Concurrent injection of a rhabdovirus-specific DNA vaccine with a polyvalent, oil-adjuvanted vaccine delays the specific anti-viral immune response in Atlantic salmon, Salmo salar L.

Fish and Shellfish Immunology

Volumn 28, Issue 4, 2010, Pages 579-586

  Skinner, Lisa A ^a   LaPatra, S E ^b   Adams, A ^c   Thompson, K D ^c   Balfry, S K ^a   McKinley, R S ^a   Schulte, P M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b CLEAR SPRINGS FOODS INC   (United States)

^c UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

Adaptive immune response; Adjuvant vaccine; Aeromonas salmonicida; Antibody titre; DNA vaccine; Innate immune response; Listonella anguillarum; Lysozyme activity; Neutralizing antibody

Indexed keywords

AEROMONAS SALMONICIDA; INFECTIOUS HEMATOPOIETIC NECROSIS VIRUS; LISTONELLA ANGUILLARUM; RHABDOVIRIDAE; SALMO SALAR; SALMONIDAE;

EID: 77949905446     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2009.12.017     Document Type: Article

References (74)

1. FAO. The state of world aquaculture (2006), Food and Agriculture Organisation of the United Nations, Rome
2. Leong J.C., and Fryer F.L. Viral vaccines for aquaculture. Annual Review of Fish Diseases 3 (1993) 225-240
3. Thorarinsson R., and Powell D.B. Effects of disease risk, vaccine efficacy, and market price on the economics of fish vaccination. Aquaculture 256 (2006) 42-49
4. Sommerset I., Krossøy B., Biering E., and Frost P. Vaccines for fish in aquaculture. Expert Review of Vaccines 4 1 (2005) 89-101
5. Austin B., and Austin D.A. Bacterial fish pathogens: Diseases of FARMED and wild fish. 4th ed. (2007), Praxis Publishing Ltd., Chichester, UK
6. Anderson D.P. Adjuvants and immunostimulants for enhancing vaccine potency in fish. In: Gudding R., Lillehaug P.J., Midtlyng P.J., and Brown F. (Eds). Fish vaccinology; developments in biological standardization vol. 90 (1997), Karger, Basel, Switzerland 257-265
7. Evensen Ø., Brudeseth B., and Mutoloki S. The vaccine formulation and its role in inflammatory processes in fish - effects and adverse effects. In: Midtlyng P.G. (Ed). Progress in fish vaccinology; developments in biological standardization vol. 121 (2005), Karger, Basel, Switzerland 117-126
8. Schijns V.E.J.C., and Tangerås A. Vaccine adjuvant technology: from theoretical mechanisms to practical approaches. In: Midtlyng P.G. (Ed). Progress in fish vaccinology; developments in biological standardization vol. 121 (2005), Karger, Basel, Switzerland 127-134
9. Mutoloki S., Reite O.B., Brudeseth B., Tverdal A., and Evensen Ø. A comparative immunopathological study of injection site reactions in salmonids following intraperitoneal injection with oil-adjuvanted vaccines. Vaccine 24 (2006) 578-588
10. Midtlyng P.J., Reitan L.J., and Speilberg L. Experimental studies on the efficacy and side-effects of intraperitoneal vaccination of Atlantic salmon (Salmo salar L.) against furunculosis. Fish and Shellfish Immunology 6 (1996) 335-350
11. Midtlyng P.J. Vaccinated fish welfare: protection versus side-effects. In: Gudding R., Lillehaug P.J., Midtlyng P.J., and Brown F. (Eds). Progress in fish vaccinology; developments in biological standardization vol. 121 (2005), Karger, Basel, Switzerland 371-379
12. Poppe T.T., and Breck O. Pathology of Atlantic salmon Salmo salar intraperitonealy immunized with oil-adjuvanted vaccine. A case report. Diseases of Aquatic Organisms 29 (1997) 219-226
13. Berg A., Rødseth T., Tangerås A., and Hansen T.J. Time of fish vaccination influences development of adherences, growth and spinal deformities in Atlantic salmon (Salmo salar L.). Diseases of Aquatic Organisms 69 (2006) 239-248
14. Berg A., Rødseth O.M., and Hansen T. Fish size at vaccination influences the development of side-effects in Atlantic salmon (Salmo salar L.). Aquaculture 265 (2007) 9-15
15. Anderson E.D., Mourich D.V., Fahrenkrug S., LaPatra S., Shepherd J., and Leong J.A.C. Genetic immunisation of rainbow trout (Oncorhynchus mykiss) against infectious hematopoietic necrosis virus. Molecular Marine Biology and Biotechnology 5 2 (1996) 114-122
16. Anderson E.D., Mourich D.V., and Leong J.A.C. Gene expression in rainbow trout (Oncorhynchus mykiss) following intramuscular injection of DNA. Molecular Marine Biology and Biotechnology 5 2 (1996) 105-113
17. Boudinot P., Blanco M., de Kinkelin P., and Benmansour A. Combined DNA immunisation with the glycoprotein gene of viral hemorrhagic septicaemia virus and infectious hematopoietic necrosis virus induces double-specific protective immunity and nonspecific responses in rainbow trout. Virology 249 (1998) 297-306
18. Lorenzen N., Lorenzen E., Einer-Jensen K., Heppell J., Wu T., and Davis H. Protective immunity to VHS in rainbow trout (Oncorhynchus mykiss, Walbaum) following DNA vaccination. Fish and Shellfish Immunology 8 (1998) 261-270
19. Heppell J., Lorenzen N., Armstrong N.K., Wu T., Lorenzen E., Einer-Jensen K., et al. Development of DNA vaccines for fish: vector design, intramuscular injection and antigen expression using viral haemorrhagic septicaemia virus genes as model. Fish and Shellfish Immunology 8 (1998) 271-286
20. Kim C.H., Johnson M.C., Drennan J.D., Simon B.E., Thomann E., and Leong J.C. DNA vaccines encoding viral glycoproteins induce nonspecific immunity and Mx protein synthesis in fish. Journal of Virology 75 15 (2000) 7048-7054
21. Boudinot P., Bernard D., Boubekeur S., Thoulouze M.I., Bremont M., and Benmansour A. The glycoprotein of a fish rhabdovirus profiles the virus-specific T-cell repertoire in rainbow trout. Journal of General Virology 85 (2004) 3099-3108
22. Purcell M.K., Kurath G., Garver K.A., Herwig R.P., and Winton J.R. Quantitative expression profiling of immune response genes in rainbow trout following infectious haematopoietic necrosis virus (IHNV) infection or DNA vaccination. Fish and Shellfish Immunology 17 (2004) 447-462
23. Purcell M.K., Nichols K.M., Winton J.R., Kurath G., Thorgaard G.H., Wheeler P., et al. Comprehensive gene expression profiling following DNA vaccination of rainbow trout against infectious hematopoietic necrosis virus. Molecular Immunology 43 (2006) 2089-2106
24. Utke K., Kock H., Schuetze H., Bergmann S.M., Lorenzen N., Einer-Jensen K., et al. Cell-mediated immune response in the rainbow trout after DNA immunisation against the viral hemorrhagic septicaemia virus. Developmental and Comparative Immunology 32 (2008) 239-252
25. Busch R.A. Polyvalent vaccines in fish: the interactive effects of multiple antigens. In: Gudding R., Lillehaug P.J., Midtlyng P.J., and Brown F. (Eds). Fish Vaccinology; Developments in Biological Standardization vol. 90 (1997), Karger, Basel, Switzerland 245-256
26. Nikoskelainen S., Verho S., Järvinen S., Madetoja J., Wiklund T., and Lilius E.M. Multiple whole bacterial antigens in polyvalent vaccine may result in inhibition of specific responses in rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology 22 (2007) 206-217
27. Hoel K., Salonius K., and Lillehaug A. Vibrio antigens of polyvalent vaccines enhance the humoral immune response to Aeromonas salmonicida antigens in Atlantic salmon (Salmo salar L.). Fish and Shellfish Immunology 7 (1997) 71-80
28. Hoel K., Reitan L.J., and Lillehaug A. Immunological cross reactions between Aeromonas salmonicida and Vibrio salmonicida in Atlantic salmon (Salmo salar L.) and rabbit. Fish and Shellfish Immunology 8 (1998) 171-182
29. Taborda C.P., Rivera J., Zaragoza O., and Casadevall A. More is not necessarily better: prozone-like effects in passive immunisation with IgG. The Journal of Immunology 170 (2003) 3621-3630
30. Amend D.F., and Johnson K.A. Evidence for lack of antigenic competition among various combinations of Vibrio anguillarum, Yersinia ruckeri, Aeromonas salmonicida and Renibacterium salmnoinarum bacterins when administered to salmonid fish. Journal of Fish Immunology 7 (1984) 293-299
31. Rørstad G., Aasjord P.M., and Robertson B. Adjuvant effect of a yeast glucans in vaccines against furunculosis in Atlantic salmon (Salmo salar L.). Fish and Shellfish Immunology 3 (1993) 179-190
32. Corbeil S., LaPatra S.E., Anderson E.D., and Kurath G. Nanogram quantities of a DNA vaccine protect rainbow trout fry against heterologous strains of infectious hematopoietic necrosis virus. Vaccine 18 (2000) 2817-2824
33. Corbeil S., Kurath G., and LaPatra S.E. Fish DNA vaccine against infectious hematopoietic necrosis virus: efficacy of various routs of immunisation. Fish and Shellfish Immunology 10 (2000) 711-723
34. LaPatra S.E., Corbeil S., Jones G.R., Shewmaker W.D., and Kurath G. The dose-dependent effect on protection and humoral response to a DNA vaccine against infectious hematopoietic necrosis (IHN) virus in sub-yearling rainbow trout. Journal of Aquatic Animal Health 12 (2000) 181-188
35. Kurath G., Garver K.A., Corbeil S., Elliott D.G., Anderson E.D., and LaPatra S.E. Protective immunity and lack of histopathological damage two years after DNA vaccination against infectious hematopoietic necrosis virus in trout. Vaccine 24 (2006) 345-354
36. Litwack G. Photometric determination of lysozyme activity. Proceedings for the Society for Experimental Biology and Medicine 89 (1955) 401-403
37. Maule A.G., Schrock R., Slater C., Fitzpatrick M.S., and Schreck C.B. Immune and endocrine responses of adult Chinook salmon during fresh-water immigration and sexual maturation. Fish and Shellfish Immunology 6 (1996) 221-233
38. Ackerman P.A., and Iwama G.K. Physiological and cellular responses of juvenile rainbow trout to vibriosis. Journal of Aquatic Animal Health 13 (2001) 173-180
39. LaPatra S.E., Turner T., Lauda K.A., Jones G.R., and Walker S. Characterization of the humoral response of rainbow trout to infectious hematopoietic necrosis virus. Journal of Aquatic Animal Health 5 (1993) 165-171
40. Toranzo A.E., Magariños B., and Romalde J.L. A review of the main bacterial fish diseases in mariculture systems. Aquaculture (2005) 37-61
41. Adams A., Thompson K.D., Morris D., Farias C., and Chen S.C. Development and use of monoclonal antibody probes for immunohistochemistry, ELISA and IFAT to detect bacterial and parasitic fish pathogens. Fish and Shellfish Immunology 5 (1995) 537-547
42. Kim W.S., Nishizawa T., and Yoshimizu M. Non-specific adsorption of fish immunoglobulin (IgM) to blocking reagents on ELISA plates. Diseases of Aquatic Organisms 78 (2007) 55-59
43. Ellis A.E. Innate host defense mechanisms of fish against viruses and bacteria. Developmental and Comparative Immunology 25 (2001) 827-839
44. Yano T. The non-specific immune system: humoral defense. In: Iwama G., and Nakanishi T. (Eds). The fish immune system: Organism, pathogen and environment (1996), Academic Press, San Diego, USA 106-159
45. Grinde B. Lysozyme from rainbow trout, Salmo gairdneri Richardson, as an antibacterial agent against fish pathogens. Journal of Fish Diseases 12 (1989) 95-104
46. Ellis A.E. Immunity to bacteria in fish. Fish and Shellfish Immunology 9 (1999) 291-308
47. Lie Ø., Evensen Ø., Sørensen A., and Frøysadal E. Study on lysozyme activity in some fish species. Diseases of Aquatic Organisms 6 (1989) 1-5
48. Alcorn S.W., Murray A.L., and Pascho R.J. Effects of rearing temperature on immune functions in sockeye salmon (Oncorhynchus nerka). Fish and Shellfish Immunology 12 (2002) 303-334
49. Magnadóttir B. Innate immunity of fish (overview). Fish and Shellfish Immunology 20 (2006) 137-151
50. Secombes C. The non-specific immune system: cellular defenses. In: Iwama G., and Nakanishi T. (Eds). The fish immune system: Organism, pathogen and environment (1996), Academic Press, San Diego, USA 63-105
51. McLauchlan P.E., Collet B., Ingerslev E., Secombes C.J., Lorenzen N., and Ellis A.E. DNA vaccination against viral haemorrhagic septicaemia (VHS) in rainbow trout: size, dose, route of injection and duration of protection - early protection correlates with Mx expression. Fish and Shellfish Immunology 15 (2003) 39-50
52. LaPatra S.E., Corbeil S., Jones G.R., Shewmaker W.D., Lorenzen N., Anderson E.D., et al. Protection of rainbow trout against infectious hematopoietic necrosis virus four days after specific or semi-specific DNA vaccination. Vaccine 19 (2001) 4011-4019
53. Robertsen B. Expression of interferon and interferon-induced genes in salmonids in response to virus infection, interferon-inducing compounds and vaccination. Fish and Shellfish Immunology 25 (2008) 351-357
54. Trobridge G.D., Chiou P.P., Kim C.H., and Leong J.C. Induction of the Mx protein of rainbow trout Oncorhynchus mykiss in vitro and in vivo with poly I: C dsRNA and infectious hematopoietic necrosis virus. Diseases of Aquatic Organisms 30 (1997) 91-98
55. Robertsen B., Trobridge G., and Leong J.C. Molecular cloning of double-stranded RNA inducible Mx genes from Atlantic salmon (Salmo salar L.). Developmental and Comparative Immunology 21 5 (1997) 397-412
56. Acosta F., Lockhart K., Gahlawat S.K., Real F., and Ellis A.E. Mx expression in Atlantic salmon (Salmo salar L.) parr in response to Listonella anguillarum bacterin, lipopolysaccharide and chromosomal DNA. Fish and Shellfish Immunology 17 (2004) 255-263
57. Chiller J.M., Hodgins H.O., and Weiser R.S. Antibody response in rainbow trout (Salmo gairdneri) II. Studies on the kinetics of development of antibody-producing cells and on complement and natural haemolysin. Journal of Immunology 102 5 (1969) 1202-1207
58. Van Muiswinkel W.B., and Wiegertjes G.F. Immune responses after injection vaccination of fish. In: Gudding R., Lillehaug A., Midtlyng P.J., and Brown F. (Eds). Fish Vaccinology; Developments in Biological Standardization vol. 90 (1997), Karger, Basel, Switzerland 55-57
59. Marsden M.J., and Secombes C.J. The influence of vaccine preparations on the induction of antigen specific responsiveness in rainbow trout Oncorhynchus mykiss. Fish and Shellfish Immunology 7 (1997) 455-469
60. Eggset G., Mikkelsen H., and Killie J.-E.A. Immunocompetence and duration of immunity against Vibrio salmonicida and Aeromonas salmonicida after vaccination of Atlantic salmon Salmo salar L. at low and high temperatures. Fish and Shellfish Immunology 7 (1997) 247-260
61. Magor B.G., and Magor K.E. Evolution of effectors and receptors of innate immunity. Developmental and Comparative Immunology 25 (2001) 651-682
62. Sinyakov M.S., Dror M., Zhevelev H., Margel S., and Avtalion R.R. Natural antibodies and their significance in active immunisation and protection against a defined pathogen in fish. Vaccine 20 (2002) 3668-3674
63. Killie J.-E., and Jørgensen T.O. Immunoregulation in fish II: intermolecular-induced suppression of antibody responses studied by haptenated antigens in Atlantic salmon (Salmo salar L.). Developmental and Comparative Immunology 19 5 (1995) 389-404
64. Mor A., and Avtalion R.R. Transfer of antibody activity from immunized mother to embryo in tilapias. Journal of Fish Biology 37 (1990) 249-255
65. Midtlyng P.J., Reitan W., and Speilberg L. Experimental studies on the efficacy and side-effects of intraperitoneal vaccination of Atlantic salmon (Salmo salar L.) against furunculosis. Fish and Shellfish Immunology 6 (1996) 335-350
66. Lund V., Børdal S., Kjellsen O., Mikkelsen H., and Schrøder M.B. Comparison of antibody responses in Atlantic cod (Gadus morhua L.) to Aeromonas salmonicida and Vibrio anguillarum. Developmental and Comparative Immunology 30 (2006) 1145-1155
67. Muthiara L.W., Raymond B.T., Dekievit T.R., and Stevenson R.H.W. Antibody specificities of polyclonal rabbit and rainbow trout antisera against Vibrio ordalii and serotype O2 strains of Vibrio anguillarum. Canadian Journal of Microbiology 39 (1993) 492-499
68. Skinner L.A., Schulte P.M., Balfry S.K., McKinley R.S., and LaPatra S.E. The association between metabolic rate, immune parameters, and growth performance of rainbow trout (Oncorhynchus mykiss) following the injection of a DNA vaccine alone and concurrently with a polyvalent, oil-adjuvant vaccine. Fish and Shellfish Immunology 28 2 (2010) 387-393 doi:10.1016/j.fsi.2009.11.026.
69. Killie J.-E., and Jørgensen T.O. Immunoregulation in fish I: intramolecular-induced suppression of antibody responses to haptenated protein antigens studied in Atlantic salmon (Salmo salar L.). Developmental and Comparative Immunology 18 2 (1994) 123-136
70. Lund T., Chiayvareesajja J., Larsen H.S.J., and Rø K.H. Antibody response after immunisation as a potential indirect marker for improved resistance against furunculosis. Fish and Shellfish Immunology 5 (1995) 109-119
71. Fjalestad K.T., Jørgen H., Larsen S., and Rø K.H. Antibody response in Atlantic salmon (Salmo salar) against Vibrio anguillarum and Vibrio salmonicida O-antigens: heritabilities, genetic correlations and correlations with survival. Aquaculture 145 (1996) 77-89
72. Gudmundsdóttir B.K., and Magnadóttir B. Protection of Atlantic salmon (Salmo salar L.) against an experimental infection of Aeromonas salmonicida ssp. Achromogenes. Fish and Shellfish Immunology 7 (1997) 55-69
73. Gudmundsdóttir B.K., Jónsdóttir H., Steinthórsdóttir V., Magnadóttir B., and Gudmundsdóttir S. Survival and humoral antibody response of Atlantic salmon, Salmo salar L., vaccinated against Aeromonas salmonicida ssp. Achromogenes. Journal of Fish Diseases 20 (1997) 351-360
74. Hedrick R.P. Relationships of host, pathogen, and environment: implications for diseases of cultured and wild fish populations. Journal of Aquatic Animal Health 10 (1998) 107-111