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Journal of Immunology Research
Volume 2015 (2015), Article ID 960859, 19 pages
http://dx.doi.org/10.1155/2015/960859
Review Article

A Review of Intra- and Extracellular Antigen Delivery Systems for Virus Vaccines of Finfish

Section of Aquatic Medicine and Nutrition, Department of Basic Sciences and Aquatic Medicine, Faculty of Veterinary Medicine and Biosciences, Norwegian University of Life Sciences, Ullevalsveien 72, P.O. Box 8146, 0033 Oslo, Norway

Received 28 October 2014; Revised 8 April 2015; Accepted 9 April 2015

Academic Editor: Kurt Blaser

Copyright © 2015 Hetron Mweemba Munang’andu and Øystein Evensen. 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. G. A. Bishop, S. A. Haxhinasto, L. L. Stunz, and B. S. Hostager, “Antigen-specific B-lymphocyte activation,” Critical Reviews in Immunology, vol. 23, no. 3, pp. 149–197, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. R. N. Germain, “MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation,” Cell, vol. 76, no. 2, pp. 287–299, 1994. View at Publisher · View at Google Scholar · View at Scopus
  3. V. Schuette and S. Burgdorf, “The ins-and-outs of endosomal antigens for cross-presentation,” Current Opinion in Immunology, vol. 26, no. 1, pp. 63–68, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. E. Segura and J. A. Villadangos, “A modular and combinatorial view of the antigen cross-presentation pathway in dendritic cells,” Traffic, vol. 12, no. 12, pp. 1677–1685, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Ciechanover, “Intracellular protein degradation: from a vague idea, through the lysosome and the ubiquitin-proteasome system, and onto human diseases and drug targeting (Nobel Lecture),” Angewandte Chemie - International Edition, vol. 44, no. 37, pp. 5944–5967, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Uebel and R. Tampé, “Specificity of the proteasome and the TAP transporter,” Current Opinion in Immunology, vol. 11, no. 2, pp. 203–208, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. J.-O. Koopmann, M. Post, J. J. Neefjes, G. J. Hämmerling, and F. Momburg, “Translocation of long peptides by transporters associated with antigen processing (TAP),” European Journal of Immunology, vol. 26, no. 8, pp. 1720–1728, 1996. View at Publisher · View at Google Scholar · View at Scopus
  8. J. O. Koopmann, G. J. Hämmerling, and F. Momburg, “Generation, intracellular transport and loading of peptides associated with MHC class I molecules,” Current Opinion in Immunology, vol. 9, no. 1, pp. 80–88, 1997. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Pamer and P. Cresswell, “Mechanisms of MHC class I—restricted antigen processing,” Annual Review of Immunology, vol. 16, pp. 323–358, 1998. View at Publisher · View at Google Scholar · View at Scopus
  10. N. Mizushima and D. J. Klionsky, “Protein turnover via autophagy: implications for metabolism,” Annual Review of Nutrition, vol. 27, pp. 19–40, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Münz, “Antigen processing via autophagy—not only for MHC class II presentation anymore?” Current Opinion in Immunology, vol. 22, no. 1, pp. 89–93, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. G. T. Haugland, A. E. O. Jordal, and H. I. Wergeland, “Characterization of small, mononuclear blood cells from salmon having high phagocytic capacity and ability to differentiate into dendritic like cells,” PLoS ONE, vol. 7, no. 11, Article ID e49260, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. D. B. Iliev, H. Thim, L. Lagos, R. Olsen, and J. B. Jørgensen, “Homing of antigen-presenting cells in head kidney and spleen—salmon head kidney hosts diverse APC types,” Frontiers in Immunology, vol. 4, article 137, Article ID Article 137, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Lugo-Villarino, K. M. Balla, D. L. Stachura, K. Bañuelos, M. B. F. Werneck, and D. Traver, “Identification of dendritic antigen-presenting cells in the zebrafish,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 36, pp. 15850–15855, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. D. T. Fearon and R. M. Locksley, “The instructive role of innate immunity in the acquired immune response,” Science, vol. 272, no. 5258, pp. 50–54, 1996. View at Publisher · View at Google Scholar · View at Scopus
  16. 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
  17. 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
  18. S. MacKenzie, J. V. Planas, and F. W. Goetz, “LPS-stimulated expression of a tumor necrosis factor-alpha mRNA in primary trout monocytes and in vitro differentiated macrophages,” Developmental and Comparative Immunology, vol. 27, no. 5, pp. 393–400, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. J. L. Stafford, P. E. McLauchlan, C. J. Secombes, A. E. Ellis, and M. Belosevic, “Generation of primary monocyte-like cultures from rainbow trout head kidney leukocytes,” Developmental and Comparative Immunology, vol. 25, no. 5-6, pp. 447–459, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. F. W. Goetz, D. B. Iliev, L. A. R. McCauley et al., “Analysis of genes isolated from lipopolysaccharide-stimulated rainbow trout (Oncorhynchus mykiss) macrophages,” Molecular Immunology, vol. 41, no. 12, pp. 1199–1210, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. D. B. Iliev, C. Q. Liarte, S. MacKenzie, and F. W. Goetz, “Activation of rainbow trout (Oncorhynchus mykiss) mononuclear phagocytes by different pathogen associated molecular pattern (PAMP) bearing agents,” Molecular Immunology, vol. 42, no. 10, pp. 1215–1223, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. D. B. Iliev, G. W. Goetz, S. MacKenzie, J. V. Planas, and F. W. Goetz, “Pathogen-associated gene expression profiles in rainbow trout macrophages,” Comparative Biochemistry and Physiology Part D: Genomics & Proteomics, vol. 1, no. 4, pp. 416–422, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. E. F. Pettersen, H.-C. Ingerslev, V. Stavang, M. Egenberg, and H. I. Wergeland, “A highly phagocytic cell line TO from Atlantic salmon is CD83 positive and M-CSFR negative, indicating a dendritic-like cell type,” Fish & Shellfish Immunology, vol. 25, no. 6, pp. 809–819, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. H. I. Wergeland and R. A. Jakobsen, “A salmonid cell line (TO) for production of infectious salmon anaemia virus (ISAV),” Diseases of Aquatic Organisms, vol. 44, no. 3, pp. 183–190, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Xu, Ø. Evensen, and H. M. Munang’andu, “De novo assembly and transcriptome analysis of Atlantic salmon macrophage/dendritic-like TO cells following type I IFN treatment and Salmonid alphavirus subtype-3 infection,” BMC Genomics, vol. 16, no. 1, 2015. View at Publisher · View at Google Scholar
  26. E. Bassity and T. G. Clark, “Functional identification of dendritic cells in the teleost model, rainbow trout (Oncorhynchus mykiss),” PLoS ONE, vol. 7, no. 3, Article ID e33196, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. J. O. Sunyer, “Evolutionary and functional relationships of B cells from fish and mammals: insights into their novel roles in phagocytosis and presentation of particulate antigen,” Infectious Disorders—Drug Targets, vol. 12, no. 3, pp. 200–212, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Ohta, D. E. Haliniewski, J. Hansen, and M. F. Flajnik, “Isolation of transporter associated with antigen processing genes, TAP1 and TAP2, from the horned shark Heterodontus francisci,” Immunogenetics, vol. 49, no. 11-12, pp. 981–986, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Ohta, S. J. Powis, W. J. Coadwell et al., “Identification and genetic mapping of Xenopus TAP2 genes,” Immunogenetics, vol. 49, no. 3, pp. 171–182, 1999. View at Publisher · View at Google Scholar · View at Scopus
  30. J. D. Hansen, P. Strassburger, G. H. Thorgaard, W. P. Young, and L. Du Pasquier, “Expression, linkage, and polymorphism of MHC-related genes in rainbow trout, Oncorhynchus mykiss,” Journal of Immunology, vol. 163, no. 2, pp. 774–786, 1999. View at Google Scholar · View at Scopus
  31. U. Grimholt, “Transport-associated proteins in Atlantic salmon (Salmo salar),” Immunogenetics, vol. 46, no. 3, pp. 213–221, 1997. View at Publisher · View at Google Scholar · View at Scopus
  32. U. H. von Andrian and T. R. Mempel, “Homing and cellular traffic in lymph nodes,” Nature Reviews Immunology, vol. 3, no. 11, pp. 867–878, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. C. M. Press and Ø. Evensen, “The morphology of the immune system in teleost fishes,” Fish and Shellfish Immunology, vol. 9, no. 4, pp. 309–318, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. I. Mulero, M. Pilar Sepulcre, F. J. Roca, J. Meseguer, A. García-Ayala, and V. Mulero, “Characterization of macrophages from the bony fish gilthead seabream using an antibody against the macrophage colony-stimulating factor receptor,” Developmental and Comparative Immunology, vol. 32, no. 10, pp. 1151–1159, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. C. Peleteiro and R. H. Richards, “Phagocytic-cells in the epidermis of rainbow-trout, Salmo-Gairdneri Richardson,” Journal of Fish Diseases, vol. 13, no. 3, pp. 225–232, 1990. View at Google Scholar
  36. B. Fuglem, E. Jirillo, I. Bjerkås et al., “Antigen-sampling cells in the salmonid intestinal epithelium,” Developmental and Comparative Immunology, vol. 34, no. 7, pp. 768–774, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. J. H. W. M. Rombout, C. H. J. Lamers, M. H. Helfrich, A. Dekker, and J. J. Taverne-Thiele, “Uptake and transport of intact macromolecules in the intestinal epithelium of carp (Cyprinus carpio L.) and the possible immunological implications,” Cell and Tissue Research, vol. 239, no. 3, pp. 519–530, 1985. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Alejo and C. Tafalla, “Chemokines in teleost fish species,” Developmental and Comparative Immunology, vol. 35, no. 12, pp. 1215–1222, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. K. J. Laing and C. J. Secombes, “Chemokines,” Developmental and Comparative Immunology, vol. 28, no. 5, pp. 443–460, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. C. J. Secombes, T. Wang, S. Hong et al., “Cytokines and innate immunity of fish,” Developmental and Comparative Immunology, vol. 25, no. 8-9, pp. 713–723, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Tafalla, J. Coll, and C. J. Secombes, “Expression of genes related to the early immune response in rainbow trout (Oncorhynchus mykiss) after viral haemorrhagic septicemia virus (VHSV) infection,” Developmental and Comparative Immunology, vol. 29, no. 7, pp. 615–626, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Doñate, N. Roher, J. C. Balasch et al., “CD83 expression in sea bream macrophages is a marker for the LPS-induced inflammatory response,” Fish & Shellfish Immunology, vol. 23, no. 4, pp. 877–885, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Johansson, Y. Corripio-Miyar, T. Wang, B. Collet, C. J. Secombes, and J. Zou, “Characterisation and expression analysis of the rainbow trout (Oncorhynchus mykiss) homologue of the human dendritic cell marker CD208/lysosomal associated membrane protein 3,” Developmental and Comparative Immunology, vol. 37, no. 3-4, pp. 402–413, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. L.-Y. Zhu, A.-F. Lin, T. Shao et al., “B cells in teleost fish act as pivotal initiating APCs in priming adaptive immunity: an evolutionary perspective on the origin of the B-1 cell subset and B7 molecules,” The Journal of Immunology, vol. 192, no. 6, pp. 2699–2714, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Abós, R. Castro, G. A. Granja et al., “Early activation of teleost B cells in response to rhabdovirus infection,” Journal of Virology, vol. 89, no. 3, pp. 1768–1780, 2015. View at Publisher · View at Google Scholar
  46. A. Pellegrini, N. Guiñazú, M. P. Aoki et al., “Spleen B cells from BALB/c are more prone to activation than spleen B cells from C57BL/6 mice during a secondary immune response to cruzipain,” International Immunology, vol. 19, no. 12, pp. 1395–1402, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Bernard, B. Riteau, J. D. Hansen et al., “Costimulatory receptors in a teleost fish: typical CD28, elusive CTLA4,” The Journal of Immunology, vol. 176, no. 7, pp. 4191–4200, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. D. Bernard, J. D. Hansen, L. Du Pasquier, M.-P. Lefranc, A. Benmansour, and P. Boudinot, “Costimulatory receptors in jawed vertebrates: conserved CD28, odd CTLA4 and multiple BTLAs,” Developmental and Comparative Immunology, vol. 31, no. 3, pp. 255–271, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. Y.-T. Chang, Y.-H. Kai, S.-C. Chi, and Y.-L. Song, “Cytotoxic CD8α+ leucocytes have heterogeneous features in antigen recognition and class I MHC restriction in grouper,” Fish & Shellfish Immunology, vol. 30, no. 6, pp. 1283–1293, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. U. Fischer, K. Utke, M. Ototake, J. M. Dijkstra, and B. Köllner, “Adaptive cell-mediated cytotoxicity against allogeneic targets by CD8-positive lymphocytes of rainbow trout (Oncorhynchus mykiss),” Developmental and Comparative Immunology, vol. 27, no. 4, pp. 323–337, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. H. M. Munang'andu, B. N. Fredriksen, S. Mutoloki, R. A. Dalmo, and Ø. Evensen, “The kinetics of CD4+ and CD8+ T-cell gene expression correlate with protection in Atlantic salmon (Salmo salar L) vaccinated against infectious pancreatic necrosis,” Vaccine, vol. 31, no. 15, pp. 1956–1963, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Nakanishi, U. Fischer, J. M. Dijkstra et al., “Cytotoxic T cell function in fish,” Developmental and Comparative Immunology, vol. 26, no. 2, pp. 131–139, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Nakanishi, H. Toda, Y. Shibasaki, and T. Somamoto, “Cytotoxic T cells in teleost fish,” Developmental and Comparative Immunology, vol. 35, no. 12, pp. 1317–1323, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Somamoto, T. Nakanishi, and N. Okamoto, “Specific cell-mediated cytotoxicity against a virus-infected syngeneic cell line in isogeneic ginbuna crucian carp,” Developmental and Comparative Immunology, vol. 24, no. 6-7, pp. 633–640, 2000. View at Publisher · View at Google Scholar · View at Scopus
  55. E. Andersson and T. Matsunaga, “Complete cDNA sequence of a rainbow trout IgM gene and evolution of vertebrate IgM constant domains,” Immunogenetics, vol. 38, no. 4, pp. 243–250, 1993. View at Google Scholar · View at Scopus
  56. I. Hordvik, A. M. Voie, J. Glette, R. Male, and C. Endresen, “Cloning and sequence analysis of two isotypic IgM heavy chain genes from Atlantic salmon, Salmo salar L,” European Journal of Immunology, vol. 22, no. 11, pp. 2957–2962, 1992. View at Publisher · View at Google Scholar · View at Scopus
  57. I. Hordvik, J. Thevarajan, I. Samdal, N. Bastani, and B. Krossøy, “Molecular cloning and phylogenetic analysis of the Atlantic salmon immunoglobulin D gene,” Scandinavian Journal of Immunology, vol. 50, no. 2, pp. 202–210, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. J. D. Hansen, E. D. Landis, and R. B. Phillips, “Discovery of a unique Ig heavy-chain (IgT) in rainbow trout: implications for a distinctive B cell developmental pathway in teleost fish,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 19, pp. 6919–6924, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. E. Bromage, F. Ramirez-Gomez, W. Greene et al., “Secretory IgD has an evolutionarily conserved role in respiratory mucosal defense,” The Journal of Immunology, vol. 188, 2012. View at Google Scholar
  60. F. Ramirez-Gomez, W. Greene, K. Rego et al., “Discovery and characterization of secretory IgD in rainbow trout: secretory IgD is produced through a novel splicing mechanism,” Journal of Immunology, vol. 188, no. 3, pp. 1341–1349, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. D. Parra, F. Takizawa, and J. O. Sunyer, “Evolution of B cell immunity,” Annual Review of Animal Biosciences, vol. 1, no. 1, pp. 65–97, 2013. View at Publisher · View at Google Scholar
  62. Y.-A. Zhang, I. Salinas, J. Li et al., “IgT, a primitive immunoglobulin class specialized in mucosal immunity,” Nature Immunology, vol. 11, no. 9, pp. 827–835, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. Z. Xu, D. Gomez, D. Parra, F. Takizawa, and J. O. Sunyer, “IgT plays a prominent role in gill immune response of rainbow trout,” Fish & Shellfish Immunology, vol. 34, no. 6, 1686 pages, 2013. View at Publisher · View at Google Scholar
  64. J. Banchereau, F. Bazan, D. Blanchard et al., “The CD40 antigen and its ligand,” Annual Review of Immunology, vol. 12, pp. 881–922, 1994. View at Publisher · View at Google Scholar · View at Scopus
  65. L. X. Lagos, D. B. Iliev, R. Helland, M. Rosemblatt, and J. B. Jørgensen, “CD40L—a costimulatory molecule involved in the maturation of antigen presenting cells in Atlantic salmon (Salmo salar L),” Developmental and Comparative Immunology, vol. 38, no. 3, pp. 416–430, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. F. Takizawa, K. Araki, M. Ohtani et al., “Transcription analysis of two Eomesodermin genes in lymphocyte subsets of two teleost species,” Fish & Shellfish Immunology, vol. 36, no. 1, pp. 215–222, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. T. Wang, J. W. Holland, S. A. M. Martin, and C. J. Secombes, “Sequence and expression analysis of two T helper master transcription factors, T-bet and GATA3, in rainbow trout Oncorhynchus mykiss and analysis of their expression during bacterial and parasitic infection,” Fish & Shellfish Immunology, vol. 29, no. 5, pp. 705–715, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. H. Chi, Z. Zhang, M. Inami, J. Bøgwald, W. Zhan, and R. A. Dalmo, “Molecular characterizations and functional assessments of GATA-3 and its splice variant in Atlantic cod (Gadus morhua L.),” Developmental and Comparative Immunology, vol. 36, no. 3, pp. 491–501, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Kumari, J. Bogwald, and R. A. Dalmo, “Transcription factor GATA-3 in Atlantic salmon (Salmo salar): molecular characterization, promoter activity and expression analysis,” Molecular Immunology, vol. 46, no. 15, pp. 3099–3107, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. F. Takizawa, E. O. Koppang, M. Ohtani et al., “Constitutive high expression of interleukin-4/13A and GATA-3 in gill and skin of salmonid fishes suggests that these tissues form Th2-skewed immune environments,” Molecular Immunology, vol. 48, no. 12-13, pp. 1360–1368, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. L. Du, X. Yang, L. Yang, X. Wang, A. Zhang, and H. Zhou, “Molecular evidence for the involvement of RORα and RORγ in immune response in teleost,” Fish & Shellfish Immunology, vol. 33, no. 2, pp. 418–426, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. M. M. Monte, T. H. Wang, M. M. Costa, N. O. Harun, and C. J. Secombes, “Cloning and expression analysis of two ROR-γ homologues (ROR-γa1 and ROR-γa2) in rainbow trout Oncorhynchus mykiss,” Fish & Shellfish Immunology, vol. 33, no. 2, pp. 365–374, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. A. Rivas-Aravena, S. Guajardo, B. Valenzuela et al., “Ribavirin stimulates the immune response of Atlantic salmon,” Veterinary Immunology and Immunopathology, vol. 164, no. 1-2, pp. 93–100, 2015. View at Publisher · View at Google Scholar
  74. T. Wang, P. Diaz-Rosales, M. M. Costa et al., “Functional characterization of a nonmammalian IL-21: rainbow trout Oncorhynchus mykiss IL-21 upregulates the expression of the Th cell signature cytokines IFN-γ, IL-10, and IL-22,” The Journal of Immunology, vol. 186, no. 2, pp. 708–721, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. H. Zhou, T. B. Stuge, N. W. Miller et al., “Heterogeneity of channel catfish CTL with respect to target recognition and cytotoxic mechanisms employed,” The Journal of Immunology, vol. 167, no. 3, pp. 1325–1332, 2001. View at Publisher · View at Google Scholar · View at Scopus
  76. K. Utke, S. Bergmann, N. Lorenzen, B. Köllner, M. Ototake, and U. Fischer, “Cell-mediated cytotoxicity in rainbow trout, Oncorhynchus mykiss, infected with viral haemorrhagic septicaemia virus,” Fish & Shellfish Immunology, vol. 22, no. 3, pp. 182–196, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. Y. H. Kai, Y. C. Wu, and S. C. Chi, “Immune gene expressions in grouper larvae (Epinephelus coioides) induced by bath and oral vaccinations with inactivated betanodavirus,” Fish and Shellfish Immunology, vol. 40, no. 2, pp. 563–569, 2014. View at Google Scholar
  78. Y.-H. Kai and S.-C. Chi, “Efficacies of inactivated vaccines against betanodavirus in grouper larvae (Epinephelus coioides) by bath immunization,” Vaccine, vol. 26, no. 11, pp. 1450–1457, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. H.-C. Ingerslev, A. Rønneseth, E. F. Pettersen, and H. I. Wergeland, “Differential expression of immune genes in Atlantic salmon (Salmo salar L.) challenged intraperitoneally or by cohabitation with IPNV,” Scandinavian Journal of Immunology, vol. 69, no. 2, pp. 90–98, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. D. L. Hetland, S. M. Jørgensen, K. Skjødt et al., “In situ localisation of major histocompatibility complex class I and class II and CD8 positive cells in infectious salmon anaemia virus (ISAV)-infected Atlantic salmon,” Fish & Shellfish Immunology, vol. 28, no. 1, pp. 30–39, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. H. M. Munang'andu, B. N. Fredriksen, S. Mutoloki, R. A. Dalmo, and Ø. Evensen, “Antigen dose and humoral immune response correspond with protection for inactivated infectious pancreatic necrosis virus vaccines in Atlantic salmon (Salmo salar L),” Veterinary Research, vol. 44, no. 1, article 7, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. H. M. Munang'andu, A. Sandtrø, S. Mutoloki, B. E. Brudeseth, N. Santi, and Ø. Evensen, “Immunogenicity and cross protective ability of the central VP2 amino acids of infectious pancreatic necrosis virus in Atlantic salmon (Salmo salar L.),” PLoS ONE, vol. 8, no. 1, Article ID e54263, 2013. View at Publisher · View at Google Scholar · View at Scopus
  83. K. A. Roberti, J. S. Rohovec, and J. R. Winton, “Vaccination of rainbow trout against infectious hematopoietic necrosis (IHN) by using attenuated mutants selected by neutralizing monoclonal antibodies,” Journal of Aquatic Animal Health, vol. 10, no. 4, pp. 328–337, 1998. View at Publisher · View at Google Scholar · View at Scopus
  84. M. Adelmann, B. Köllner, S. M. Bergmann et al., “Development of an oral vaccine for immunisation of rainbow trout (Oncorhynchus mykiss) against viral haemorrhagic septicaemia,” Vaccine, vol. 26, no. 6, pp. 837–844, 2008. View at Publisher · View at Google Scholar · View at Scopus
  85. J. L. Fryer, J. S. Rohovec, G. L. Tebbit, J. S. McMichael, and K. S. Pilcher, “Vaccination for the control of infectious diseases in Pacific salmon,” Fish Pathology, vol. 10, no. 2, pp. 155–164, 1976. View at Google Scholar
  86. G. L. Tebbit, Viruses infecting salmonid fishes from Oregon. A. The occurence and distribution of infectious pancreatic necrosis virus; B. The development of an attenuated strain of infectious hematopoietic necrosis virus (IHNV) for the immunization of salmonids [Ph.D. thesis], Oregon State University, Corvallis, Ore, USA, 1976.
  87. J. C. Leong and J. L. Fryer, “Viral vaccines for aquaculture,” Annual Review of Fish Diseases, vol. 3, pp. 225–240, 1993. View at Publisher · View at Google Scholar · View at Scopus
  88. J. S. Rohovec, J. R. Winton, and J. L. Fryer, “Bacterins and vaccines for the control of infectious diseases of fish,” in Proceedings of the Republic of China-United State Cooperative Science Seminar on Fish diseases, NSC Symposium Series no. 3, National Science Council, Beijing, China, 1981.
  89. M. Dorson, J. Castric, and C. Torchy, “Infectious pancreatic necrosis virus of salmonids: biological and antigenic features of a pathogenic strain and of a non-pathogenic variant selected in RTG-2 cells,” Journal of Fish Diseases, vol. 1, no. 4, pp. 309–320, 1978. View at Publisher · View at Google Scholar
  90. M. I. Thoulouze, E. Bouguyon, C. Carpentier, and M. Brémont, “ssential role of the NV protein of Novirhabdovirus for pathogenicity in rainbow trout,” Journal of Virology, vol. 78, no. 8, pp. 4098–4107, 2004. View at Publisher · View at Google Scholar · View at Scopus
  91. A. Romero, A. Figueras, M.-I. Thoulouze, M. Bremont, and B. Novoa, “Recombinant infectious hematopoietic necrosis viruses induce protection for rainbow trout Oncorhynchus mykiss,” Diseases of Aquatic Organisms, vol. 80, no. 2, pp. 123–135, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. N. Santi, V. N. Vakharia, and Ø. Evensen, “Identification of putative motifs involved in the virulence of infectious pancreatic necrosis virus,” Virology, vol. 322, no. 1, pp. 31–40, 2004. View at Publisher · View at Google Scholar · View at Scopus
  93. S. Mutoloki, H. Munang'andu, and Ø. Evensen, “Clinical and subclinical forms of infectious pancreatic necrosis virus infections show specific viral genetic fingerprints that link differences in virulence to immunogenicity,” Fish & Shellfish Immunology, vol. 34, no. 6, p. 1667, 2013. View at Publisher · View at Google Scholar
  94. K. Gadan, A. Sandtrø, I. S. Marjara, N. Santi, H. M. Munang'andu, and Ø. Evensen, “Stress-induced reversion to virulence of infectious pancreatic necrosis virus in naive fry of Atlantic salmon (Salmo salar L.),” PLoS ONE, vol. 8, no. 2, Article ID e54656, 2013. View at Publisher · View at Google Scholar · View at Scopus
  95. P. Boudinot, M. Blanco, P. De Kinkelin, and A. Benmansour, “Combined DNA immunization with the glycoprotein gene of viral hemorrhagic septicemia virus and infectious hematopoietic necrosis virus induces double-specific protective immunity and nonspecific response in rainbow trout,” Virology, vol. 249, no. 2, pp. 297–306, 1998. View at Publisher · View at Google Scholar · View at Scopus
  96. K. Utke, H. Kock, H. Schuetze et al., “Cell-mediated immune responses in rainbow trout after DNA immunization against the viral hemorrhagic septicemia virus,” Developmental and Comparative Immunology, vol. 32, no. 3, pp. 239–252, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. R. Castro, S. Martínez-Alonso, U. Fischer et al., “DNA vaccination against a fish rhabdovirus promotes an early chemokine-related recruitment of B cells to the muscle,” Vaccine, vol. 32, no. 10, pp. 1160–1168, 2014. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Corbeil, S. E. Lapatra, E. D. Anderson, and G. Kurath, “Nanogram quantities of a DNA vaccine protect rainbow trout fry against heterologous strains of infectious hematopoietic necrosis virus,” Vaccine, vol. 18, no. 25, pp. 2817–2824, 2000. View at Publisher · View at Google Scholar · View at Scopus
  99. D. J. Shedlock and D. B. Weiner, “DNA vaccination: antigen presentation and the induction of immunity,” Journal of Leukocyte Biology, vol. 68, no. 6, pp. 793–806, 2000. View at Google Scholar · View at Scopus
  100. F. Fu, Y. Lang, X. Li et al., “Evaluation of the enhancing ability of three adjuvants for DNA vaccination using the porcine circovirus type 2 ORF2 (capsid) gene in mice,” Virus Research, vol. 171, no. 1, pp. 247–251, 2013. View at Publisher · View at Google Scholar · View at Scopus
  101. N. Jimenez, J. Coll, F. J. Salguero, and C. Tafalla, “Co-injection of interleukin 8 with the glycoprotein gene from viral haemorrhagic septicemia virus (VHSV) modulates the cytokine response in rainbow trout (Oncorhynchus mykiss),” Vaccine, vol. 24, no. 27-28, pp. 5615–5626, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. D. C. Smith, R. A. Spooner, P. D. Watson et al., “Internalized pseudomonas exotoxin A can exploit multiple pathways to reach the endoplasmic reticulum,” Traffic, vol. 7, no. 4, pp. 379–393, 2006. View at Publisher · View at Google Scholar · View at Scopus
  103. H. M. Munang'andu, B. N. Fredriksen, S. Mutoloki et al., “Comparison of vaccine efficacy for different antigen delivery systems for infectious pancreatic necrosis virus vaccines in Atlantic salmon (Salmo salar L.) in a cohabitation challenge model,” Vaccine, vol. 30, no. 27, pp. 4007–4016, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. Z. Li-Li, L. Min, G. Jun-Wei, Q. Xin-Yuan, L. Yi-Jing, and L. Di-Qiu, “Expression of infectious pancreatic necrosis virus (IPNV) VP2-VP3 fusion protein in Lactobacillus casei and immunogenicity in rainbow trouts,” Vaccine, vol. 30, no. 10, pp. 1823–1829, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. T. Akagi, M. Baba, and M. Akashi, “Biodegradable nanoparticles as vaccine adjuvants and delivery systems: regulation of immune responses by nanoparticle-based vaccine,” in Polymers in Nanomedicine, vol. 247 of Advances in Polymer Science, pp. 31–64, Springer, Berlin, Germany, 2012. View at Publisher · View at Google Scholar
  106. M. L. Hans, C. Maxwell, R. S. Ehrlichman et al., “Evaluation of in vitro release and in vivo efficacy of mPEG-PLA-haloperidol conjugate micelle-like structures,” Journal of Biomedical Materials Research B: Applied Biomaterials, vol. 83, no. 2, pp. 422–430, 2007. View at Publisher · View at Google Scholar · View at Scopus
  107. E. Schlosser, M. Mueller, S. Fischer et al., “TLR ligands and antigen need to be coencapsulated into the same biodegradable microsphere for the generation of potent cytotoxic T lymphocyte responses,” Vaccine, vol. 26, no. 13, pp. 1626–1637, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. J. Y. Tian, X. Q. Sun, X. G. Chen, J. Yuc, L. Y. Qu, and L. C. Wang, “The formulation and immunisation of oral poly(DL-lactide-co-glycolide) microcapsules containing a plasmid vaccine against lymphocystis disease virus in Japanese flounder (Paralichthys olivaceus),” International Immunopharmacology, vol. 8, no. 6, pp. 900–908, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. J. Y. Tian, X. Q. Sun, and X. G. Chen, “Formation and oral administration of alginate microspheres loaded with pDNA coding for lymphocystis disease virus (LCDV) to Japanese flounder,” Fish and Shellfish Immunology, vol. 24, no. 5, pp. 592–599, 2008. View at Publisher · View at Google Scholar · View at Scopus
  110. J. Tian, J. Yu, and X. Q. Sun, “Chitosan microspheres as candidate plasmid vaccine carrier for oral immunisation of Japanese flounder (Paralichthys olivaceus),” Veterinary Immunology and Immunopathology, vol. 126, no. 3-4, pp. 220–229, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. F.-R. Zheng, X.-Q. Sun, H.-Z. Liu, and J.-X. Zhang, “Study on the distribution and expression of a DNA vaccine against lymphocystis disease virus in Japanese flounder (Paralichthys olivaceus),” Aquaculture, vol. 261, no. 4, pp. 1128–1134, 2006. View at Publisher · View at Google Scholar · View at Scopus
  112. S. Rajeshkumar, C. Venkatesan, M. Sarathi et al., “Oral delivery of DNA construct using chitosan nanoparticles to protect the shrimp from white spot syndrome virus (WSSV),” Fish and Shellfish Immunology, vol. 26, no. 3, pp. 429–437, 2009. View at Publisher · View at Google Scholar · View at Scopus
  113. G. Sahay, D. Y. Alakhova, and A. V. Kabanov, “Endocytosis of nanomedicines,” Journal of Controlled Release, vol. 145, no. 3, pp. 182–195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  114. S. M. Standley, Y. J. Kwon, N. Murthy et al., “Acid-degradable particles for protein-based vaccines: Enhanced survival rate for tumor-challenged mice using ovalbumin model,” Bioconjugate Chemistry, vol. 15, no. 6, pp. 1281–1288, 2004. View at Publisher · View at Google Scholar · View at Scopus
  115. R. A. Jones, C. Y. Cheung, F. E. Black et al., “Poly(2-alkylacrylic acid) polymers deliver molecules to the cytosol by pH-sensitive disruption of endosomal vesicles,” Biochemical Journal, vol. 372, no. 1, pp. 65–75, 2003. View at Publisher · View at Google Scholar · View at Scopus
  116. N. Murthy, J. R. Robichaud, D. A. Tirrell, P. S. Stayton, and A. S. Hoffman, “The design and synthesis of polymers for eukaryotic membrane disruption,” Journal of Controlled Release, vol. 61, no. 1-2, pp. 137–143, 1999. View at Publisher · View at Google Scholar · View at Scopus
  117. T. Yoshikawa, N. Okada, A. Oda et al., “Development of amphiphilic γ-PGA-nanoparticle based tumor vaccine: potential of the nanoparticulate cytosolic protein delivery carrier,” Biochemical and Biophysical Research Communications, vol. 366, no. 2, pp. 408–413, 2008. View at Publisher · View at Google Scholar · View at Scopus
  118. C. Kusonwiriyawong, P. van de Wetering, J. A. Hubbell, H. P. Merkle, and E. Walter, “Evaluation of pH-dependent membrane-disruptive properties of poly(acrylic acid) derived polymers,” European Journal of Pharmaceutics and Biopharmaceutics, vol. 56, no. 2, pp. 237–246, 2003. View at Publisher · View at Google Scholar · View at Scopus
  119. S. Foster, C. L. Duvall, E. F. Crownover, A. S. Hoffman, and P. S. Stayton, “Intracellular delivery of a protein antigen with an endosomal-releasing polymer enhances CD8 T-cell production and prophylactic vaccine efficacy,” Bioconjugate Chemistry, vol. 21, no. 12, pp. 2205–2212, 2010. View at Publisher · View at Google Scholar · View at Scopus
  120. C. B. He, Y. P. Hu, L. C. Yin, C. Tang, and C. H. Yin, “Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles,” Biomaterials, vol. 31, no. 13, pp. 3657–3666, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. L. Thiele, B. Rothen-Rutishauser, S. Jilek, H. Wunderli-Allenspach, H. P. Merkle, and E. Walter, “Evaluation of particle uptake in human blood monocyte-derived cells in vitro. Does phagocytosis activity of dendritic cells measure up with macrophages?” Journal of Controlled Release, vol. 76, no. 1-2, pp. 59–71, 2001. View at Publisher · View at Google Scholar · View at Scopus
  122. S. Burgdorf and C. Kurts, “Endocytosis mechanisms and the cell biology of antigen presentation,” Current Opinion in Immunology, vol. 20, no. 1, pp. 89–95, 2008. View at Publisher · View at Google Scholar · View at Scopus
  123. S. A. Agnihotri, N. N. Mallikarjuna, and T. M. Aminabhavi, “Recent advances on chitosan-based micro- and nanoparticles in drug delivery,” Journal of Controlled Release, vol. 100, no. 1, pp. 5–28, 2004. View at Publisher · View at Google Scholar · View at Scopus
  124. I. Gutierro, R. M. Hernández, M. Igartua, A. R. Gascón, and J. L. Pedraz, “Size dependent immune response after subcutaneous, oral and intranasal administration of BSA loaded nanospheres,” Vaccine, vol. 21, no. 1-2, pp. 67–77, 2002. View at Publisher · View at Google Scholar · View at Scopus
  125. T. Fehr, D. Skrastina, P. Pumpens, and R. M. Zinkernagel, “T cell-independent type I antibody response against B cell epitopes expressed repetitively on recombinant virus particles,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 16, pp. 9477–9481, 1998. View at Publisher · View at Google Scholar · View at Scopus
  126. A. Ruyra, M. Cano-Sarabia, S. A. MacKenzie, D. Maspoch, and N. Roher, “A novel liposome based nanocarrier loaded with an LPS-dsRNA cocktail for fish innate immune system stimulation,” PLoS ONE, vol. 8, no. 10, Article ID e76338, 2013. View at Publisher · View at Google Scholar · View at Scopus
  127. B. N. Fredriksen and J. Grip, “PLGA/PLA micro- and nanoparticle formulations serve as antigen depots and induce elevated humoral responses after immunization of Atlantic salmon (Salmo salar L.),” Vaccine, vol. 30, no. 3, pp. 656–667, 2012. View at Publisher · View at Google Scholar · View at Scopus
  128. S. Broos, K. Lundberg, T. Akagi et al., “Immunomodulatory nanoparticles as adjuvants and allergen-delivery system to human dendritic cells: implications for specific immunotherapy,” Vaccine, vol. 28, no. 31, pp. 5075–5085, 2010. View at Publisher · View at Google Scholar · View at Scopus
  129. M. Diwan, P. Elamanchili, H. Lane, A. Gainer, and J. Samuel, “Biodegradable nanoparticle mediated antigen delivery to human cord blood derived dendritic cells for induction of primary T cell responses,” Journal of Drug Targeting, vol. 11, no. 8–10, pp. 495–507, 2003. View at Publisher · View at Google Scholar · View at Scopus
  130. Y. K. Katare, T. Muthukumaran, and A. K. Panda, “Influence of particle size, antigen load, dose and additional adjuvant on the immune response from antigen loaded PLA microparticles,” International Journal of Pharmaceutics, vol. 301, no. 1-2, pp. 149–160, 2005. View at Publisher · View at Google Scholar · View at Scopus
  131. J. Samuel, P. Elamanchili, C. Chong et al., “Biodegradable nanoparticles for targeted delivery of therapeutic vaccines to dendritic cells,” The FASEB Journal, vol. 17, no. 7, p. C332, 2003. View at Google Scholar
  132. Ø. Haugland, J. Torgersen, M. Syed, and Ø. Evensen, “Expression profiles of inflammatory and immune-related genes in Atlantic salmon (Salmo salar L.) at early time post vaccination,” Vaccine, vol. 23, no. 48-49, pp. 5488–5499, 2005. View at Publisher · View at Google Scholar · View at Scopus
  133. H. M. Munang'andu, S. Mutoloki, and Ø. Evensen, “Acquired immunity and vaccination against infectious pancreatic necrosis virus of salmon,” Developmental & Comparative Immunology, vol. 43, no. 2, pp. 184–196, 2014. View at Publisher · View at Google Scholar · View at Scopus
  134. H. M. Munang'andu, S. Mutoloki, and O. Evensen, “Non-replicating vaccines,” in Fish Vaccination, chapter 3, p. 22, Wiley, 2014. View at Publisher · View at Google Scholar
  135. I. Salinas, Y. A. Zhang, and J. O. Sunyer, “Mucosal immunoglobulins and B cells of teleost fish,” Developmental and Comparative Immunology, vol. 35, no. 12, pp. 1346–1365, 2011. View at Publisher · View at Google Scholar · View at Scopus
  136. A. Estepa and J. M. Coll, “Enhancement of fish mortality by rhabdovirus infection after immunization with a viral nucleoprotein peptide,” Viral Immunology, vol. 6, no. 4, pp. 237–243, 1993. View at Publisher · View at Google Scholar · View at Scopus
  137. B. Noonan, P. J. Enzmann, and T. J. Trust, “Recombinant infectious hematopoietic necrosis virus and viral hemorrhagic septicemia virus glycoprotein epitopes expressed in Aeromonas salmonicida induce protective immunity in rainbow trout (Oncorhynchus mykiss),” Applied and Environmental Microbiology, vol. 61, no. 10, pp. 3586–3591, 1995. View at Google Scholar · View at Scopus
  138. L. A. Oberg, J. Wirkkula, D. Mourich, and J. C. Leong, “Bacterially expressed nucleoprotein of infectious hematopoietic necrosis virus augments protective immunity induced by the glycoprotein vaccine in fish,” Journal of Virology, vol. 65, no. 8, pp. 4486–4489, 1991. View at Google Scholar · View at Scopus
  139. F. C. T. Allnutt, R. M. Bowers, C. G. Rowe, V. N. Vakharia, S. E. LaPatra, and A. K. Dhar, “Antigenicity of infectious pancreatic necrosis virus VP2 subviral particles expressed in yeast,” Vaccine, vol. 25, no. 26, pp. 4880–4888, 2007. View at Publisher · View at Google Scholar · View at Scopus
  140. A. B. Mikalsen, J. Torgersen, P. Aleström, A.-L. Hellemann, E.-O. Koppang, and E. Rimstad, “Protection of Atlantic salmon, Salmo salar L, against infectious pancreatic necrosis after DNA vaccination,” Diseases of Aquatic Organisms, vol. 60, no. 1, pp. 11–20, 2004. View at Publisher · View at Google Scholar · View at Scopus
  141. R. B. Shivappa, P. E. McAllister, G. H. Edwards, N. Santi, Ø. Evensen, and V. N. Vakharia, “Development of a subunit vaccine for infectious pancreatic necrosis virus using a baculovirus insect/larvae system,” Developments in Biologicals, vol. 121, pp. 165–174, 2005. View at Google Scholar · View at Scopus
  142. F. Lecocq-Xhonneux, M. Thiry, I. Dheur et al., “A recombinant viral haemorrhagic septicaemia virus glycoprotein expressed in insect cells induces protective immunity in rainbow trout,” Journal of General Virology, vol. 75, no. 7, pp. 1579–1587, 1994. View at Publisher · View at Google Scholar · View at Scopus
  143. A. C. Moore and C. L. Hutchings, “Combination vaccines: synergistic simultaneous induction of antibody and T-cell immunity,” Expert Review of Vaccines, vol. 6, no. 1, pp. 111–121, 2007. View at Publisher · View at Google Scholar · View at Scopus
  144. A.-C. Øvergård, S. Patel, O. J. Nøstbakken, and A. H. Nerland, “Atlantic halibut (Hippoglossus hippoglossus L.) T-cell and cytokine response after vaccination and challenge with nodavirus,” Vaccine, vol. 31, no. 19, pp. 2395–2402, 2013. View at Publisher · View at Google Scholar · View at Scopus
  145. A.-C. Øvergård, A. H. Nerland, I. U. Fiksdal, and S. Patel, “Atlantic halibut experimentally infected with nodavirus shows increased levels of T-cell marker and IFNγ transcripts,” Developmental & Comparative Immunology, vol. 37, no. 1, pp. 139–150, 2012. View at Publisher · View at Google Scholar · View at Scopus
  146. W. Liu, C.-H. Hsu, C.-Y. Chang, H.-H. Chen, and C.-S. Lin, “Immune response against grouper nervous necrosis virus by vaccination of virus-like particles,” Vaccine, vol. 24, no. 37–39, pp. 6282–6287, 2006. View at Publisher · View at Google Scholar · View at Scopus
  147. L. Tang, C.-S. Lin, N. K. Krishna, M. Yeager, A. Schneemann, and J. E. Johnson, “Virus-like particles of a fish nodavirus display a capsid subunit domain organization different from that of insect nodaviruses,” Journal of Virology, vol. 76, no. 12, pp. 6370–6375, 2002. View at Publisher · View at Google Scholar · View at Scopus
  148. C.-S. Lin, M.-W. Lu, L. Tang et al., “Characterization of virus-like particles assembled in a recombinant baculovirus system expressing the capsid protein of a fish nodavirus,” Virology, vol. 290, no. 1, pp. 50–58, 2001. View at Publisher · View at Google Scholar · View at Scopus
  149. Q. Fang, E. K. Seng, Q. Q. Ding, and L. L. Zhang, “Characterization of infectious particles of grass carp reovirus by treatment with proteases,” Archives of Virology, vol. 153, no. 4, pp. 675–682, 2008. View at Publisher · View at Google Scholar · View at Scopus
  150. A. K. Dhar, R. M. Bowers, C. G. Rowe, and F. C. T. Allnutt, “Expression of a foreign epitope on infectious pancreatic necrosis virus VP2 capsid protein subviral particle (SVP) and immunogenicity in rainbow trout,” Antiviral Research, vol. 85, no. 3, pp. 525–531, 2010. View at Publisher · View at Google Scholar · View at Scopus
  151. A. Rivas-Aravena, M. C.-S. Martin, J. Galaz et al., “Evaluation of the immune response against immature viral particles of infectious pancreatic necrosis virus (IPNV): a new model to develop an attenuated vaccine,” Vaccine, vol. 30, no. 34, pp. 5110–5117, 2012. View at Publisher · View at Google Scholar · View at Scopus
  152. M. W. Lu and C.-S. Lin, “Involvement of the terminus of grouper betanodavirus capsid protein in virus-like particle assembly,” Archives of Virology, vol. 148, no. 2, pp. 345–355, 2003. View at Publisher · View at Google Scholar · View at Scopus
  153. Y.-X. Lai, B.-L. Jin, Y. Xu et al., “Immune responses of orange-spotted grouper, Epinephelus coioides, against virus-like particles of betanodavirus produced in Escherichia coli,” Veterinary Immunology and Immunopathology, vol. 157, no. 1-2, pp. 87–96, 2014. View at Publisher · View at Google Scholar · View at Scopus
  154. R. A. Goldsby, T. Kindt, J. Kiby, and B. Osborne, Immunology, W.H. Freeman, 5th edition, 2003.
  155. M. O. V. Osinubi, X. Wu, R. Franka et al., “Enhancing comparative rabies DNA vaccine effectiveness through glycoprotein gene modifications,” Vaccine, vol. 27, no. 51, pp. 7214–7218, 2009. View at Publisher · View at Google Scholar · View at Scopus
  156. N. B. Ray, L. C. Ewalt, and D. L. Lodmell, “Nanogram quantities of plasmid DNA encoding the rabies virus glycoprotein protect mice against lethal rabies virus infection,” Vaccine, vol. 15, no. 8, pp. 892–895, 1997. View at Publisher · View at Google Scholar · View at Scopus
  157. C. Xu, S. Mutoloki, and Ø. Evensen, “Superior protection conferred by inactivated whole virus vaccine over subunit and DNA vaccines against salmonid alphavirus infection in Atlantic salmon (Salmo salar L.),” Vaccine, vol. 30, no. 26, pp. 3918–3928, 2012. View at Publisher · View at Google Scholar · View at Scopus
  158. M. Howarth and T. Elliott, “The processing of antigens delivered as DNA vaccines,” Immunological Reviews, vol. 199, pp. 27–39, 2004. View at Publisher · View at Google Scholar · View at Scopus
  159. T. Shao, L.-Y. Zhu, L. Nie et al., “Characterization of surface phenotypic molecules of teleost dendritic cells,” Developmental & Comparative Immunology, vol. 49, no. 1, pp. 38–43, Mar 2015. View at Google Scholar
  160. M.-F. Li, Y.-X. Li, and L. Sun, “CD83 is required for the induction of protective immunity by a DNA vaccine in a teleost model,” Developmental & Comparative Immunology, vol. 51, no. 1, pp. 141–147, 2015. View at Publisher · View at Google Scholar
  161. J. Wiik-Nielsen, M. Løvoll, C. Fritsvold et al., “Characterization of myocardial lesions associated with cardiomyopathy syndrome in atlantic salmon, Salmo salar L., using laser capture microdissection,” Journal of Fish Diseases, vol. 35, no. 12, pp. 907–916, 2012. View at Publisher · View at Google Scholar · View at Scopus
  162. 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,” The Journal of Immunology, vol. 183, no. 11, pp. 7398–7410, 2009. View at Publisher · View at Google Scholar · View at Scopus
  163. R. D. Pinto, E. Randelli, F. Buonocore, P. J. B. Pereira, and N. M. S. dos Santos, “Molecular cloning and characterization of sea bass (Dicentrarchus labrax, L.) MHC class I heavy chain and β2-microglobulin,” Developmental and Comparative Immunology, vol. 39, no. 3, pp. 234–254, 2013. View at Publisher · View at Google Scholar · View at Scopus
  164. Z. Y. Xu, P. Nie, M. X. Chang, and B. J. Sun, “Cloning, characterization and expression analysis of SIMP (source of immunodominant MHC-associated peptides) in grass carp Ctenopharyngodon idella,” Fish & Shellfish Immunology, vol. 24, no. 6, pp. 701–714, 2008. View at Publisher · View at Google Scholar · View at Scopus
  165. M. A. Noakes, T. Reimer, and R. B. Phillips, “Genotypic characterization of an MHC class II locus in lake trout (Salvelinus namaycush) from Lake Superior by single-stranded conformational polymorphism analysis and reference strand-mediated conformational analysis,” Marine Biotechnology, vol. 5, no. 3, pp. 270–278, 2003. View at Publisher · View at Google Scholar · View at Scopus
  166. Y. Liu, L. Moore, E. O. Koppang, and I. Hordvik, “Characterization of the CD3ζ, CD3γδ and CD3ε subunits of the T cell receptor complex in Atlantic salmon,” Developmental & Comparative Immunology, vol. 32, no. 1, pp. 26–35, 2008. View at Publisher · View at Google Scholar
  167. K. J. Laing and J. D. Hansen, “Fish T cells: recent advances through genomics,” Developmental and Comparative Immunology, vol. 35, no. 12, pp. 1282–1295, 2011. View at Publisher · View at Google Scholar · View at Scopus
  168. P. Ronza, R. Bermúdez, A. P. Losada, A. Robles, and M. I. Quiroga, “Mucosal CD3ε+ cell proliferation and gut epithelial apoptosis: implications in rainbow trout gastroenteritis (RTGE),” Journal of Fish Diseases, vol. 34, no. 6, pp. 433–443, 2011. View at Publisher · View at Google Scholar
  169. K. Maisey, D. Toro-Ascuy, R. Montero, F. E. Reyes-López, and M. Imarai, “Identification of CD3ε, CD4, CD8β splice variants of Atlantic salmon,” Fish & Shellfish Immunology, vol. 31, no. 6, pp. 815–822, 2011. View at Publisher · View at Google Scholar · View at Scopus
  170. S. Partula, A. De Guerra, J. S. Fellah, and J. Charlemagne, “Structure and diversity of the TCR α-chain in a teleost fish,” The Journal of Immunology, vol. 157, no. 1, pp. 207–212, 1996. View at Google Scholar · View at Scopus
  171. B. H. Nam, I. Hirono, and T. Aoki, “The four TCR genes of teleost fish: The cDNA and genomic DNA analysis of Japanese flounder (Paralichthys olivaceus) TCR alpha-, beta-, gamma-, and delta-chains,” Journal of Immunology, vol. 170, no. 6, pp. 3081–3090, 2003. View at Publisher · View at Google Scholar · View at Scopus
  172. C.-I. Park, J. Y. Hwang, I. Hirono, and T. Aoki, “Characterization and expression of a CD40 homolog gene in Japanese flounder Paralichthys olivaceus,” Immunogenetics, vol. 57, no. 9, pp. 682–689, 2005. View at Publisher · View at Google Scholar · View at Scopus
  173. F. Takizawa, J. M. Dijkstra, P. Kotterba et al., “The expression of CD8α discriminates distinct T cell subsets in teleost fish,” Developmental and Comparative Immunology, vol. 35, no. 7, pp. 752–763, 2011. View at Publisher · View at Google Scholar · View at Scopus
  174. I. Hordvik, “Immunoglobulin isotypes in Atlantic salmon, Salmo Salar,” Biomolecules, vol. 5, no. 1, pp. 166–177, 2015. View at Publisher · View at Google Scholar
  175. E. Bromage, P. Kataria, and F. Ramirez-Gomez, “The structure of rainbow trout IgM influences antibody-mediated phagocytosis of bacteria,” The Journal of Immunology, vol. 188, 2012. View at Google Scholar
  176. Y.-L. Hu, L.-X. Xiang, and J.-Z. Shao, “Identification and characterization of a novel immunoglobulin Z isotype in zebrafish: implications for a distinct B cell receptor in lower vertebrates,” Molecular Immunology, vol. 47, no. 4, pp. 738–746, 2010. View at Publisher · View at Google Scholar · View at Scopus
  177. A. Perelberg, A. Ronen, M. Hutoran, Y. Smith, and M. Kotler, “Protection of cultured Cyprinus carpio against a lethal viral disease by an attenuated virus vaccine,” Vaccine, vol. 23, no. 26, pp. 3396–3403, 2005. View at Publisher · View at Google Scholar · View at Scopus
  178. P. de Kinkelin, M. Bearzotti-Le Berre, and J. Bernard, “Viral hemorrhagic septicemia of rainbow trout: selection of a thermoresistant virus variant and comparison of polypeptide synthesis with the wild-type virus strain,” Journal of Virology, vol. 36, no. 3, pp. 652–658, 1980. View at Google Scholar · View at Scopus
  179. W. S. Kim, C. S. Kim, J. K. Cho, J. I. Myung, and M. J. Oh, “Disease control efficacy of synthetic double-stranded RNA Poly(I:C) administration for viral nervous necrosis (VNN) in sevenband grouper (Epinephelus septemfasciatus),” Aquaculture, vol. 364-365, pp. 259–262, 2012. View at Publisher · View at Google Scholar · View at Scopus
  180. P.-J. Enzmann, D. Fichtner, H. Schütze, and G. Walliser, “Development of vaccines against VHS and IHN: oral application, molecular marker and discrimination of vaccinated fish from infected populations,” Journal of Applied Ichthyology, vol. 14, no. 3-4, pp. 179–183, 1998. View at Publisher · View at Google Scholar
  181. B. Novoa, A. Romero, V. Mulero, I. Rodríguez, I. Fernández, and A. Figueras, “Zebrafish (Danio rerio) as a model for the study of vaccination against viral haemorrhagic septicemia virus (VHSV),” Vaccine, vol. 24, no. 31-32, pp. 5806–5816, 2006. View at Publisher · View at Google Scholar · View at Scopus
  182. C. H. Kim, J. R. Winton, and J. C. Leong, “Neutralization-resistant variants of infectious hematopoietic necrosis virus have altered virulence and tissue tropism,” Journal of Virology, vol. 68, no. 12, pp. 8447–8453, 1994. View at Google Scholar · View at Scopus
  183. S. S. Ristow, S. E. LaPatra, R. Dixon et al., “Responses of cloned rainbow trout Oncorhynchus mykiss to an attenuated strain of infectious hematopoietic necrosis virus,” Diseases of Aquatic Organisms, vol. 42, no. 3, pp. 163–172, 2000. View at Publisher · View at Google Scholar · View at Scopus
  184. S.-Y. Oh and T. Nishizawa, “Optimizing the quantitative detection of red seabream iridovirus (RSIV) genome from splenic tissues of rock bream Oplegnathus fasciatus using a qPCR Assay,” Fish Pathology, vol. 48, no. 1, pp. 21–24, 2013. View at Publisher · View at Google Scholar
  185. C. M. A. Caipang, T. Takano, I. Hirono, and T. Aoki, “Genetic vaccines protect red seabream, Pagrus major, upon challenge with red seabream iridovirus (RSIV),” Fish & Shellfish Immunology, vol. 21, no. 2, pp. 130–138, 2006. View at Publisher · View at Google Scholar · View at Scopus
  186. K. E. Nusbaum, B. F. Smith, P. DeInnocentes, and R. C. Bird, “Protective immunity induced by DNA vaccination of channel catfish with early and late transcripts of the channel catfish herpesvirus (IHV-1),” Veterinary Immunology and Immunopathology, vol. 84, no. 3-4, pp. 151–168, 2002. View at Publisher · View at Google Scholar · View at Scopus
  187. J. C. Leong, E. Anderson, L. M. Bootland et al., “Fish vaccine antigens produced or delivered by recombinant DNA technologies,” Fish Vaccinology, vol. 90, pp. 267–277, 1997. View at Google Scholar
  188. J. R. Winton, “Immunization with viral antigens: infectious haematopoietic necrosis,” Fish Vaccinology, vol. 90, pp. 211–220, 1997. View at Google Scholar
  189. E. J. Emmenegger and G. Kurath, “DNA vaccine protects ornamental koi (Cyprinus carpio koi) against North American spring viremia of carp virus,” Vaccine, vol. 26, no. 50, pp. 6415–6421, 2008. View at Publisher · View at Google Scholar · View at Scopus
  190. T. Kanellos, I. D. Sylvester, F. D'Mello et al., “DNA vaccination can protect Cyprinus Carpio against spring viraemia of carp virus,” Vaccine, vol. 24, no. 23, pp. 4927–4933, 2006. View at Publisher · View at Google Scholar · View at Scopus
  191. T. Takano, A. Iwahori, I. Hirono, and T. Aoki, “Development of a DNA vaccine against hirame rhabdovirus and analysis of the expression of immune-related genes after vaccination,” Fish & Shellfish Immunology, vol. 17, no. 4, pp. 367–374, 2004. View at Publisher · View at Google Scholar · View at Scopus
  192. A. B. Mikalsen, H. Sindre, J. Torgersen, and E. Rimstad, “Protective effects of a DNA vaccine expressing the infectious salmon anemia virus hemagglutinin-esterase in Atlantic salmon,” Vaccine, vol. 23, no. 41, pp. 4895–4905, 2005. View at Publisher · View at Google Scholar · View at Scopus
  193. I. Sommerset, E. Lorenzen, N. Lorenzen, H. Bleie, and A. H. Nerland, “A DNA vaccine directed against a rainbow trout rhabdovirus induces early protection against a nodavirus challenge in turbot,” Vaccine, vol. 21, no. 32, pp. 4661–4667, 2003. View at Publisher · View at Google Scholar · View at Scopus
  194. J. Y. Tian and J. Yu, “Corrigendum to ‘poly (lactic-co-glycolic acid) nanoparticles as candidate DNA vaccine carrier for oral immunization of Japanese flounder (Paralichthys olivaceus) against lymphocystis disease virus’ Fish Shellfish Immun. 30 (2011) 109–117,” Fish & Shellfish Immunology, vol. 31, no. 2, p. 364, 2011. View at Publisher · View at Google Scholar
  195. M. Adomako, S. St-Hilaire, Y. Zheng et al., “Oral DNA vaccination of rainbow trout, Oncorhynchus mykiss (Walbaum), against infectious haematopoietic necrosis virus using PLGA [Poly(D,L-Lactic-Co-Glycolic Acid)] nanoparticles,” Journal of Fish Diseases, vol. 35, no. 3, pp. 203–214, 2012. View at Publisher · View at Google Scholar · View at Scopus
  196. S. Vimal, S. Abdul Majeed, G. Taju et al., “Chitosan tripolyphosphate (CS/TPP) nanoparticles: preparation, characterization and application for gene delivery in shrimp,” Acta Tropica, vol. 128, no. 3, pp. 486–493, 2013. View at Publisher · View at Google Scholar · View at Scopus
  197. P. de Kinkelin, M. Béarzotti, J. Castric, P. Nougayrède, F. Lecocq-Xhonneux, and M. Thiry, “Eighteen years of vaccination against viral haemorrhagic septicaemia in France,” Veterinary Research, vol. 26, no. 5-6, pp. 379–387, 1995. View at Google Scholar · View at Scopus
  198. E. Anderson, S. Clouthier, W. Shewmaker, A. Weighall, and S. LaPatra, “Inactivated infectious haematopoietic necrosis virus (IHNV) vaccines,” Journal of Fish Diseases, vol. 31, no. 10, pp. 729–745, 2008. View at Publisher · View at Google Scholar · View at Scopus
  199. J. Tesarcík, B. Macura, L. Dedek, L. Valicek, and B. Smíd, “Isolation and electron microscopy of a rhabdovirus from the acute form of infectious dropsy of carp (spring viraemia of carp),” Zentralblatt für Veterinärmedizin Reihe B, vol. 24, no. 4, pp. 340–343, 1977. View at Google Scholar
  200. M. V. López-Dóriga, D. A. Smail, R. J. Smith et al., “Isolation of salmon pancreas disease virus (SPDV) in cell culture and its ability to protect against infection by the ‘wild-type’ agent,” Fish & Shellfish Immunology, vol. 11, no. 6, pp. 505–522, 2001. View at Publisher · View at Google Scholar · View at Scopus
  201. C. M. A. Caipang, I. Hirono, and T. Aoki, “Immunogenicity, retention and protective effects of the protein derivatives of formalin-inactivated red seabream iridovirus (RSIV) vaccine in red seabream, Pagrus major,” Fish & Shellfish Immunology, vol. 20, no. 4, pp. 597–609, 2006. View at Publisher · View at Google Scholar · View at Scopus
  202. Z. L. Ou-Yang, P. R. Wang, X. H. Huang et al., “Immunogenicity and protective effects of inactivated Singapore grouper iridovirus (SGIV) vaccines in orange-spotted grouper, Epinephelus coioides,” Developmental and Comparative Immunology, vol. 38, no. 2, pp. 254–261, 2012. View at Publisher · View at Google Scholar · View at Scopus
  203. P. Dixon, “Immunization with viral antigens: viral diseases of carp and catfish,” Fish Vaccinology, vol. 90, pp. 221–232, 1997. View at Google Scholar
  204. S. Yasumoto, Y. Kuzuya, M. Yasuda, T. Yoshimura, and T. Miyazaki, “Oral immunization of common carp with a liposome vaccine fusing koi herpesvirus antigen,” Fish Pathology, vol. 41, no. 4, pp. 141–145, 2006. View at Publisher · View at Google Scholar · View at Scopus
  205. R. Pakingking Jr., N. B. Bautista, E. G. de Jesus-Ayson, and O. Reyes, “Protective immunity against viral nervous necrosis (VNN) in brown-marbled grouper (Epinephelus fuscogutattus) following vaccination with inactivated betanodavirus,” Fish & Shellfish Immunology, vol. 28, no. 4, pp. 525–533, 2010. View at Publisher · View at Google Scholar · View at Scopus
  206. R. Pakingking Jr., R. Seron, L. Dela Peña, K. Mori, H. Yamashita, and T. Nakai, “Immune responses of Asian sea bass, Lates calcarifer Bloch, against an inactivated betanodavirus vaccine,” Journal of Fish Diseases, vol. 32, no. 5, pp. 457–463, 2009. View at Publisher · View at Google Scholar · View at Scopus
  207. A. Lauscher, B. Krossøy, P. Frost et al., “Immune responses in Atlantic salmon (Salmo salar) following protective vaccination against Infectious salmon anemia (ISA) and subsequent ISA virus infection,” Vaccine, vol. 29, no. 37, pp. 6392–6401, 2011. View at Publisher · View at Google Scholar · View at Scopus
  208. L. Min, Z. Li-Li, G. Jun-Wei, Q. Xin-Yuan, L. Yi-Jing, and L. Di-Qiu, “Immunogenicity of Lactobacillus-expressing VP2 and VP3 of the infectious pancreatic necrosis virus (IPNV) in rainbow trout,” Fish and Shellfish Immunology, vol. 32, no. 1, pp. 196–203, 2012. View at Publisher · View at Google Scholar · View at Scopus
  209. B. M. McKenna, R. M. Fitzpatrick, K. V. Phenix, D. Todd, L. M. Vaughan, and G. J. Atkins, “Formation of infectious pancreatic necrosis virus-like particles following expression of segment a by recombinant semliki forest virus,” Marine Biotechnology, vol. 3, no. 2, pp. 103–110, 2001. View at Publisher · View at Google Scholar · View at Scopus
  210. P. de Kinkelin, “Vaccination in fish,” Veterinary Research, vol. 26, no. 3, pp. 205–206, 1995. View at Google Scholar · View at Scopus
  211. A. Estepa, M. Thiry, and J. M. Coll, “Recombinant protein fragments from haemorrhagic septicaemia rhabdovirus stimulate trout leukocyte anamnestic responses in vitro,” Journal of General Virology, vol. 75, no. 6, pp. 1329–1338, 1994. View at Publisher · View at Google Scholar · View at Scopus
  212. S. H. Choi, M. S. Kim, and K. H. Kim, “Immunization of olive flounder (Paralichthys olivaceus) with an auxotrophic Edwardsiella tarda mutant harboring the VHSV DNA vaccine,” Fish & Shellfish Immunology, vol. 33, no. 3, pp. 569–574, 2012. View at Publisher · View at Google Scholar · View at Scopus
  213. B. Simon, J. Nomellini, P. Chiou et al., “Recombinant vaccines against infectious hematopoietic necrosis virus: production by the Caulobacter crescentus S-layer protein secretion system and evaluation in laboratory trials,” Diseases of Aquatic Organisms, vol. 44, no. 1, pp. 17–27, 2001. View at Publisher · View at Google Scholar · View at Scopus
  214. K. D. Cain, S. E. LaPatra, B. Shewmaker, J. Jones, K. M. Byrne, and S. S. Ristow, “Immunogenicity of a recombinant infectious hematopoietic necrosis virus glycoprotein produced in insect cells,” Diseases of Aquatic Organisms, vol. 36, no. 1, pp. 67–72, 1999. View at Publisher · View at Google Scholar · View at Scopus
  215. Y. Y. Tian, X. Ye, L. L. Zhang, G. C. Deng, and Y. Q. Bai, “Development of a novel candidate subunit vaccine against Grass carp reovirus Guangdong strain (GCRV-GD108),” Fish & Shellfish Immunology, vol. 35, no. 2, pp. 351–356, 2013. View at Publisher · View at Google Scholar · View at Scopus
  216. L. Shao, X. Sun, and Q. Fang, “Antibodies against outer-capsid proteins of grass carp reovirus expressed in E. coli are capable of neutralizing viral infectivity,” Virology Journal, vol. 8, article 347, 2011. View at Publisher · View at Google Scholar · View at Scopus
  217. I. Sommerset, R. Skern, E. Biering et al., “Protection against Atlantic halibut nodavirus in turbot is induced by recombinant capsid protein vaccination but not following DNA vaccination,” Fish and Shellfish Immunology, vol. 18, no. 1, pp. 13–29, 2005. View at Publisher · View at Google Scholar · View at Scopus
  218. Y. R. Choi, H. J. Kim, J. Y. Lee, H. A. Kang, and H.-J. Kim, “Chromatographically-purified capsid proteins of red-spotted grouper nervous necrosis virus expressed in Saccharomyces cerevisiae form virus-like particles,” Protein Expression and Purification, vol. 89, no. 2, pp. 162–168, 2013. View at Publisher · View at Google Scholar · View at Scopus
  219. S. Martinez-Alonso, V. N. Vakharia, S. R. Saint-Jean, S. Pérez-Prieto, and C. Tafalla, “Immune responses elicited in rainbow trout through the administration of infectious pancreatic necrosis virus-like particles,” Developmental and Comparative Immunology, vol. 36, no. 2, pp. 378–384, 2012. View at Publisher · View at Google Scholar · View at Scopus
  220. Q. Fang, S. Shah, Y. Liang, and Z. H. Zhou, “3D reconstruction and capsid protein characterization of grass carp reovirus,” Science in China, Series C: Life Sciences, vol. 48, no. 6, pp. 593–600, 2005. View at Publisher · View at Google Scholar · View at Scopus
  221. R. Thiéry, J. Cozien, J. Cabon, F. Lamour, M. Baud, and A. Schneemann, “Induction of a protective immune response against viral nervous necrosis in the European sea bass Dicentrarchus labrax by using betanodavirus virus-like particles,” Journal of Virology, vol. 80, no. 20, pp. 10201–10207, 2006. View at Publisher · View at Google Scholar · View at Scopus