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Trehalose prevents glyphosate-induced hepatic steatosis in roosters by activating the Nrf2 pathway and inhibiting NLRP3 inflammasome activation

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Abstract

Glyphosate (Gly) is a globally spread herbicide that can cause toxic injuries to hepatocytes. Dietary trehalose (Tre) exerts cytoprotective effect in numerous liver diseases through anti-oxidant and anti-inflammatory properties. However, it is yet to be investigated whether Tre affords protection against Gly-induced hepatotoxicity. To evaluate the negative effect of Gly in liver and assess the possible protective role of Tre, sixty Hy-line Brown roosters were allocated into three groups: the first group presented the control with a normal diet, the second group fed normal feed containing 200mg/kg Gly, and the third group fed normal feed containing 200 mg/kg Gly and 5 g/kg Tre. Plasma and liver tissues were collected and analyzed after 120 days. Firstly, Gly-elevated serum levels of hepatic injury markers and liver histopathological damages were evidently alleviated by Tre administration. Also, Tre normalized Gly-altered serum and hepatic lipid profiles and Oil Red O-stained lipid levels, suggesting the improvement of hepatic steatosis. The severely accumulated malondialdehyde levels and impaired antioxidant status in Gly-exposed roosters were markedly improved by administration with Tre. Simultaneously, Gly-inhibited nuclear factor erythroid 2-related factor 2 (Nrf2) level and consequent reduced levels of Nrf2-downstream targets in liver were markedly normalized by Tre treatment. Additionally, Tre treatment evidently mitigated Gly-induced inflammasome response via inhibiting NLRP3 inflammasome activation. Overall, these observations provide novel insights that the protective action of Tre against Gly-induced hepatic steatosis is attributed to activation of Nrf2 pathway and inhibition of NLRP3 inflammasome activation.

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Data availability

Data and materials are available upon request.

Abbreviations

Gly:

Glyphosate

Tre:

Trehalose

EFSA:

European Food Safety Authority

NOAEL:

No Adverse Effects Level

SDS-PAGE:

Sodium dodecyl sulfate polyacrylamide gel electrophoresis

PVDF:

Polyvinylidene fluoride

NLRP3:

NOD-like receptor thermal protein domain associated protein 3

IL-1β:

Interleukin-1β;

Nrf2:

Nuclear factor erythriod2-related factor2

Keap1:

Kelch-like ECH associated protein-1

NQO1, NADPH:

quinone oxidoreductase

HO-1:

Hemoxygenase 1

TC:

Total cholesterol

TG:

Triacylglycerol

LDL-C:

Low-density lipoprotein cholesterol

HDL-C:

High-density lipoprotein cholesterol

AST:

Aspartate aminotransferase

ALT:

Alanine aminotransferase

γ-GT:

γ-glutamyltransferase

ALP:

Alkaline phosphatase

MDA:

Malondialdehyde

T-AOC:

Total antioxidant capacity

GSH-Px:

Glutathione peroxidase

SOD:

Superoxide dismutase

CAT:

Catalase

ROS:

Reactive oxygen species

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Acknowledgements

We would like to thank Professor Rui-Feng Fan his professional advice.

Funding

This work was supported by grants from the National Natural Science Foundation of China (32172920, 31873030, 32072927), Shandong Provincial Natural Science Foundation of China (no. ZR2019MC068), Youth Innovation and Technology Program in Colleges and Universities of Shandong Province (no. 2020KJF009) and project of Shandong province higher educational science and technology program (no. J18KA119).

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Authors and Affiliations

  1. College of Animal Science and Veterinary Medicine, Shandong Agricultural University, 61 Daizong Street, Tai’an City, 271018, Shandong Province, China

    Cai-Yu Lian, Run-Zhou Wang, Jie Wang, Zhen-Yong Wang & Lin Wang

  2. Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural University, 61 Daizong Street, Tai’an City, 271018, Shandong Province, China

    Cai-Yu Lian, Run-Zhou Wang, Jie Wang, Zhen-Yong Wang & Lin Wang

  3. Shandong Provincial Engineering Technology Research Center of Animal Disease Control and Prevention, Shandong Agricultural University, 61 Daizong Street, Tai’an City, 271018, Shandong Province, China

    Cai-Yu Lian, Run-Zhou Wang, Jie Wang, Zhen-Yong Wang & Lin Wang

  4. Yantai Academy of Agricultural Sciences, Yan’tai City, 265500, Shandong Province, China

    Wei Zhang

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  1. Cai-Yu Lian
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  2. Run-Zhou Wang
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Contributions

Cai-Yu Lian, and Run-Zhou Wang: Conceptualization, Methodology, Data curation, Writing-Original draft preparation. Jie Wang, Zhen-Yong Wang and Wei Zhang: Writing-review and editing. Lin Wang: Writing-Reviewing and Editing, Project administration, Funding acquisition. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Wei Zhang or Lin Wang.

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All animal experimental protocols were in accordance with the animal welfare and accredited by the Ethic Animal Care Committee of Shandong Agricultural University (NO: SDAUA-2021-038).

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Lian, CY., Wang, RZ., Wang, J. et al. Trehalose prevents glyphosate-induced hepatic steatosis in roosters by activating the Nrf2 pathway and inhibiting NLRP3 inflammasome activation. Vet Res Commun 47, 651–661 (2023). https://doi.org/10.1007/s11259-022-10021-w

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