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Molecular and immunohistochemical studies on epidermal responses in Atlantic salmon Salmo salar L. induced by Gyrodactylus salaris Malmberg, 1957

Published online by Cambridge University Press:  04 September 2009

P. W. Kania ,
O. Evensen ,
T. B. Larsen  and
K. Buchmann
P. W. Kania
Affiliation:
Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen, Frederiksberg C, Denmark
O. Evensen
Affiliation:
Norwegian School of Veterinary Science, Oslo, Norway
T. B. Larsen
Affiliation:
Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen, Frederiksberg C, Denmark
K. Buchmann*
Affiliation:
Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen, Frederiksberg C, Denmark
*
*Fax: +45 35332711 E-mail: [email protected]
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Abstract

Various strains of Atlantic salmon exhibit different levels of susceptibility to infections with the ectoparasitic monogenean Gyrodactylus salaris. The basic mechanisms involved in this differential ability to respond to this monogenean were elucidated using controlled and duplicated challenge experiments. Highly susceptible East Atlantic salmon allowed parasite populations to reach up to 3000 parasites per host within 6 weeks, whereas less susceptible Baltic salmon never reached larger parasite burdens than 122 parasites per host during the same period. The present study, comprising immunohistochemistry and gene expression analyses, showed that highly susceptible salmon erected a response mainly associated with an increased expression of interleukin-1β (IL-1β), interferon-γ (IFN-γ), IL-10 and infiltration of CD3-positive cells in the epidermis of infected fins. Less susceptible salmon showed no initial response in fins but 3–6 weeks post-infection a number of other genes (encoding the immune-regulating cytokine IL-10, cell marker MHC II and the pathogen-binding protein serum amyloid A) were found to be up-regulated. No proliferation of epithelial cells was seen in the skin of less susceptible salmon, and IL-10 may play a role in this regard. It can be hypothesized that resistant salmon regulate the parasite population by restricting nutrients (sloughed epithelial cells and associated material) and thereby starve the parasites. In association with this ‘scorched-earth strategy’, the production of pathogen-binding effector molecules such as serum amyloid A (SAA) (or others still not detected) may contribute to the resistance status of the fish during the later infection phases.

Type
Research Papers
Information
Journal of Helminthology , Volume 84 , Issue 2 , June 2010 , pp. 166 - 172
Copyright
Copyright © Cambridge University Press 2009

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References

Bakke, T.A. & Mackenzie, K. (1993) Comparative susceptibility of native Scottish and Norwegian stocks of Atlantic salmon, Salmo salar L. to Gyrodactylus salaris Malmberg: laboratory experiments. Fisheries Research 17, 69–85.CrossRefGoogle Scholar
Bakke, T.A., Harris, P.D. & Cable, J. (2002) Host specificity dynamics: observations on gyrodactylid monogeneans. International Journal for Parasitology 32, 281–308.CrossRefGoogle ScholarPubMed
Bakke-McKellep, A.M., Frøystad, M.K., Lilleng, E., Dapra, F., Refstie, S., Krogdahl, Å. & Landsverk, T. (2007) Response to soy: T-cell like reactivity in the intestine of Atlantic salmon, Salmo salar L. Journal of Fish Diseases 30, 13–25.CrossRefGoogle ScholarPubMed
Buchmann, K. (1998a) Binding and lethal effect of complement from Oncorhynchus mykiss on Gyrodactylus derjavini (Platyhelminthes: Monogenea). Diseases of Aquatic Organisms 32, 195–200.CrossRefGoogle ScholarPubMed
Buchmann, K. (1998b) Some histochemical characteristics of the mucous microenvironment in four salmonids with different susceptibilities to gyrodactylid infections. Journal of Helminthology 72, 101–107.CrossRefGoogle Scholar
Buchmann, K. & Uldal, A. (1997) Gyrodactylus derjavini infections in four salmonids: comparative host susceptibility and site selection of parasites. Diseases of Aquatic Organisms 28, 13–22.CrossRefGoogle Scholar
Buchmann, K., Madsen, K.K. & Dalgaard, M. (2004) Homing of Gyrodactylus salaris and G. derjavini (Monogenea) on different hosts and response post-attachment. Folia Parasitologica 51, 263–267.CrossRefGoogle Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M., & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle ScholarPubMed
Collins, C.M., Olstad, K., Sterud, E., Jones, C.S., Noble, L.R., Mo, T.A. & Cunningham, C.O. (2007a) Isolation of a FIP2-like gene from Atlantic salmon (Salmo salar L.) found upregulated following infection with the monogenean parasite Gyrodactylus salaris Malmberg, 1957. Fish and Shellfish Immunology 22, 282–288.CrossRefGoogle ScholarPubMed
Collins, C.M., Olstad, K., Sterud, E., Jones, C.S., Noble, L.R., Mo, T.A. & Cunningham, C.O. (2007b) Isolation of a thymidylate kinase gene, upregulated in Atlantic salmon (Salmo salar L.) following infection with the monogenean parasite. Gyrodactylus salaris. Fish and Shellfish Immunology 23, 793–807.CrossRefGoogle ScholarPubMed
Dalgaard, M.B., Nielsen, C.V. & Buchmann, K. (2003) Comparative susceptibility of two races of Salmo salar (Baltic Lule river and Atlantic Conon river strains) to infection with Gyrodactylus salaris. Diseases of Aquatic Organisms 53, 173–176.CrossRefGoogle ScholarPubMed
Dalgaard, M.B., Larsen, T.B., Jorndrup, S. & Buchmann, K. (2004) Differing resistance of Atlantic salmon strains and rainbow trout to Gyrodactylus salaris infection. Journal of Aquatic Animal Health 16, 109–115.CrossRefGoogle Scholar
Fast, M.D., Muise, D.M., Easy, R.E., Ross, N.W. & Johnson, S.C. (2006) The effects of Lepeophtheirus salmonis infections on the stress response and immunological status of Atlantic salmon (Salmo salar). Fish and Shellfish Immunology 21, 228–241.CrossRefGoogle ScholarPubMed
Grimholt, U., Drablos, F., Jorgensen, S.M., Hoyheim, B. & Stet, R.J.M. (2002) The major histocompatibility class I locus in Atlantic salmon (Salmo salar L.): polymorphism, linkage analysis and protein modeling. Immunogenetics 54, 570–581.CrossRefGoogle Scholar
Harris, P.D., Soleng, A. & Bakke, T.A. (1998) Killing of Gyrodactylus salaris (Platyhelminthes, Monogenea) mediated by host complement. Parasitology 117, 137–143.CrossRefGoogle ScholarPubMed
Heggberget, T.G., Johnsen, B.O., Hindar, K., Jonsson, B., Hansen, L.P., Hvidsten, N.A. & Jensen, A.J. (1993) Interactions between wild and cultured Atlantic salmon – A review of the Norwegian experience. Fisheries Research 18, 123–146.CrossRefGoogle Scholar
Heinecke, R.D., Martinussen, T. & Buchmann, K. (2007) Microhabitat selection of Gyrodactylus salaris Malmberg on different salmonids. Journal of Fish Diseases 30, 733–743.CrossRefGoogle ScholarPubMed
Johnsen, B.O. (1978) The effect of an attack by the parasite Gyrodactylus salaris on the population of salmon parr in the river Lakselva, Misvaer in northern Norway. Astarte 11, 7–9.Google Scholar
Johnsen, B.O. & Jensen, A.J. (1986) Infestations of Atlantic salmon, Salmo salar, by Gyrodactylus salaris in Norwegian rivers. Journal of Fish Biology 29, 233–241.CrossRefGoogle Scholar
Johnsen, B.O. & Jensen, A.J. (1991) The Gyrodactylus story in Norway. Aquaculture 98, 289–302.CrossRefGoogle Scholar
Jones, S.R., Fast, M.D. & Johnson, S.C. (2008) Influence of reduced feed ration on Lepeophtheirus salmonis infestation and inflammatory gene expression in juvenile pink salmon. Journal of Aquatic Animal Health 20, 103–109.CrossRefGoogle ScholarPubMed
Jørndrup, S. & Buchmann, K. (2005) Carbohydrate localization on Gyrodactylus salaris and G. derjavini and corresponding carbohydrate binding capacity of their hosts Salmo salar and S. trutta. Journal of Helminthology 79, 41–46.CrossRefGoogle Scholar
Kania, P.W., Larsen, T.B., Ingerslev, H.C. & Buchmann, K. (2007) Baltic salmon activates immune relevant genes in fin tissue when responding to Gyrodactylus salaris infection. Diseases of Aquatic Organisms 76, 81–85.CrossRefGoogle ScholarPubMed
Lilleeng, E., Penn, M.H., Haugland, Ø., Xu, C., Bakke, A.M., Krogdahl, Å., Landsverk, T. & Frøystad-Saugen, M.K. (2009) Decreased expression of TGF-β, GILT, and T-cell markers in the early stages of soybean enteropathy in Atlantic salmon (Salmo salar L.). Fish and Shellfish Immunology, in press.CrossRefGoogle ScholarPubMed
Lindenstrøm, T., Sigh, J., Dalgaard, M.B. & Buchmann, K. (2006) Skin expression of IL-1 beta in East Atlantic salmon, Salmo salar L., highly susceptible to Gyrodactylus salaris infection is enhanced compared to a low susceptibility Baltic stock. Journal of Fish Diseases 29, 123–128.CrossRefGoogle Scholar
Liu, Y., Moore, L., Koppang, E.O. & Hordvik, I. (2008) Characterization of the CD3 zeta, CD3 gamma delta and CD3 epsilon subunits of the T-cell receptor complex in Atlantic salmon. Developmental and Comparative Immunology 32, 26–35.CrossRefGoogle Scholar
Livak, K. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and 2− ΔΔCT method. Methods (Orlando) 25, 402–408.Google Scholar
Malmberg, G. (1993) Gyrodactylidae and gyrodactylosis of salmonidae. Bulletin Francais de Peche et Pisciculture 1, 5–46.CrossRefGoogle Scholar
Malmberg, G. (2004) How the ‘salmon killer’ Gyrodactylus salaris Malmberg, 1957 was discovered and described in Sweden. Report from the front. pp. 12-18 in Buchmann, K. (Ed.) Diagnosis and control of fish diseases. Denmark, Frederiksberg Bogtrykkeri.Google Scholar
Matejusova, I., Felix, B.M., Sorsa-Leslie, T., Gilbey, J., Noble, L.R., Jones, C.S. & Cunningham, C.O. (2006) Gene expression profiles of some immune relevant genes from skin of susceptible and responding Atlantic salmon (Salmo salar L.) infected with Gyrodactylus salaris. International Journal for Parasitology 36, 1175–1183.CrossRefGoogle ScholarPubMed
Mo, T.A. (1994) Status of Gyrodactylus salaris problems and research in Norway. pp. 43–56in Pike, A.W. & Lewis, J.W. (Eds) Parasitic diseases of fish. Tresaith, Dyfed, Samara Publishing.Google Scholar
Raida, M. & Buchmann, K. (2008) Development of adaptive immunity in rainbow trout, Oncorhynchus mykiss (Walbaum) surviving an infection with Yersinia ruckeri. Fish and Shellfish Immunology 25, 533–541.CrossRefGoogle ScholarPubMed
Shah, C., Hari-Dass, R. & Raynes, J.G. (2006) Serum amyloid A is an innate immune opsonin for Gram-negative bacteria. Blood 108, 1751–1757.CrossRefGoogle ScholarPubMed
Sterud, E., Harris, P.H. & Bakke, T.A. (1998) The influence of Gyrodactylus salaris Malmberg, 1957 (Monogenea) on the epidermis of Atlantic salmon, Salmo salar L., and brook trout, Salvelinus fontinalis (Mitchell), experimental studies. Journal of Fish Diseases 21, 257–263.CrossRefGoogle Scholar