mast cell activation by myelin through scavenger receptor,” Journal of Neuroimmunology, vol. 200, no. 1-2, pp. 27–40, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. J. E. Murphy, P. R. Tedbury, S. Homer-Vanniasinkam, J. H. Walker, and S. Ponnambalam, “Biochemistry and cell biology of mammalian scavenger receptors,” Atherosclerosis, vol. 182, no. 1, pp. 1–15, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Plüddemann, C. Neyen, and S. Gordon, “Macrophage scavenger receptors and host-derived ligands,” Methods, vol. 43, no. 3, pp. 207–217, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. T. Areschoug and S. Gordon, “Pattern recognition receptors and their role in innate immunity: focus on microbial protein ligands,” Contributions to Microbiology, vol. 15, pp. 45–60, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. S. E. Doyle, R. M. O'Connell, G. A. Miranda et al., “Toll-like receptors induce a phagocytic gene program through p38,” Journal of Experimental Medicine, vol. 199, no. 1, pp. 81–90, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. K. Hoebe, P. Georgel, S. Rutschmann et al., “CD36 is a sensor of diacylglycerides,” Nature, vol. 433, no. 7025, pp. 523–527, 2005. View at Publisher · View at Google Scholar · View at Scopus
  76. P. Jeannin, B. Bottazzi, M. Sironi et al., “Complexity and complementarity of outer membrane protein A recognition by cellular and humoral innate immunity receptors,” Immunity, vol. 22, no. 5, pp. 551–560, 2005. View at Publisher · View at Google Scholar · View at Scopus
  77. L. Peiser, P. J. Gough, T. Kodama, and S. Gordon, “Macrophage class A scavenger receptor-mediated phagocytosis of Escherichia coli: role of cell heterogeneity, microbial strain, and culture conditions in vitro,” Infection and Immunity, vol. 68, no. 4, pp. 1953–1963, 2000. View at Publisher · View at Google Scholar · View at Scopus
  78. L. Peiser, M. P. J. De Winther, K. Makepeace et al., “The class A macrophage scavenger receptor is a major pattern recognition receptor for Neisseria meningitidis which is independent of lipopolysaccharide and not required for secretory responses,” Infection and Immunity, vol. 70, no. 10, pp. 5346–5354, 2002. View at Publisher · View at Google Scholar · View at Scopus
  79. M. S. Arredouani, Z. Yang, A. Imrich, Y. Ning, G. Qin, and L. Kobzik, “The macrophage scavenger receptor SR-AI/II and lung defense against pneumococci and particles,” American Journal of Respiratory Cell and Molecular Biology, vol. 35, no. 4, pp. 474–478, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. O. Elomaa, M. Kangas, C. Sahlberg et al., “Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages,” Cell, vol. 80, no. 4, pp. 603–609, 1995. View at Google Scholar · View at Scopus
  81. M. Arredouani, Z. Yang, Y. Y. Ning et al., “The scavenger receptor MARCO is required for lung defense against pneumococcal pneumonia and inhaled particles,” Journal of Experimental Medicine, vol. 200, no. 2, pp. 267–272, 2004. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Mukhopadhyay, Y. Chen, M. Sankala et al., “MARCO, an innate activation marker of macrophages, is a class A scavenger receptor for Neisseria meningitidis,” European Journal of Immunology, vol. 36, no. 4, pp. 940–949, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. D. M. E. Bowdish, K. Sakamoto, M. J. Kim et al., “MARCO, TLR2, and CD14 are required for macrophage cytokine responses to mycobacterial trehalose dimycolate and Mycobacterium tuberculosis,” PLoS Pathogens, vol. 5, no. 6, Article ID e1000474, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. L. M. Stuart, J. Deng, J. M. Silver et al., “Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain,” Journal of Cell Biology, vol. 170, no. 3, pp. 477–485, 2005. View at Publisher · View at Google Scholar · View at Scopus
  85. T. G. Vishnyakova, R. Kurlander, A. V. Bocharov et al., “CLA-1 and its splicing variant CLA-2 mediate bacterial adhesion and cytosolic bacterial invasion in mammalian cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 45, pp. 16888–16893, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. V. Wittamer, J. Y. Bertrand, P. W. Gutschow, and D. Traver, “Characterization of the mononuclear phagocyte system in zebrafish,” Blood, vol. 117, no. 26, pp. 7126–7135, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. A. Zakrzewska, C. Cui, O. W. Stockhammer, E. L. Benard, H. P. Spaink, and A. H. Meijer, “Macrophage-specific gene functions in Spi1-directed innate immunity,” Blood, vol. 116, no. 3, pp. e1–e11, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. P. Encinas, M. A. Rodriguez-Milla, B. Novoa, A. Estepa, A. Figueras, and J. Coll, “Zebrafish fin immune responses during high mortality infections with viral haemorrhagic septicemia rhabdovirus. A proteomic and transcriptomic approach,” BMC Genomics, vol. 11, no. 1, article no. 518, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. A. N. Zelensky and J. E. Gready, “The C-type lectin-like domain superfamily,” FEBS Journal, vol. 272, no. 24, pp. 6179–6217, 2005. View at Publisher · View at Google Scholar · View at Scopus
  90. M. J. Robinson, D. Sancho, E. C. Slack, S. LeibundGut-Landmann, and C. R. Sousa, “Myeloid C-type lectins in innate immunity,” Nature Immunology, vol. 7, no. 12, pp. 1258–1265, 2006. View at Publisher · View at Google Scholar
  91. L. L. Lanier, “NK cell recognition,” Annual Review of Immunology, vol. 23, pp. 225–274, 2005. View at Publisher · View at Google Scholar
  92. M. Takahashi, D. Iwaki, A. Matsushita et al., “Cloning and characterization of mannose-binding lectin from lamprey (Agnathans),” Journal of Immunology, vol. 176, no. 8, pp. 4861–4868, 2006. View at Google Scholar · View at Scopus
  93. T. B. H. Geijtenbeek and S. I. Gringhuis, “Signalling through C-type lectin receptors: shaping immune responses,” Nature Reviews Immunology, vol. 9, no. 7, pp. 465–479, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. J. Herre, A. S. J. Marshall, E. Caron et al., “Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages,” Blood, vol. 104, no. 13, pp. 4038–4045, 2004. View at Publisher · View at Google Scholar · View at Scopus
  95. D. M. Underhill, E. Rossnagle, C. A. Lowell, and R. M. Simmons, “Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production,” Blood, vol. 106, no. 7, pp. 2543–2550, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. P. J. Tacken, R. Torensma, and C. G. Figdor, “Targeting antigens to dendritic cells in vivo,” Immunobiology, vol. 211, no. 6-8, pp. 599–608, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. N. C. Rogers, E. C. Slack, A. D. Edwards et al., “Syk-dependent cytokine induction by dectin-1 reveals a novel pattern recognition pathway for C type lectins,” Immunity, vol. 22, no. 4, pp. 507–517, 2005. View at Publisher · View at Google Scholar · View at Scopus
  98. K. Sato, X. L. Yang, T. Yudate et al., “Dectin-2 is a pattern recognition receptor for fungi that couples with the Fc receptor γ chain to induce innate immune responses,” Journal of Biological Chemistry, vol. 281, no. 50, pp. 38854–38866, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. S. Yamasaki, M. Matsumoto, O. Takeuchi et al., “C-type lectin Mincle is an activating receptor for pathogenic fungus, Malassezia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 6, pp. 1897–1902, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. O. Gross, A. Gewies, K. Finger et al., “Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity,” Nature, vol. 442, no. 7103, pp. 651–656, 2006. View at Publisher · View at Google Scholar · View at Scopus
  101. S. I. Gringhuis, J. den Dunnen, M. Litjens, B. van het Hof, Y. van Kooyk, and T. H. Geijtenbeek, “C-Type Lectin DC-SIGN modulates toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-κB,” Immunity, vol. 26, no. 5, pp. 605–616, 2007. View at Publisher · View at Google Scholar · View at Scopus
  102. A. N. Jackson, C. A. McLure, R. L. Dawkins, and P. J. Keating, “Mannose binding lectin (MBL) copy number polymorphism in Zebrafish (D. rerio) and identification of haplotypes resistant to L. anguillarum,” Immunogenetics, vol. 59, no. 11, pp. 861–872, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. M. Fukuda, K. Ohtani, S.-J. Jang et al., “Molecular cloning and functional analysis of scavenger receptor zebrafish CL-P1,” Biochimica et Biophysica Acta, vol. 1810, no. 12, pp. 1150–1159, 2011. View at Publisher · View at Google Scholar
  104. K. Ohtani, Y. Suzuki, S. Eda et al., “The membrane-type collectin CL-P1 is a scavenger receptor on vascular endothelial cells,” Journal of Biological Chemistry, vol. 276, no. 47, pp. 44222–44228, 2001. View at Publisher · View at Google Scholar · View at Scopus
  105. A. F. Lin, L. X. Xiang, Q. L. Wang, W. R. Dong, Y. F. Gong, and J. Z. Shao, “The DC-SIGN of zebrafish: insights into the existence of a CD209 homologue in a lower vertebrate and its involvement in adaptive immunity,” Journal of Immunology, vol. 183, no. 11, pp. 7398–7410, 2009. View at Publisher · View at Google Scholar · View at Scopus
  106. P. G. Panagos, K. P. Dobrinski, X. Chen et al., “Immune-related, lectin-like receptors are differentially expressed in the myeloid and lymphoid lineages of zebrafish,” Immunogenetics, vol. 58, no. 1, pp. 31–40, 2006. View at Publisher · View at Google Scholar · View at Scopus
  107. Z. Hegedus, A. Zakrzewska, V. C. Ágoston et al., “Deep sequencing of the zebrafish transcriptome response to mycobacterium infection,” Molecular Immunology, vol. 46, no. 15, pp. 2918–2930, 2009. View at Publisher · View at Google Scholar · View at Scopus
  108. B. Lin, S. Chen, Z. Cao et al., “Acute phase response in zebrafish upon Aeromonas salmonicida and Staphylococcus aureus infection: striking similarities and obvious differences with mammals,” Molecular Immunology, vol. 44, no. 4, pp. 295–301, 2007. View at Publisher · View at Google Scholar · View at Scopus
  109. I. Rojo, O. M. de Ilárduya, A. Estonba, and M. A. Pardo, “Innate immune gene expression in individual zebrafish after Listonella anguillarum inoculation,” Fish and Shellfish Immunology, vol. 23, no. 6, pp. 1285–1293, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. S. P. Commins, L. Borish, and J. W. Steinke, “Immunologic messenger molecules: cytokines, interferons, and chemokines,” Journal of Allergy and Clinical Immunology, vol. 125, no. 2, supplement 2, pp. S53–S72, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. C. Perez, I. Albert, K. DeFay, N. Zachariades, L. Gooding, and M. Kriegler, “A nonsecretable cell surface mutant of tumor necrosis factor (TNF) kills by cell-to-cell contact,” Cell, vol. 63, no. 2, pp. 251–258, 1990. View at Publisher · View at Google Scholar · View at Scopus
  112. D. P. Cerretti, C. J. Kozlosky, B. Mosley et al., “Molecular cloning of the interleukin-1β converting enzyme,” Science, vol. 256, no. 5053, pp. 97–100, 1992. View at Google Scholar · View at Scopus
  113. I. Lalani, K. Bhol, and A. R. Ahmed, “Interleukin-10: biology, role in inflammation and autoimmunity,” Annals of Allergy, Asthma and Immunology, vol. 79, no. 6, pp. 469–484, 1997. View at Google Scholar · View at Scopus
  114. H. Nomiyama, K. Hieshima, N. Osada et al., “Extensive expansion and diversification of the chemokine gene family in zebrafish: identification of a novel chemokine subfamily CX,” BMC Genomics, vol. 9, article no. 222, 2008. View at Publisher · View at Google Scholar · View at Scopus
  115. M. O. Huising, R. J. M. Stet, H. F. J. Savelkoul, and B. M. L. Verburg-Van Kemenade, “The molecular evolution of the interleukin-1 family of cytokines; IL-18 in teleost fish,” Developmental and Comparative Immunology, vol. 28, no. 5, pp. 395–413, 2004. View at Publisher · View at Google Scholar · View at Scopus
  116. D.-C. Zhang, Y.-Q. Shao, Y.-Q. Huang, and S.-G. Jiang, “Cloning, characterization and expression analysis of interleukin-10 from the zebrafish (Danio reriori),” Journal of Biochemistry and Molecular Biology, vol. 38, no. 5, pp. 571–576, 2005. View at Google Scholar
  117. M. Varela, S. Dios, B. Novoa, and A. Figueras, “Characterisation, expression and ontogeny of interleukin-6 and its receptors in zebrafish (Danio rerio),” Developmental and Comparative Immunology, vol. 37, no. 1, pp. 97–106, 2012. View at Publisher · View at Google Scholar
  118. L. Grayfer and M. Belosevic, “Molecular characterization of novel interferon gamma receptor 1 isoforms in zebrafish (Danio rerio) and goldfish (Carassius auratus L.),” Developmental & Comparative Immunology, vol. 36, no. 2, pp. 408–417, 2012. View at Publisher · View at Google Scholar
  119. S. H. B. Oehlers, M. V. Flores, C. J. Hall et al., “Expression of zebrafish cxcl8 (interleukin-8) and its receptors during development and in response to immune stimulation,” Developmental and Comparative Immunology, vol. 34, no. 3, pp. 352–359, 2010. View at Publisher · View at Google Scholar · View at Scopus
  120. L. M. van der Aa, M. Chadzinska, E. Tijhaar, P. Boudinot, and B. M. Lidy verburg-Van kemenade, “CXCL8 chemokines in teleost fish: two lineages with distinct expression profiles during early phases of inflammation,” PLoS One, vol. 5, no. 8, Article ID e12384, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. A. E. Clatworthy, J. S. W. Lee, M. Leibman, Z. Kostun, A. J. Davidson, and D. T. Hung, “Pseudomonas aeruginosa infection of zebrafish involves both host and pathogen determinants,” Infection and Immunity, vol. 77, no. 4, pp. 1293–1303, 2009. View at Publisher · View at Google Scholar · View at Scopus
  122. M. E. Pressley, P. E. Phelan, P. Eckhard Witten, M. T. Mellon, and C. H. Kim, “Pathogenesis and inflammatory response to Edwardsiella tardainfection in the zebrafish,” Developmental and Comparative Immunology, vol. 29, no. 6, pp. 501–513, 2005. View at Publisher · View at Google Scholar · View at Scopus
  123. J. J. Van Soest, O. W. Stockhammer, A. Ordas, G. V. Bloemberg, H. P. Spaink, and A. H. Meijer, “Comparison of static immersion and intravenous injection systems for exposure of zebrafish embryos to the natural pathogen Edwardsiella tarda,” BMC Immunology, vol. 12, Article ID 58, 2011. View at Publisher · View at Google Scholar
  124. H. Clay, H. E. Volkman, and L. Ramakrishnan, “Tumor necrosis factor signaling mediates resistance to mycobacteria by inhibiting bacterial growth and macrophage death,” Immunity, vol. 29, no. 2, pp. 283–294, 2008. View at Publisher · View at Google Scholar · View at Scopus
  125. F. J. Roca, I. Mulero, A. López-Muñoz et al., “Evolution of the inflammatory response in vertebrates: fish TNF-α is a powerful activator of endothelial cells but hardly activates phagocytes,” Journal of Immunology, vol. 181, no. 7, pp. 5071–5081, 2008. View at Google Scholar · View at Scopus
  126. D. Aggad, C. Stein, D. Sieger et al., “In vivo analysis of Ifn-γ1 and Ifn-γ2 signaling in zebrafish,” Journal of Immunology, vol. 185, no. 11, pp. 6774–6782, 2010. View at Publisher · View at Google Scholar · View at Scopus
  127. D. Sieger, C. Stein, D. Neifer, A. M. Van Der Sar, and M. Leptin, “The role of gamma interferon in innate immunity in the zebrafish embryo,” Disease Models and Mechanisms, vol. 2, no. 11-12, pp. 571–581, 2009. View at Publisher · View at Google Scholar · View at Scopus
  128. O. J. Hamming, G. Lutfalla, J. P. Levraud, and R. Hartmann, “Crystal structure of zebrafish interferons I and II reveals conservation of type I interferon structure in vertebrates,” Journal of Virology, vol. 85, no. 16, pp. 8181–8187, 2011. View at Publisher · View at Google Scholar · View at Scopus
  129. J. P. Levraud, P. Boudinot, I. Colin et al., “Identification of the zebrafish IFN receptor: implications for the origin of the vertebrate IFN system,” Journal of Immunology, vol. 178, no. 7, pp. 4385–4394, 2007. View at Google Scholar · View at Scopus
  130. K. Kwiatkowska and A. Sobota, “Signaling pathways in phagocytosis,” BioEssays, vol. 21, no. 5, pp. 422–431, 1999. View at Publisher · View at Google Scholar
  131. P. J. Sansonetti, “Phagocytosis, a cell biology view,” Journal of Cell Science, vol. 113, part 19, pp. 3355–3356, 2000. View at Google Scholar
  132. A. Pitt, L. S. Mayorga, P. D. Stahl, and A. L. Schwartz, “Alterations in the protein composition of maturing phagosomes,” Journal of Clinical Investigation, vol. 90, no. 5, pp. 1978–1983, 1992. View at Google Scholar · View at Scopus
  133. T. E. Tjelle, T. Løvdal, and T. Berg, “Phagosome dynamics and function,” BioEssays, vol. 22, no. 3, pp. 255–263, 2000. View at Publisher · View at Google Scholar
  134. H. Tapper, “Out of the phagocyte or into its phagosome: signalling to secretion,” European Journal of Haematology, vol. 57, no. 3, pp. 191–201, 1996. View at Google Scholar · View at Scopus
  135. A. W. Segal, “How neutrophils kill microbes,” Annual Review of Immunology, vol. 23, pp. 197–223, 2005. View at Publisher · View at Google Scholar · View at Scopus
  136. W. L. Lee, R. E. Harrison, and S. Grinstein, “Phagocytosis by neutrophils,” Microbes and Infection, vol. 5, no. 14, pp. 1299–1306, 2003. View at Publisher · View at Google Scholar · View at Scopus
  137. S. Duclos and M. Desjardins, “Subversion of a young phagosome: the survival strategies of intracellular pathogens,” Cellular Microbiology, vol. 2, no. 5, pp. 365–377, 2000. View at Publisher · View at Google Scholar · View at Scopus
  138. J. Gruenberg and F. G. Van Der Goot, “Mechanisms of pathogen entry through the endosomal compartments,” Nature Reviews Molecular Cell Biology, vol. 7, no. 7, pp. 495–504, 2006. View at Publisher · View at Google Scholar · View at Scopus
  139. J. M. Davis, H. Clay, J. L. Lewis, N. Ghori, P. Herbomel, and L. Ramakrishnan, “Real-time visualization of Mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos,” Immunity, vol. 17, no. 6, pp. 693–702, 2002. View at Publisher · View at Google Scholar · View at Scopus
  140. L. M. Stamm, J. H. Morisaki, L. Y. Gao et al., “Mycobacterium marinum escapes from phagosomes and is propelled by actin-based motility,” Journal of Experimental Medicine, vol. 198, no. 9, pp. 1361–1368, 2003. View at Publisher · View at Google Scholar · View at Scopus
  141. N. van der Wel, D. Hava, D. Houben et al., “M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells,” Cell, vol. 129, no. 7, pp. 1287–1298, 2007. View at Publisher · View at Google Scholar · View at Scopus
  142. B. Levine, N. Mizushima, and H. W. Virgin, “Autophagy in immunity and inflammation,” Nature, vol. 469, no. 7330, pp. 323–335, 2011. View at Publisher · View at Google Scholar · View at Scopus
  143. E. Itakura, C. Kishi, K. Inoue, and N. Mizushima, “Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG,” Molecular Biology of the Cell, vol. 19, no. 12, pp. 5360–5372, 2008. View at Publisher · View at Google Scholar · View at Scopus
  144. H. Nakatogawa, J. Ishii, E. Asai, and Y. Ohsumi, “Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis,” Autophagy, vol. 8, no. 2, 2012. View at Publisher · View at Google Scholar
  145. M. A. Sanjuan and D. R. Green, “Eating for good health: linking autophagy and phagocytosis in host defense,” Autophagy, vol. 4, no. 5, pp. 607–611, 2008. View at Google Scholar · View at Scopus
  146. M. Ponpuak, A. S. Davis, E. A. Roberts et al., “Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties,” Immunity, vol. 32, no. 3, pp. 329–341, 2010. View at Publisher · View at Google Scholar · View at Scopus
  147. R. Sumpter and B. Levine, “Autophagy and innate immunity: triggering, targeting and tuning,” Seminars in Cell and Developmental Biology, vol. 21, no. 7, pp. 699–711, 2010. View at Publisher · View at Google Scholar · View at Scopus
  148. C. Hall, M. V. Flores, A. Chien, A. Davidson, K. Crosier, and P. Crosier, “Transgenic zebrafish reporter lines reveal conserved Toll-like receptor signaling potential in embryonic myeloid leukocytes and adult immune cell lineages,” Journal of Leukocyte Biology, vol. 85, no. 5, pp. 751–765, 2009. View at Publisher · View at Google Scholar · View at Scopus
  149. D. Le Guyader, M. J. Redd, E. Colucci-Guyon et al., “Origins and unconventional behavior of neutrophils in developing zebrafish,” Blood, vol. 111, no. 1, pp. 132–141, 2008. View at Publisher · View at Google Scholar · View at Scopus
  150. E. Colucci-Guyon, J.-Y. Tinevez, S. A. Renshaw, and P. Herbomel, “Strategies of professional phagocytes in vivo: unlike macrophages, neutrophils engulf only surface-associated microbes,” Journal of Cell Science, vol. 124, no. 18, pp. 3053–3059, 2011. View at Publisher · View at Google Scholar
  151. J. Ulvila, L. M. Vanha-Aho, A. Kleino et al., “Cofilin regulator 14-3-3ζ is an evolutionarily conserved protein required for phagocytosis and microbial resistance,” Journal of Leukocyte Biology, vol. 89, no. 5, pp. 649–659, 2011. View at Publisher · View at Google Scholar · View at Scopus
  152. C. He, C. R. Bartholomew, W. Zhou, and D. J. Klionsky, “Assaying autophagic activity in transgenic GFP-Lc3 and GFP-Gabarap zebrafish embryos,” Autophagy, vol. 5, no. 4, pp. 520–526, 2009. View at Publisher · View at Google Scholar · View at Scopus
  153. A. Lu, X. Hu, J. Xue, J. Zhu, Y. Wang, and G. Zhou, “Gene expression profiling in the skin of zebrafish infected with Citrobacter freundii,” Fish and Shellfish Immunology, vol. 32, no. 2, pp. 273–283, 2012. View at Publisher · View at Google Scholar
  154. C. Delclaux, C. Delacourt, M. P. D'Ortho, V. Boyer, C. Lafuma, and A. Harf, “Role of gelatinase B and elastase in human polymorphonuclear neutrophil migration across basement membrane,” American Journal of Respiratory Cell and Molecular Biology, vol. 14, no. 3, pp. 288–295, 1996. View at Google Scholar · View at Scopus
  155. H. Sengelov, L. Kjeldsen, and N. Borregaard, “Control of exocytosis in early neutrophil activation,” Journal of Immunology, vol. 150, no. 4, pp. 1535–1543, 1993. View at Google Scholar · View at Scopus
  156. K. A. Joiner, T. Ganz, J. Albert, and D. Rotrosen, “The opsonizing ligand on Salmonella typhimurium influences incorporation of specific, but not azurophil, granule constituents into neutrophil phagosomes,” Journal of Cell Biology, vol. 109, no. 6 I, pp. 2771–2782, 1989. View at Publisher · View at Google Scholar · View at Scopus
  157. M. Faurschou and N. Borregaard, “Neutrophil granules and secretory vesicles in inflammation,” Microbes and Infection, vol. 5, no. 14, pp. 1317–1327, 2003. View at Publisher · View at Google Scholar · View at Scopus
  158. C. Zhang, J. Yang, J. D. Jacobs, and L. K. Jennings, “Interaction of myeloperoxidase with vascular NAD(P)H oxidase-derived reactive oxygen species in vasculature: implications for vascular diseases,” American Journal of Physiology, Heart and Circulatory Physiology, vol. 285, no. 6, pp. H2563–H2572, 2003. View at Google Scholar · View at Scopus
  159. V. Brinkmann, U. Reichard, C. Goosmann et al., “Neutrophil extracellular traps kill bacteria,” Science, vol. 303, no. 5663, pp. 1532–1535, 2004. View at Publisher · View at Google Scholar · View at Scopus
  160. J. D. Lambeth, “NOX enzymes and the biology of reactive oxygen,” Nature Reviews Immunology, vol. 4, no. 3, pp. 181–189, 2004. View at Google Scholar · View at Scopus
  161. B. M. Babior, “The activity of leukocyte NADPH oxidase: regulation by p47PHOX cysteine and serine residues,” Antioxidants and Redox Signaling, vol. 4, no. 1, pp. 35–38, 2002. View at Google Scholar · View at Scopus
  162. D. Roos and C. C. Winterbourn, “Immunology: lethal weapons,” Science, vol. 296, no. 5568, pp. 669–671, 2002. View at Publisher · View at Google Scholar · View at Scopus
  163. E. Peranzoni, I. Marigo, L. Dolcetti et al., “Role of arginine metabolism in immunity and immunopathology,” Immunobiology, vol. 212, no. 9-10, pp. 795–812, 2008. View at Publisher · View at Google Scholar · View at Scopus
  164. C. Bogdan, “Nitric oxide and the immune response,” Nature Immunology, vol. 2, no. 10, pp. 907–916, 2001. View at Publisher · View at Google Scholar · View at Scopus
  165. S. El-Gayar, H. Thüring-Nahler, J. Pfeilschifter, M. Röllinghoff, and C. Bogdan, “Translational control of inducible nitric oxide synthase by IL-13 and arginine availability in inflammatory macrophages,” Journal of Immunology, vol. 171, no. 9, pp. 4561–4568, 2003. View at Google Scholar · View at Scopus
  166. G. Wu and S. M. Morris, “Arginine metabolism: nitric oxide and beyond,” Biochemical Journal, vol. 336, no. 1, pp. 1–17, 1998. View at Google Scholar · View at Scopus
  167. S. Pfeiffer, A. Lass, K. Schmidt, and B. Mayer, “Protein tyrosine nitration in cytokine-activated murine macrophages. Involvement of a peroxidase/nitrite pathway rather than peroxynitrite,” Journal of Biological Chemistry, vol. 276, no. 36, pp. 34051–34058, 2001. View at Publisher · View at Google Scholar · View at Scopus
  168. C. J. Hall, M. V. Flores, S. H. Oehlers et al., “Infection-responsive expansion of the hematopoietic stem and progenitor cell compartment in zebrafish is dependent upon inducible nitric oxide,” Cell Stem Cell, vol. 10, no. 2, pp. 198–209, 2012. View at Publisher · View at Google Scholar
  169. J. Arnhold and J. Flemmig, “Human myeloperoxidase in innate and acquired immunity,” Archives of Biochemistry and Biophysics, vol. 500, no. 1, pp. 92–106, 2010. View at Publisher · View at Google Scholar · View at Scopus
  170. J. D. Shearer, J. R. Richards, C. D. Mills, and M. D. Caldwell, “Differential regulation of macrophage arginine metabolism: a proposed role in wound healing,” American Journal of Physiology, Endocrinology and Metabolism, vol. 272, no. 2, pp. E181–E190, 1997. View at Google Scholar · View at Scopus
  171. J. R. Mathias, B. J. Perrin, T. X. Liu, J. Kanki, A. T. Look, and A. Huttenlocher, “Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish,” Journal of Leukocyte Biology, vol. 80, no. 6, pp. 1281–1288, 2006. View at Publisher · View at Google Scholar · View at Scopus
  172. P. Niethammer, C. Grabher, A. T. Look, and T. J. Mitchison, “A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish,” Nature, vol. 459, no. 7249, pp. 996–999, 2009. View at Publisher · View at Google Scholar · View at Scopus
  173. Q. Deng, E. A. Harvie, and A. Huttenlocher, “Distinct signalling mechanisms mediate neutrophil attraction to bacterial infection and tissue injury,” Cellular Microbiology, vol. 14, no. 4, pp. 517–528, 2012. View at Publisher · View at Google Scholar
  174. S. K. Yoo, T. W. Starnes, Q. Deng, and A. Huttenlocher, “Lyn is a redox sensor that mediates leukocyte wound attraction in vivo,” Nature, vol. 480, no. 7375, pp. 109–112, 2011. View at Publisher · View at Google Scholar
  175. M. V. Flores, K. C. Crawford, L. M. Pullin, C. J. Hall, K. E. Crosier, and P. S. Crosier, “Dual oxidase in the intestinal epithelium of zebrafish larvae has anti-bacterial properties,” Biochemical and Biophysical Research Communications, vol. 400, no. 1, pp. 164–168, 2010. View at Publisher · View at Google Scholar · View at Scopus
  176. K. M. Brothers, Z. R. Newman, and R. T. Wheeler, “Live imaging of disseminated candidiasis in zebrafish reveals role of phagocyte oxidase in limiting filamentous growth,” Eukaryotic Cell, vol. 10, no. 7, pp. 932–944, 2011. View at Publisher · View at Google Scholar · View at Scopus
  177. Y. Feng, C. Santoriello, M. Mione, A. Hurlstone, and P. Martin, “Live imaging of innate immune cell sensing of transformed cells in zebrafish larvae: parallels between tumor initiation and wound inflammation,” PLoS Biology, vol. 8, no. 12, Article ID e1000562, 2010. View at Publisher · View at Google Scholar · View at Scopus
  178. A. C. Hermann, P. J. Millard, S. L. Blake, and C. H. Kim, “Development of a respiratory burst assay using zebrafish kidneys and embryos,” Journal of Immunological Methods, vol. 292, no. 1-2, pp. 119–129, 2004. View at Publisher · View at Google Scholar · View at Scopus
  179. S. Lepiller, V. Laurens, A. Bouchot, P. Herbomel, E. Solary, and J. Chluba, “Imaging of nitric oxide in a living vertebrate using a diaminofluorescein probe,” Free Radical Biology and Medicine, vol. 43, no. 4, pp. 619–627, 2007. View at Publisher · View at Google Scholar
  180. P. M. Elks, F. J. Van Eeden, G. Dixon et al., “Activation of hypoxia-inducible factor-1α (hif-1α) delays inflammation resolution by reducing neutrophil apoptosis and reverse migration in a zebrafish inflammation model,” Blood, vol. 118, no. 3, pp. 712–722, 2011. View at Publisher · View at Google Scholar · View at Scopus
  181. M. De Jong, H. Rauwerda, O. Bruning, J. Verkooijen, H. P. Spaink, and T. M. Breit, “RNA isolation method for single embryo transcriptome analysis in zebrafish,” BMC Research Notes, vol. 3, article no. 73, 2010. View at Publisher · View at Google Scholar · View at Scopus
  182. A. H. Meijer, F. J. Verbeek, E. Salas-Vidal et al., “Transcriptome profiling of adult zebrafish at the late stage of chronic tuberculosis due to Mycobacterium marinum infection,” Molecular Immunology, vol. 42, no. 10, pp. 1185–1203, 2005. View at Publisher · View at Google Scholar · View at Scopus
  183. Z. Wu, W. Zhang, Y. Lu, and C. Lu, “Transcriptome profiling of zebrafish infected with Streptococcus suis,” Microbial Pathogenesis, vol. 48, no. 5, pp. 178–187, 2010. View at Publisher · View at Google Scholar · View at Scopus
  184. P. S. Srinivasa Rao, T. M. Lim, and K. Y. Leung, “Functional genomics approach to the identification of virulence genes involved in Edwardsiella tardapathogenesis,” Infection and Immunity, vol. 71, no. 3, pp. 1343–1351, 2003. View at Publisher · View at Google Scholar · View at Scopus
  185. A. M. van der Sar, R. J. P. Musters, F. J. M. van Eeden, B. J. Appelmelk, C. M. J. E. Vandenbroucke-Grauls, and W. Bitter, “Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections,” Cellular Microbiology, vol. 5, no. 9, pp. 601–611, 2003. View at Publisher · View at Google Scholar · View at Scopus
  186. D. M. Tobin and L. Ramakrishnan, “Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis,” Cellular Microbiology, vol. 10, no. 5, pp. 1027–1039, 2008. View at Publisher · View at Google Scholar · View at Scopus
  187. H. E. Volkman, H. Clay, D. Beery, J. C. W. Chang, D. R. Sherman, and L. Ramakrishnan, “Tuberculous granuloma formation is enhanced by a Mycobacterium virulence determinant,” PLoS Biology, vol. 2, no. 11, article e367, 2004. View at Publisher · View at Google Scholar · View at Scopus
  188. H. Clay, J. M. Davis, D. Beery, A. Huttenlocher, S. E. Lyons, and L. Ramakrishnan, “Dichotomous Role of the Macrophage in Early Mycobacterium marinum Infection of the Zebrafish,” Cell Host and Microbe, vol. 2, no. 1, pp. 29–39, 2007. View at Publisher · View at Google Scholar · View at Scopus
  189. K. Spilsbury, M. A. O'Mara, Wan Man Wu, P. B. Rowe, G. Symonds, and Y. Takayama, “Isolation of a novel macrophage-specific gene by differential cDNA analysis,” Blood, vol. 85, no. 6, pp. 1620–1629, 1995. View at Google Scholar · View at Scopus
  190. B. Chen, D. Zhang, and J. W. Pollard, “Progesterone regulation of the mammalian ortholog of methylcitrate dehydratase (Immune Response Gene 1) in the uterine epithelium during implantation through the protein kinase C pathway,” Molecular Endocrinology, vol. 17, no. 11, pp. 2340–2354, 2003. View at Publisher · View at Google Scholar · View at Scopus
  191. H. T. Tran, N. Barnich, and E. Mizoguchi, “Potential role of chitinases and chitin-binding proteins in host-microbial interactions during the development of intestinal inflammation,” Histology and Histopathology, vol. 26, no. 11, pp. 1453–1464, 2011. View at Google Scholar
  192. R. Carvalho, J. de Sonneville, O. W. Stockhammer et al., “A high-throughput screen for tuberculosis progression,” PLoS One, vol. 6, no. 2, Article ID e16779, 2011. View at Publisher · View at Google Scholar
  193. E. J. M. Stoop, T. Schipper, S. K. Rosendahl Huber et al., “Zebrafish embryo screen for mycobacterial genes involved in the initiation of granuloma formation reveals a newly identified ESX-1 component,” Disease Models and Mechanisms, vol. 4, no. 4, pp. 526–536, 2011. View at Publisher · View at Google Scholar · View at Scopus
  194. M. G. Morash, S. E. Douglas, A. Robotham, C. M. Ridley, J. W. Gallant, and K. H. Soanes, “The zebrafish embryo as a tool for screening and characterizing pleurocidin host-defense peptides as anti-cancer agents,” Disease Models and Mechanisms, vol. 4, no. 5, pp. 622–633, 2011. View at Publisher · View at Google Scholar
  195. G. F. Wiegertjes and M. Forlenza, “Nitrosative stress during infection-induced inflammation in fish: lessons from a host-parasite infection model,” Current Pharmaceutical Design, vol. 16, no. 38, pp. 4194–4202, 2010. View at Publisher · View at Google Scholar · View at Scopus
  196. F. O. Martinez, L. Helming, and S. Gordon, “Alternative activation of macrophages: an immunologic functional perspective,” Annual Review of Immunology, vol. 27, pp. 451–483, 2009. View at Publisher · View at Google Scholar · View at Scopus
  197. Z. G. Fridlender, J. Sun, S. Kim et al., “Polarization of tumor-associated neutrophil phenotype by TGF-β: “N1” versus “N2” TAN,” Cancer Cell, vol. 16, no. 3, pp. 183–194, 2009. View at Publisher · View at Google Scholar · View at Scopus
  198. A. H. Meijer, A. M. van der Sar, C. Cunha et al., “Identification and real-time imaging of a myc-expressing neutrophil population involved in inflammation and mycobacterial granuloma formation in zebrafish,” Developmental and Comparative Immunology, vol. 32, no. 1, pp. 36–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  199. A. J. Sadler, O. Latchoumanin, D. Hawkes, J. Mak, and B. R. G. Williams, “An antiviral response directed by PKR phosphorylation of the RNA helicase A,” PLoS Pathogens, vol. 5, no. 2, Article ID e1000311, 2009. View at Publisher · View at Google Scholar · View at Scopus
  200. A. Takaoka, Z. Wang, M. K. Choi et al., “DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response,” Nature, vol. 448, no. 7152, pp. 501–505, 2007. View at Publisher · View at Google Scholar · View at Scopus
  201. V. Hornung, A. Ablasser, M. Charrel-Dennis et al., “AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC,” Nature, vol. 458, no. 7237, pp. 514–518, 2009. View at Publisher · View at Google Scholar · View at Scopus
  202. V. Deretic, “Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors,” Current Opinion in Immunology, vol. 24, no. 1, pp. 21–31, 2012. View at Publisher · View at Google Scholar
  203. D. M. Tobin, R. C. May, and R. T. Wheeler, “Zebrafish: a see-through host and a fluorescent toolbox to probe host-pathogen interaction,” PLoS Pathogens, vol. 8, no. 1, Article ID e1002349, 2012. View at Publisher · View at Google Scholar
  204. S. A. Renshaw and N. S. Trede, “A model 450 million years in the making: zebrafish and vertebrate immunity,” Disease Models and Mechanisms, vol. 5, no. 1, pp. 38–47, 2012. View at Publisher · View at Google Scholar
  205. K. J. Clark, D. F. Voytas, and S. C. Ekker, “A Tale of two nucleases: gene targeting for the masses?” Zebrafish, vol. 8, no. 3, pp. 147–149, 2011. View at Publisher · View at Google Scholar