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Involvement of the heat shock response (HSR) regulatory pathway in cadmium-elicited cerebral damage

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Abstract

The heat shock response (HSR) is a cellular protective mechanism that is characterized by the induction of heat shock transcription factors (HSFs) and heat shock proteins (HSPs) in response to diverse cellular and environmental stressors, including cadmium (Cd). However, little is known about the relationship between the damaging effects of Cd and the HSR pathway in the chicken cerebrum following Cd exposure. To explore whether Cd exposure elicits cerebral damage and triggers the HSR pathway, chicks were exposed to Cd in the daily diet at different concentrations (35, 70, or 140 mg/kg feed) for 90 days, while a control group was fed the standard diet without Cd. Histopathological examination of cerebral tissue from Cd-exposed chickens showed neuronal damage, as evidenced by swelling and degeneration of neurons, loss of neurons, and capillary damage. Cd exposure significantly increased mRNA expression of HSF1, HSF2, and HSF3, and mRNA and protein expression of three major stress-inducible HSPs (HSP60, HSP70, and HSP90). Moreover, Cd exposure differentially modulated mRNA expression of small HSP (sHSPs), most notably reducing expression of HSP27 (HSPB1). Furthermore, Cd exposure increased TUNEL-positive neuronal apoptotic cells and up-regulated protein expression of caspase-1, caspase-8, caspase-3, and p53, leading to apoptosis. Taken together, these data demonstrate that activation of the HSR and apoptotic pathways by Cd exposure is involved in Cd-elicited cerebral damage in the chicken.

Graphical Abstract

Synopsis for the graphical abstract

Cadmium (Cd)-induced neuronal damage triggers the heat shock response (HSR) by activating heat shock transcription factors (HSFs) and subsequent induction of major heat shock proteins (notably, HSP60, HSP70, and HSP90). Moreover, Cd exposure activates caspase-1, caspase-8, caspase-3, and p53 protein, thereby resulting in neuronal apoptosis in the chicken brain.

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Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Funding

This study was supported by the National Natural Science Foundation of China (No. 32172932), the Key Program of the Natural Science Foundation of Heilongjiang Province of China (No. ZD2021C003), the China Agriculture Research System of MOF and MARA (No. CARS-35), Distinguished Professor of the Longjiang Scholars Support Project (No. T201908), and the Heilongjiang Touyan Innovation Team Program.

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Authors and Affiliations

  1. College of Veterinary Medicine, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Milton Talukder, Shao-Shuai Bi, Mei-Wei Lv, Jing Ge, Cong Zhang & Jin-Long Li

  2. Department of Physiology and Pharmacology, Faculty of Animal Science and Veterinary Medicine, Patuakhali Science and Technology University, Barishal, 8210, Bangladesh

    Milton Talukder

  3. College of Biological and Pharmaceutical Engineering, West Anhui University, Luan, 237012, People’s Republic of China

    Shao-Shuai Bi

  4. College of Veterinary Medicine, Henan Agricultural University, 450046, Zhengzhou, Henan, People’s Republic of China

    Cong Zhang

  5. Key Laboratory of the Provincial Education, Department of Heilongjiang for Common Animal Disease Prevention and Treatment, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Jin-Long Li

  6. Heilongjiang Key Laboratory for Laboratory Animals and Comparative Medicine, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Jin-Long Li

Authors
  1. Milton Talukder
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  2. Shao-Shuai Bi
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  3. Mei-Wei Lv
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  4. Jing Ge
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  5. Cong Zhang
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  6. Jin-Long Li
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Contributions

Milton Talukder: conceptualization, methodology, investigation, formal analysis, writing—original draft, writing—review and editing. Shao-Shuai Bi: methodology, formal analysis, writing—review and editing. Mei-Wei Lv: investigation, formal analysis. Jing Ge: formal analysis, writing—review and editing. Cong Zhang: writing—review and editing. Jin-Long Li: conceptualization, funding acquisition, supervision, writing—review and editing.

Corresponding author

Correspondence to Jin-Long Li.

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Animal experiments were performed in accordance with the guidelines for the care and use of laboratory animals and were approved by the Animal Care and Use Committee of Northeast Agricultural University, China (approval number: NEAUEC20190314).

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All authors have approved the final version of the manuscript for publication.

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The authors declare no competing interests.

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Responsible Editor: Mohamed M. Abdel-Daim

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Talukder, M., Bi, SS., Lv, MW. et al. Involvement of the heat shock response (HSR) regulatory pathway in cadmium-elicited cerebral damage. Environ Sci Pollut Res 30, 106648–106659 (2023). https://doi.org/10.1007/s11356-023-29880-0

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