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The expression of immune-regulatory genes in rainbow trout, Oncorhynchus mykiss, during a natural outbreak of proliferative kidney disease (PKD)

Published online by Cambridge University Press:  10 November 2003

J. W. HOLLAND
Affiliation:
Scottish Fish Immunology Research Centre, School of Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK
C. R. W. GOULD
Affiliation:
Schering-Plough Aquaculture, Aquaculture Centre, Saffron Walden, Essex, CB10 1EJ, UK
C. S. JONES
Affiliation:
Scottish Fish Immunology Research Centre, School of Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK
L. R. NOBLE
Affiliation:
Scottish Fish Immunology Research Centre, School of Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK
C. J. SECOMBES
Affiliation:
Scottish Fish Immunology Research Centre, School of Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK

Abstract

Proliferative kidney disease (PKD) is a parasitic infection of salmonid fish characterized by an apparently abnormal immune response to the presence of the myxozoan parasite, Tetracapsuloides bryosalmonae. In order to examine the nature of the immune response at the molecular level, the expression of a range of immune regulatory genes, including cytokines and cyclooxygenase (COX)-2 was examined in naive unexposed fish and in naive fish exposed to parasite-infected water at three points during the course of a natural outbreak of PKD. Since fish with advanced PKD pathology generally exhibit increased susceptibility to secondary infections which is typical of stress/cortisol-mediated immune suppression, a further aim of this work was to examine in vitro the influence of the glucocorticoid cortisol on the bacterial lipopolysaccharide (LPS)-induced expression of the trout cytokine genes studied. Two weeks after the initial sampling, naive exposed fish showed a specific profile of up-regulated tumor necrosis factor (TNF)-α2, COX-2 and, to a lesser extent, transforming growth factor (TGF)-β1 expression. As the disease pathology increased, TNF-α2 and COX-2 expression returned to normal levels. Stress levels of cortisol suppressed the LPS inducibility of pro-inflammatory cytokine genes, although TGF-β1 and TNF-α2 appeared to be refractory. These data demonstrate that specific immune responses at the molecular level are affected during PKD infection, with the cortisol suppression of cytokine expression in vitro providing a possible link to PKD-mediated cytokine down-regulation and immune suppression.

Type
Research Article
Copyright
© 2003 Cambridge University Press

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References

REFERENCES

CANNING, E. U., CURRY, A., FEIST, S. W., LONGSHAW, M. & OKAMURA, B. (1999). Tetracapsula bryosalmonae n. sp. for PKX organism, the cause of PKD in salmonid fish. Bulletin of the European Association of Fish Pathologists 19, 203206.Google Scholar
CANNING, E. U., TOPS, S., CURRY, A., WOOD, T. S. & OKAMURA, B. (2002). Ecology, development and pathogenicity of Buddenbrockia plumatellae Schröder, 1910 (Myxozoa, Malacosporea) (syn. Tetracapsula bryozoides) and establishment of Tetracapsuloides n. gen. for Tetra capsula bryosalmonae. Journal of Eukaryotic Microbiology 49, 280295.Google Scholar
CHILMONCZYK, S., MONGE, D. & De KINKELIN, P. (2002). Proliferative kidney disease: cellular aspects of the rainbow trout, Oncorhynchus mykiss (Walbaum), response to parasitic infection. Journal of Fish Diseases 25, 217226.CrossRefGoogle Scholar
CLIFTON-HADLEY, R. S., BUCKE, D. & RICHARDS, R. H. (1987). A study of the sequential clinical and pathological changes during proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson. Journal of Fish Diseases 10, 335352.CrossRefGoogle Scholar
DAVIS, K. B., GRIFFIN, B. R. & GRAY, W. L. (2002). Effect of handling stress on susceptibility of channel catfish Ictaluras punctatus to Ichthyophthirius multifiliis and channel catfish virus infection. Aquaculture 214, 5566.CrossRefGoogle Scholar
DINARELLO, C. A. (1997). Interleukin-1. Cytokine and Growth Factor Reviews 8, 253265.CrossRefGoogle Scholar
Di PIRO, J. T. (1997). Cytokine networks with infection: mycobacterial infections, leishmaniasis, human immunodeficiency virus infection, and sepsis. Pharmacotherapy 17, 205223.Google Scholar
ELENKOV, I. J. & CHROUSOS, G. P. (1999). Stress hormones, Th1Th2 patterns, pro/anti-inflammatory cytokines and susceptibility to disease. Trends in Endocrinology and Metabolism 9, 359368.CrossRefGoogle Scholar
FEIST, S. W., LONGSHAW, M., CANNING, E. U. & OKAMURA, B. (2001). Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae. Diseases of Aquatic Organisms 45, 6168.CrossRefGoogle Scholar
FOOTT, J. S. & HEDRICK, R. P. (1987). Seasonal occurrence of the infectious stage of proliferative kidney disease (PKD) and resistence of rainbow trout, Salmo gairdneri Richardson to re-infection. Journal of Fish Biology 30, 477483.CrossRefGoogle Scholar
GOLDFIELD, A. E. & TSAI, E. Y. (1996). TNF-α and genetic susceptibility to parasitic disease. Experimental Parasitology 84, 300303.CrossRefGoogle Scholar
GOULD, C. R. W. (1995). Studies on proliferative kidney disease (PKD) in rainbow trout, Oncorhynchus mykiss. Ph.D. Thesis. University of Aberdeen.
GRAYSON, T. H., COOPER, L. F., WRATHMELL, A. B., ROPER, J., EVENDEN, A. J. & GILPIN, M. L. (2002). Host responses to Renibacterium salmoninarum and specific components of the pathogen reveal the mechanisms of immune suppression and activation. Immunology 106, 273283.CrossRefGoogle Scholar
HARRIS, P. D., SOLENG, A. & BAKKE, T. A. (2000). Increased susceptibility of salmonids to the monogenean Gyrodactylus salaris following administration of hydrocortisone acetate. Parasitology 120, 5764.CrossRefGoogle Scholar
HERSCHMAN, H. R. (1996). Prostaglandin synthase 2. Biochimica et Biophysica Acta 1299, 125140.CrossRefGoogle Scholar
HOLLAND, J. W., POTTINGER, T. G. & SECOMBES, C. J. (2002). Recombinant interleukin-1β activates the hypothalamic-pituitary-interrenal axis in rainbow trout, Oncorhynchus mykiss. Journal of Endocrinology 175, 261267.CrossRefGoogle Scholar
HONG, S., ZOU, J., CRAMPE, M., PEDDIE, S., SCAPIGLIATI, G., BOLS, N., CUNNINGHAM, C. & SECOMBES, C. J. (2001). The production and bioactivity of rainbow trout (Oncorhynchus mykiss) recombinant IL-1β. Veterinary Immunology and Immunopathology 81, 114.CrossRefGoogle Scholar
JANKOVIC, D., SHER, A. & YAP, G. (2001). Th1/Th2 effector choice in parasite infection: decision making by committee. Current Opinion in Immunology 13, 403409.CrossRefGoogle Scholar
LAING, K. J., ZOU, J. J., WANG, T., BOLS, N., HIRONO, I., AOKI, T. & SECOMBES, C. J. (2002). Identification and analysis of an interleukin 8-like molecule in rainbow trout Oncorhynchus mykiss. Developmental and Comparative Immunology 26, 433444.CrossRefGoogle Scholar
LAURENT, F., ECKMANN, L., SAVIDGE, T. C., MORGAN, G., THEODOS, C., NACIRI, M. & KAGNOFF, M. F. (1997). Cryptosporidium parvum infection of human intestinal epithelial cells induces the polarized secretion of C-X-C chemokines. Infection and Immunity 65, 50675073.Google Scholar
LAURENT, F., MANCASSOLA, R., LACROIX, S., MENEZES, R. & NACIRI, M. (2001). Analysis of chicken mucosal immune response to Eimeria tenella and Eimeria maxima infection by quantitative reverse transcription-PCR. Infection and Immunity 69, 25272534.CrossRefGoogle Scholar
LETTERIO, J. J. & ROBERTS, A. B. (1998). Regulation of immune responses by TGF-β. Annual Review of Immunology 16, 137161.CrossRefGoogle Scholar
McGUIRE, W., HILL, A. V. S., ALLSOPP, C. E. M., GREENWOOD, B. M. & KWIATOWSKI, D. (1994). Variation in the TNF-α promoter region associated with susceptibility to cerebral malaria. Nature 371, 508511.CrossRefGoogle Scholar
MUKAIDA, N., HARADA, A. & MATSUSHIMA, K. (1998). Interleukin-8 (IL-8) and monocyte chemotactic and activating factor (MCAF/MCP-1), chemokines essentially involved in inflammatory and immune reactions. Cytokine and Growth Factor Reviews 9, 923.CrossRefGoogle Scholar
OLESEN, N. J. & JORGENSEN, P. E. V. (1986). Quantification of serum immunoglobulin in rainbow trout Salmo gairdneri under various environmental conditions. Diseases of Aquatic Organisms 1, 183189.Google Scholar
OMER, F. M., KURTZHALS, J. A. L. & RILEY, E. M. (2000). Maintaining the immunological balance in parasitic infections: a role for TGF-β? Parasitology Today 16, 1823.Google Scholar
RAMASWAMY, K., KUMAR, P. & HE, Y. X. (2000). A role for parasite-induced PGE2 in IL-10-mediated host immunoregulation by skin stage schistosomula of Schistosoma mansoni. Journal of Immunology 165, 45674574.CrossRefGoogle Scholar
SAEIJ, J. P. J., VERBURG-VAN KEMENADE, L. B. M., VAN MUISWINKEL, W. B. & WIEGERTJES, G. F. (2003). Daily handling stress reduces resistence of carp to Trypanoplasma borreli: in vitro modulatory effects of cortisol on leukocyte function and apoptosis. Developmental and Comparative Immunology 27, 233245.CrossRefGoogle Scholar
SAPOLSKY, R. M., ROMERO, L. M. & MUNCK, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21, 5589.CrossRefGoogle Scholar
SAULNIER, D. & De KINKELIN, P. (1996). Antigenic and biochemical study of PKX, the myxosporean causative agent of proliferative kidney disease of salmonid fish. Diseases of Aquatic Organisms 27, 103114.CrossRefGoogle Scholar
SECOMBES, C. J., WANG, T., HONG, S., PEDDIE, S., CRAMPE, M., LAING, K. J., CUNNINGHAM, C. & ZOU, J. (2001). Cytokines and innate immunity of fish. Developmental and Comparative Immunology 25, 713723.CrossRefGoogle Scholar
SHER, A. & COFFMAN, R. L. (1992). Regulation of immunity to parasites by T cells and T cell-derived cytokines. Annual Review of Immunology 10, 385409.CrossRefGoogle Scholar
VILCEK, J. & LEE, T. H. (1991). Tumor necrosis factor. Journal of Biological Chemistry 266, 73137316.Google Scholar
WIENS, G. D. & KAATTARI, S. L. (1999). Bacterial kidney disease (Renibacterium salmoninarum). In Fish Diseases and Disorders: Viral, Bacterial and Fungal Infections, Vol. 3 (ed. Woo, P. T. K. & Bruno, D. W.), pp. 269301. New York, CABI Publishing.
ZOU, J., CUNNINGHAM, C. & SECOMBES, C. J. (1999 a). The rainbow trout Oncorhynchus mykiss interleukin-1β gene has a different organisation to mammals and undergoes incomplete splicing. European Journal of Biochemistry 259, 901908.Google Scholar
ZOU, J., HOLLAND, J., PLEGUEZUELOS, O., CUNNINGHAM, C. & SECOMBES, C. J. (2000). Factors influencing the expression of interleukin-1β in cultured rainbow trout (Oncorhynchus mykiss) leucocytes. Developmental and Comparative Immunology 24, 575582.CrossRefGoogle Scholar
ZOU, J., NEUMANN, N. F., HOLLAND, J. W., BELOSEVIC, M., CUNNINGHAM, C., SECOMBES, C. J. & ROWLEY, A. F. (1999 b). Fish macrophages express a cyclo-oxygenase-2 homologue after activation. Biochemical Journal 340, 153159.Google Scholar
ZOU, J., WANG, T., HIRONO, I., AOKI, T., INAGAWA, H., HONDA, T., SOMA, G.-I., OTOTAKE, M., NAKANISHI, T., ELLIS, A. E. & SECOMBES, C. J. (2002). Differential expression of two tumor necrosis factor genes in rainbow trout, Oncorhynchus mykiss. Developmental and Comparative Immunology 26, 161172.CrossRefGoogle Scholar