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Effects of seasonal and latitudinal cold on oxidative stress parameters and activation of hypoxia inducible factor (HIF-1) in zoarcid fish

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Abstract

Acute, short term cooling of North Sea eelpout Zoarces viviparus is associated with a reduction of tissue redox state and activation of hypoxia inducible factor (HIF-1) in the liver. The present study explores the response of HIF-1 to seasonal cold in Zoarces viviparus, and to latitudinal cold by comparing the eurythermal North Sea fish to stenothermal Antarctic eelpout (Pachycara brachycephalum). Hypoxic signalling (HIF-1 DNA binding activity) was studied in liver of summer and winter North Sea eelpout as well as of Antarctic eelpout at habitat temperature of 0°C and after long-term warming to 5°C. Biochemical parameters like tissue iron content, glutathione redox ratio, and oxidative stress indicators were analyzed to see whether the cellular redox state or reactive oxygen species formation and HIF activation in the fish correlate. HIF-1 DNA binding activity was significantly higher at cold temperature, both in the interspecific comparison, polar vs. temperate species, and when comparing winter and summer North Sea eelpout. Compared at the low acclimation temperatures (0°C for the polar and 6°C for the temperate eelpout) the polar fish showed lower levels of lipid peroxidation although the liver microsomal fraction turned out to be more susceptible to lipid radical formation. The level of radical scavenger, glutathione, was twofold higher in polar than in North Sea eelpout and also oxidised to over 50%. Under both conditions of cold exposure, latitudinal cold in the Antarctic and seasonal cold in the North Sea eelpout, the glutathione redox ratio was more oxidised when compared to the warmer condition. However, oxidative damage parameters (protein carbonyls and thiobarbituric acid reactive substances (TBARS) were elevated only during seasonal cold exposure in Z. viviparus. Obviously, Antarctic eelpout are keeping oxidative defence mechanisms high enough to avoid accumulation of oxidative damage products at low habitat temperature. The paper discusses how HIF could be instrumental in cold adaptation in fish.

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Acknowledgments

The authors would like to thank Maike Schmidt for her help in preparing the fish samples, as well as Tamara Zaobornyj and Laura Valdez for adjusting the chemiluminescence assay protocol to fish liver tissue. We further thank Hanna Tranberg, Eeva Rissanen and Kristiina Vuori for their contribution to adjust EMSA and Western blot methodology to eelpout samples. This study was supported by grants from Deutscher Akademischer Austauschdienst (DAAD) to KH.

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Authors and Affiliations

  1. Alfred-Wegener-Institute for Polar and Marine Research, Am Handelshafen 12, 27570, Bremerhaven, Germany

    K. Heise, H. O. Pörtner & D. Abele

  2. Physical Chemistry-PRALIB, School of Pharmacy and Biochemistry University of Buenos Aires, Junin 956, C 1113 AAD, Buenos Aires, Argentina

    M. S. Estevez, S. Puntarulo & M. Galleano

  3. Animal Physiology, Department of Biology, University of Turku, 20014, Turku, Finland

    M. Nikinmaa

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  1. K. Heise
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  2. M. S. Estevez
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  3. S. Puntarulo
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  4. M. Galleano
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  5. M. Nikinmaa
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  6. H. O. Pörtner
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  7. D. Abele
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Correspondence to D. Abele.

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Communicated by G. Heldmaier.

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Heise, K., Estevez, M.S., Puntarulo, S. et al. Effects of seasonal and latitudinal cold on oxidative stress parameters and activation of hypoxia inducible factor (HIF-1) in zoarcid fish. J Comp Physiol B 177, 765–777 (2007). https://doi.org/10.1007/s00360-007-0173-4

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  • DOI: https://doi.org/10.1007/s00360-007-0173-4

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