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Correlation between heat-shock protein induction and reduced metabolic condition in juvenile steelhead trout (Oncorhynchus mykiss) chronically exposed to elevated temperature

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Abstract

The metabolic condition, stress response, and growth rates of juvenile steelhead trout (Oncorhynchus mykiss) were assessed throughout a 10-week exposure to 15 and 20 °C, each at full and half food ration. Metabolic measurements included white muscle phosphocreatine (PCr), ATP, ADP and AMP, hepatic glycogen, and global metabolite profiling of muscle and liver using 1H nuclear magnetic resonance (NMR) spectroscopy. Stress was assessed via induction of heat shock proteins (hsps) 63, 72, 78 and 89, and growth was determined from otolith measurements. Exposure to 20 °C induced hsp synthesis, particularly hsp72. Principal components analyses revealed positive correlations between increased stress (elevated hsp72 and hsp89) and decreased metabolic condition (decreased PCr, ATP and glycogen). However, no effect on growth was observed, suggesting that 20 °C is the upper limit of the steelhead trout's preferred range. The NMR analysis of multiple metabolite classes not only identified a decrease in PCr, ATP and glycogen in temperature exposed fish, but also provided a more integrated description of the biochemical response to thermal stress.

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References

  • Abe, H. and Ohmama, S. 1987. Effect of starvation and seawater acclimation on the concentration of free L-histidine and related dipeptides in the muscle of eel, rainbow trout and Japanese dace. Comp. Biochem. Physiol. B88: 507–511.

    Google Scholar 

  • Ally, A. and Park, G. 1992. Rapid determination of creatine, phosphocreatine, purine bases and nucleotides (ATP, ADP, AMP, GTP, GDP) in heart biopsies by gradient ion-pair reversed-phase liquid chromatography. J. Chromatogr. 575: 19–27.

    PubMed  CAS  Google Scholar 

  • Blatter, D.P., Garner, F., Van Slyke, K. and Bradley, A. 1972. Quantitative electrophoresis in polyacrylamide gels of 2-40%. J. Chromatogr. 64: 147–155.

    Article  Google Scholar 

  • Bollard, M.E., Garrod, S., Holmes, E., Lindon, J.C., Humpfer, E., Spraul, M. and Nicholson, J.K. 2000. High-resolution 1H and 1H-13C magic angle spinning NMR spectroscopy of rat liver. Magn. Reson. Med. 44: 201–207.

    Article  PubMed  CAS  Google Scholar 

  • Bundy, J.G., Lenz, E.M., Bailey, N.J., Gavaghan, C.L., Svendsen, C., Spurgeon, D., Hankard, P.K., Osborn, D., Weeks, J.M. and Trauger, S.A. 2002. Metabonomic assessment of toxicity of 4-fluoroaniline, 3,5-difluoroaniline and 2-fluoro-4-methylaniline to the earthworm Eisenia veneta: Identification of new endogenous biomarkers. Environ. Toxicol. Chem. 21: 1966–1972.

    Article  Google Scholar 

  • Bundy, J.G., Osborn, D., Weeks, J.M., Lindon, J.C. and Nicholson, J.K. 2001. An NMR-based metabonomic approach to the investigation of coelomic fluid biochemistry in earthworms under toxic stress. FEBS Lett. 500: 31–35.

    Article  PubMed  CAS  Google Scholar 

  • Carr, R.S. and Neff, J.M. 1984. Quantitative semi-automated enzymatic assay for tissue glycogen. Comp. Biochem. Physiol. B77: 447–449.

    Google Scholar 

  • Coutant, C.C. 1977. Compilation of temperature preference data. J. Fish. Res. Board Can. 34: 739–745.

    Google Scholar 

  • Fan, W.M.T. 1996. Metabolite profiling by one-and twodimensional NMR analysis of complex mixtures. Prog. Nucl. Mag. Res. 28: 161–219.

    CAS  Google Scholar 

  • Farkas, T., Fodor, E., Kitajka, K. and Halver, J.E. 2001. Response of fish membranes to environmental temperature. Aquac. Res. 32: 645–655.

    Article  CAS  Google Scholar 

  • Feder, J.H., Rossi, J.M., Solomon, J., Solomon, N. and Lindquist, S. 1992. The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes Dev. 6: 1402–1413.

    PubMed  CAS  Google Scholar 

  • Feder, M.E. and Hofmann, G.E. 1999. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annu. Rev. Physiol. 61: 243–282.

    Article  PubMed  CAS  Google Scholar 

  • Feige, U., Morimoto, R.I., Yahara, I. and Polla, B.S. 1996. Stress-inducible cellular responses. Birkhauser Verlag, Basel, Switzerland.

  • Hawkins, A.J.S. 1985. Relationships between the synthesis and breakdown of protein, dietary absorption and turnovers of nitrogen and carbon in the blue mussel, mytilus edulis. Oecologia 66: 42–49.

    Article  Google Scholar 

  • Hochachka, P.W. and Somero, G.N. 1984. Biochemical Adaptation. p. 538. Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  • Iwama, G.K., Thomas, P.T., Forsyth, R.B. and Vijayan, M.M. 1998.Heat shock protein expression in fish. Rev. Fish Biol. Fisher. 8: 35–56.

    Article  Google Scholar 

  • Krebs, R.A. and Feder, M.E. 1997. Deleterious consequences of Hsp70 over-expression in Drosophila melanogaster larvae. Cell Stress Chaperones 2: 60–71.

    Article  PubMed  CAS  Google Scholar 

  • Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.

    Article  PubMed  CAS  Google Scholar 

  • Lehoux, E.A. and Guderley, H.E. 1997. Thermally induced changesin intracellular pH and modulators of phosphofructokinase in trout white muscle. J. Exp. Biol. 200: 931–939.

    PubMed  CAS  Google Scholar 

  • Lindon, J.C., Holmes, E. and Nicholson, J.K. 2001. Pattern recognition methods and applications in biomedical magnetic resonance. Prog. Nucl. Magn. Reson. Spec. 39: 1–40.

    Article  CAS  Google Scholar 

  • Moon, T.W. and Foster, G.D. 1995. Tissue carbohydrate metabolism, gluconeogenesis and hormonal and environmental influences. In: Biochemistry and molecular biology of fishes. Vol. 4, Metabolic Biochemistry, pp. 65–100. Edited by P.W. Hochachka and T.P. Mommsen. Elsevier, Amsterdam.

    Google Scholar 

  • Morgan, I.J., McDonald, D.G. and Wood, C.M. 2001. The cost of living for freshwater fish in a warmer more polluted environment. Global Change Biol. 7: 345–355.

    Article  Google Scholar 

  • Morita, K. and Matsuishi, T. 2001. A new model of growth backcalculation incorporating age effect based on otoliths. Can. J. Fish. Aquat. Sci. 58: 1805–1811.

    Article  Google Scholar 

  • Myrick, C.A. and Cech, Jr. J.J. 2001. Temperature effects on chinook salmon and steelhead: a review focusing on California's Central Valley populations. Tech. Pub. 01-1. California Water and Environmental Modeling Forum, P.O. Box 488, Sacramento, CA 95812, U.S.A.

  • Nicholson, J.K., Connelly, J., Lindon, J.C. and Holmes, E. 2002. Metabonomics: a platform for studying drug toxicity and gene function. Nat. Rev. Drug Discov. 1: 153–161.

    Article  PubMed  CAS  Google Scholar 

  • Pereira, C., Vijayan, M.M. and Moon, T.W. 1995. In vitro hepatocyte metabolism of alanine and glucose and the response to insulin in fed and fasted rainbow trout. J. Exp. Zool. 271: 425–431.

    Article  CAS  Google Scholar 

  • Piper, R.G., McElwain, I.B., Orme, L.E., McCraren, J.P., Fowler, L.G. and Leonard, J.R. 1986. Fish Hatchery Management. American Fisheries Society and United States Dept. of the Interior, Fish and Wildlife Service, Washington, D.C.

    Google Scholar 

  • Robosky, L.C., Robertson, D.G., Baker, J.D., Rane, S. and Reily, M.D. 2002. In vivo toxicity screening programs using metabonomics. Comb. Chem. High T. Scr. 5: 651–662.

    CAS  Google Scholar 

  • Shiau, C.Y., Pong, Y.P., Chiou, T.K. and Tin, Y.Y. 2001. Effect of starvation on free histidine and amino acids in white muscle of milkfish Chanos chanos. Comp. Biochem. Physiol. B128: 501–506.

    Google Scholar 

  • Smutna, M., Vorlova, L. and Svobodova, Z. 2002. Pathobiochemistry of ammonia in the internal environment of fish. Acta Vet. Brno 71: 169–181.

    CAS  Google Scholar 

  • Sullivan, K., Douglas, J.M., Cardwell, R.D., Toll, J.E. and Duke, S. 2000. An analysis of the effects of temperature on salmonids of the Pacific Northwest with implications for selecting temperature criteria. Sustainable Ecosystems Institute, 8835 SW Canyon Lane, Suite 210, Portland, OR 97225, U.S.A.

    Google Scholar 

  • Viant, M.R. 2003. Improved methods for the acquisition and interpretation of NMR metabolomic data. Biochem. Biophys. Res. Comm. 310: 943–948.

    Article  PubMed  CAS  Google Scholar 

  • Viant, M.R., Rosenblum, E.S. and Tjeerdema, R.S. 2003. NMRbased metabolomics: A powerful approach for characterizing the effects of environmental stressors on organism health. Environ. Sci. Technol. 37: 4982–4989.

    Article  PubMed  CAS  Google Scholar 

  • Werner, I., Smith, T.B., Feliciano, J. and Johnson, M.L. 2004. Heatshock proteins in juvenile steelhead trout (Oncorhynchus mykiss) reflect thermal conditions in the Navarro River watershed, California, U.S.A. Trans. Am. Fish. Soc. (accepted).

  • Williams, E.E. and Hazel, J.R. 1994. Thermal adaptation in fish membranes: temporal resolution of adaptive mechanisms. In: Temperature adaptation of biological membranes. pp. 91–106. Edited by A.R. Cossins. Portland Press, Chapel Hill.

    Google Scholar 

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Author notes

  1. M.R. Viant

    Present address: School of Biosciences, The University of Birmingham, Egdbaston, Birmingham, B15 2TT, UK

  2. A.S. Gantner

    Present address: Pacific Ecorisk, 832 Arnold Drive,Suite 104, Martinez, 94553, CA, USA

Authors and Affiliations

  1. Department of Environmental Toxicology, College of Agricultural and Environmental Sciences, University of California, One Shields Avenue, Davis, 95616, CA, USA

    M.R. Viant, E.S. Rosenblum & R.S. Tjeerdema

  2. Department of Anatomy,Physiology and Cell Biology,School of Veterinary Medicine, University of California, One Shields Avenue, Davis, 95616, CA, USA

    I. Werner

  3. John Muir Institute of the Environment, University of California, One Shields Avenue, Davis, 95616, CA, USA

    A.S. Gantner & M.L. Johnson

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Correspondence to M.R. Viant.

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Viant, M., Werner, I., Rosenblum, E. et al. Correlation between heat-shock protein induction and reduced metabolic condition in juvenile steelhead trout (Oncorhynchus mykiss) chronically exposed to elevated temperature. Fish Physiology and Biochemistry 29, 159–171 (2003). https://doi.org/10.1023/B:FISH.0000035938.92027.81

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