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Enhancing resistance and cell survival in Acipenser ruthenus liver, gill, and kidney cells: The potential of heat shock protein inducers against PAH-benzo[a]pyrene stress

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Abstract

The Caspian Sea has faced many environmental challenges, such as oil pollution. Heat shock proteins (HSPs) play a critical role in stress conditions and physiological changes caused by disease or injury. By evaluating the effects of various HSP inducers (HSPi), including Pro-Tex® (NOP: 800 mM), amygdalin (AMG: 80 mM), and a novel synthetic compound derived from pirano piranazole (SZ: 80 µm) on isolated cells from Sterlet Sturgeon (Acipenser ruthenus) treated with 75% IC50 PAH-benzo[a]pyrene (BaP; B75). This study examines whether there is a correlation between exposure to the BaP pollutant and HSPs in fish. In vitro, after culturing cells from the liver, kidney, and gills, they were treated with HSPi compounds in the presence and absence of BaP. Western blotting was used to assess HSP27, HSP70, and HSP90 expression patterns. A variety of enzyme activities were measured before (without treatment) and after treatment with HSPis and HSPi + B75, including cytochrome P450 (CYP450) activity, specific enzyme activity for acetylcholinesterase (AChE), antioxidant capacity, liver indicator enzymes, cortisol levels, and immunity parameters. When compared to the control group, cells treated with B75 showed the lowest AChE enzyme activity (p < 0.0001). CYP450 activity was highest in group B75, while HSPi caused the opposite effect (p < 0.0001). HSPi + B75 increased HSP levels and antioxidant parameters while decreasing cortisol and liver indicator enzymes (p < 0.0001). HSPi may be a powerful and reliable method for enhancing the resistance of A. ruthenus to BaP stresses before exposure. Treating cells with HSP-inducing compounds, such as NOP, AMG, and SZ, can assist them in managing stress and increase HSP (27, 70, and 90) protein expression. Furthermore, the study findings suggest that HSPis can also mitigate the adverse effects of stress, ultimately increasing cell survival and resistance.

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Acknowledgements

We express our gratitude to Dr. Mohammed Ghadamyari for helping us determine the IC50 of BaP. Additionally, we are grateful to the Shahid Beheshti Sturgeon Breeding and Rearing Center (Rasht, Iran) for providing fish.

Funding

This work was supported by the Iranian National Science Foundation (INSF, Grant No. 97015418) and the University of Guilan. Furthermore, funds from the Caspian Sea Water Basin Research Institute grant have been utilized (Grant No. 961113100001).

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Authors and Affiliations

  1. Department of Biology, Faculty of Science, University of Guilan, Rasht, Iran

    Sevda Zarei, Hossein Ghafouri, Leila Vahdatiraad & Behrooz Heidari

  2. Department of Marine Sciences, the Caspian Sea Basin Research Center, University of Guilan, Rasht, Iran

    Hossein Ghafouri & Behrooz Heidari

  3. International Sturgeon Research Institute, Agricultural Research Education and Organization (AREEO), Iranian Fisheries Sciences Research Institute, Tehran, Iran

    Tooraj Sohrabi

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  1. Sevda Zarei
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  2. Hossein Ghafouri
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Contributions

Sevda Zarei: Performing the experiments, Writing – original draft, Statistical Analysis. Hossein Ghafouri: Conceptualization, supervision, methodology, writing – review & editing. Leila Vahadatiraad: Performing the experiments. Behrooz Heidari: Methodology, Advisor, Writing – review & editing. Tooraj Sohrabi: Providing the sample and advice on fish physiology.

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Correspondence to Hossein Ghafouri.

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Highlights

• The role of HSPs in the immune system and antioxidant systems is vital.

• Sterlet sturgeon cells were treated with HSP inducers with and without BaP.

• In response to HSPi and BaP, a significant increase in HSPs expression was observed.

• HSPi can modulate the antioxidant, liver indicator enzymes, AChE, and cytochrome P450 activities of Acipenser ruthenus against BaP.

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Zarei, S., Ghafouri, H., Vahdatiraad, L. et al. Enhancing resistance and cell survival in Acipenser ruthenus liver, gill, and kidney cells: The potential of heat shock protein inducers against PAH-benzo[a]pyrene stress. Environ Sci Pollut Res 31, 9445–9460 (2024). https://doi.org/10.1007/s11356-024-31884-3

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