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Chaperone roles for TMAO and HSP70 during hyposmotic stress in the spiny dogfish shark (Squalus acanthias)

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Abstract

Salinity decreases are experienced by many marine elasmobranchs. To understand how these fishes cope with hyposmotic stress on a cellular level, we used the spiny dogfish shark (Squalus acanthias) as a model to test whether a reciprocal relationship exists between the cell’s two primary protein protection mechanisms, the chemical (e.g., trimethylamine oxide, TMAO) and molecular (e.g., heat shock protein 70, HSP70) chaperone systems. This relationship is interesting given that many elasmobranchs are expected to gain water and lose osmolytes, chemical chaperones, and ions as they osmoconform to new, lowered salinity. Dogfish were cannulated for repeated blood sampling and exposed to 70 % seawater (SW) for 48 h. These hyposmotic conditions had no effect on red blood cell (RBC) and white muscle TMAO concentrations, and did not result in HSP70 induction or signs of protein damage (i.e., increased ubiquitin), suggesting that TMAO levels were sufficiently protective in these tissues. However, in the gill, we observed a significant decrease in TMAO concentration and a significant induction of HSP70 as well as signs of protein damage. In the face of this cellular stress response, gill Na+/K+-ATPase (NKA) activity significantly increased during hyposmotic conditions, as expected. We suggest that this functional preservation in the gill is partly the result of HSP70 induction with lowered salinity. We conclude a reciprocal relationship between TMAO and HSP70 in the gills of dogfish as a result of in vivo hyposmotic stress. When osmotically induced protein damage surpasses the protective capacity of remaining TMAO, HSP70 is induced to preserve tissue and organismal function.

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Acknowledgments

The authors wish to thank the staff of MDIBL for their assistance and support with this project, especially Michelle Bailey and her team for their help with animal care and acquisition and Wayne Sinclair for assistance with our experimental setup. We are also grateful to Natalie Donaher for her technical expertise, Dr. Diana Hamilton for her statistical prowess, Neal Callaghan for his invaluable help with the NKA assay, and Mike Lawrence for his assistance while at MDIBL and with the urea protocol. This work was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants (SC, PAW, TJM), by a Mount Allison University Carnegie Undergraduate Scholarship (RM), and by a Minogue Medical Inc. Undergraduate Research Award (RM).

Conflict of interest

The authors hereby disclose no conflict of interest, whether financial or otherwise. All procedures performed in studies involving animals were in accordance with the ethical standards of an approved IACUC at the MDIBL.

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Authors and Affiliations

  1. Department of Biochemistry, Mount Allison University, Sackville, NB, Canada

    Robyn J. MacLellan & Tyson MacCormack

  2. Department of Biology, Mount Allison University, Sackville, NB, E4L 1G7, Canada

    Louise Tunnah & Suzanne Currie

  3. Atlantic Cancer Research Institute, Moncton, NB, Canada

    David Barnett

  4. Department of Integrative Biology, University of Guelph, Guelph, ON, Canada

    Patricia A. Wright

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  1. Robyn J. MacLellan
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  2. Louise Tunnah
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Correspondence to Suzanne Currie.

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Communicated by H. V. Carey.

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MacLellan, R.J., Tunnah, L., Barnett, D. et al. Chaperone roles for TMAO and HSP70 during hyposmotic stress in the spiny dogfish shark (Squalus acanthias). J Comp Physiol B 185, 729–740 (2015). https://doi.org/10.1007/s00360-015-0916-6

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