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Estrogen Modulates Hepatic Gene Expression and Survival of Rainbow Trout Infected with Pathogenic Bacteria Yersinia ruckeri

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Abstract

In the aquatic environment, fish are exposed to various stimuli at once and have developed different response mechanisms to deal with these multiple stimuli. The current study assessed the combined impacts of estrogens and bacterial infection on the physiological status of fish. Juvenile rainbow trout were exposed to two different concentrations of 17β-estradiol (E2) (2 or 20 mg/kg feed) and then infected with three concentrations of Yersinia ruckeri, a bacterial pathogen causing massive losses in wild and farmed salmonid populations. Organism-level endpoints to assess the impact of the single and combined treatments included hepatic vitellogenin transcript expression to evaluate the E2 exposure efficiency and survival rate of pathogen-challenged fish. The two E2 doses increased vitellogenin levels within the physiological range. Infection with Y. ruckeri caused mortality of trout, and this effect was significantly enhanced by a simultaneous exposure to high E2 dose. The hormone reduced survival at intermediate and high (104 and 106 colony forming units, cfu) bacterial concentrations, but not for a low one (102 cfu). Analysis of hepatic gene expression profiles by a salmonid 2 k cDNA microarray chip revealed complex regulations of pathways involved in immune responses, stress responses, and detoxicification pathways. E2 markedly reduced the expression of several genes implicated in xenobiotic metabolism. The results suggest that the interaction between pathogen and E2 interfered with the fish’s capability of clearing toxic compounds. The findings of the current study add to our understanding of multiple exposure responses in fish.

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Acknowledgments

We kindly thank the Pisciculture de la Gruyère, Neirivue, Switzerland, for providing the juvenile rainbow trout used for this study. We also wish to thank the Turku Centre of Biotechnology (Finland) for the preparation of microarrays. Additionally, we thank Dr. Markus Doherr for his valuable help on statistical matters. This study was supported by the European Commission through the project MODELKEY (contract no. 511237-GOCE) and through the Swiss National Fond SNF project “Mitogenic and growth-promoting hormones: do they regulate development, growth and function of immune genes in fish”.

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Authors and Affiliations

  1. Neuro-Endocrine Immune Interactions Research Group, Institute of Anatomy, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland

    Michael Wenger

  2. Nofima, Postbox 210, 1431, Ås, Norway

    Aleksei Krasnov, Stanko Skugor & Sergey Afanasyev

  3. Institute of Veterinary Bacteriology, University of Bern, Länggass-Strasse 122, 3012, Bern, Switzerland

    Elinor Goldschmidt-Clermont

  4. Center for Fish and Wildlife Health, Department of Pathobiology, University of Berne, Laenggassstrasse 122, 3012, Bern, Switzerland

    Ursula Sattler & Helmut Segner

  5. Sechenov Institute of Evolutionary Physiology and Biochemistry, St. Petersburg, 194223, Russia

    Sergey Afanasyev

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  1. Michael Wenger
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  2. Aleksei Krasnov
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  3. Stanko Skugor
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Correspondence to Michael Wenger.

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Wenger, M., Krasnov, A., Skugor, S. et al. Estrogen Modulates Hepatic Gene Expression and Survival of Rainbow Trout Infected with Pathogenic Bacteria Yersinia ruckeri . Mar Biotechnol 14, 530–543 (2012). https://doi.org/10.1007/s10126-012-9473-0

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