Abstract
This study aims to explore the effects of dietary selenium on hepatic mitochondrial quality and energy supply of grass carp (Ctenopharyngodon idella) fed with high-fat diet (HFD) after heat stress (HS). Grass carp were fed with HFD, and HFD contained 0.3 mg/kg nano-selenium for 10 weeks, thereafter exposed to HS from 26 to 34 °C, and named the HFD + HS (control) group and the HFD + Se + HS group, respectively. The results show that selenium significantly prompted the growth, increased glutathione peroxidase (GPX) activity, but reduced malondialdehyde (MDA) content in the liver and the levels of aspartate aminotransferase (AST) and alanine aminotransferase (ALT) in the serum of grass carp fed with HFD after HS. Further, selenium alleviated mitochondrial damage and increased the number of mitochondrial DNA copies in the liver of the grass carp fed with HFD after HS. And selenium also maintained mitochondrial homeostasis by upregulating the expression of mitochondrial quality control-related genes (pgc-1α, nrf1/2, tfam, opa1, mfn1/2, and drp1), mitophagy-related genes (beclin1, atg5, atg12, pink1, and parkin), and the protein expression of parkin and LC3-II/I in the liver of grass carp. Finally, selenium reduced the triglyceride (TG) level and increased the free fatty acid (FFA) level and adenosine triphosphate (ATP) production in the liver of grass carp fed with HFD after HS. In conclusion, dietary selenium alleviated liver damage and improved liver mitochondrial quality and ATP production by increasing liver antioxidant capacity and promoting liver mitochondrial quality in grass carp fed with HFD after HS, which help grass carp to resist these two stressors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are not publicly available but are available from the corresponding author on reasonable request.
Code availability
Not applicable.
References
Abasubong KP, Li XF, Zhang DD, Jia ET, Xiang-Yang Y, Xu C, Liu WB (2018) Dietary supplementation of xylooligosaccharides benefits the growth performance and lipid metabolism of common carp (Cyprinus carpio) fed high-fat diets. Aquacult Nutr 24(5):1416–1424. https://doi.org/10.1111/anu.12678
Akbarian A, Michiels J, Degroote J, Majdeddin M, Golian A, De Smet S (2016) Association between heat stress and oxidative stress in poultry; mitochondrial dysfunction and dietary interventions with phytochemicals. J Anim Sci Biotechnol 7(1):1–14. https://doi.org/10.1186/s40104-016-0097-5
Cao XF, Liu WB, Zheng XC, Yuan XY, Wang CC, Jiang GZ (2019) Effects of high-fat diets on growth performance, endoplasmic reticulum stress and mitochondrial damage in blunt snout bream (Megalobrama amblycephala). Aquacult Nutr 25(1):97–109. https://doi.org/10.1111/anu.12834
Cao XF, Liu WB, Ai QH, Li XS, Li JB, Fang W, Huang YY, Wang CC, Jiang GZ (2020) High-fat diet-induced inflammation aggravates hepatic steatosis of blunt snout bream (Megalobrama amblycephala) through the transcription regulation of fatty acid synthesis and oxidation. Aquacult Nutr 26(5):1493–1504. https://doi.org/10.1111/anu.13097
Cheng CH, Yang FF, Liao SA, Miao YT, Ye CX, Wang AL, Tan JW, Chen XY (2015) High temperature induces apoptosis and oxidative stress in pufferfish (Takifugu obscurus) blood cells. J Therm Biol 53:172–179. https://doi.org/10.1016/j.jtherbio.2015.08.002
Cheng CH, Guo ZX, Luo SW, Wang AL (2018) Effects of high temperature on biochemical parameters, oxidative stress, DNA damage and apoptosis of pufferfish (Takifugu obscurus). Ecotoxicol Environ Saf 150:190–198. https://doi.org/10.1016/j.ecoenv.2017.12.045
Cheng CH, Guo ZX, Ye CX, Wang AL (2018) Effect of dietary astaxanthin on the growth performance, non-specific immunity, and antioxidant capacity of pufferfish (Takifugu obscurus) under high temperature stress. Fish Physiol Biochem 44(1):209–218. https://doi.org/10.1007/s10695-017-0425-5
Civelek M, Mehrkens JF, Carstens NM, Fitzenberger E, Wenzel U (2019) Inhibition of mitophagy decreases survival of Caenorhabditis elegans by increasing protein aggregation. Mol Cell Biochem 452(1):123–131. https://doi.org/10.1007/s11010-018-3418-5
Cline SD (2012) Mitochondrial DNA damage and its consequences for mitochondrial gene expression. Biochim Biophys Acta Gene Regul Mech 1819(9–10):979–991. https://doi.org/10.1016/j.bbagrm.2012.06.002
Cui YT, Liu B, Xie J, Xu P, Habte-Tsion HM, Zhang YY (2014) Effect of heat stress and recovery on viability, oxidative damage, and heat shock protein expression in hepatic cells of grass carp (Ctenopharyngodon idellus). Fish Physiol Biochem 40(3):721–729. https://doi.org/10.1007/s10695-013-9879-2
Dai YJ, Cao XF, Zhang DD, Li XF, Liu WB, Jiang GZ (2019) Chronic inflammation is a key to inducing liver injury in blunt snout bream (Megalobrama amblycephala) fed with high-fat diet. Dev Comp Immunol 97:28–37. https://doi.org/10.1016/j.dci.2019.03.009
Dong YZ, Xia T, Lin JB, Wang L, Song K, Zhang CX (2021) Quercetin attenuates high-fat diet-induced excessive fat deposition of spotted seabass (Lateolabrax maculatus) through the regulatory for mitochondria and endoplasmic reticulum. Front Mar Sci. https://doi.org/10.3389/fmars.2021.746811
FAO (2022) The State of World Fisheries and Aquaculture 2022 - Towards Blue Transformation. FAO Rome. https://doi.org/10.4060/cc0461en
Feng WR, Liu SF, Zhuang ZM, Ma Q, Su YQ, Tang QS (2014) Optimization of quantitative PCR-based measurement of mitochondrial DNA content in different tissues of Cynoglossus semilaevis. J Fish Sci China 21(5):920–928. https://doi.org/10.3724/SP.J.1118.2014.00920
Forgati M, Kandalski PK, Herrerias T, Zaleski T, Machado C, Souza MRDP, Donatti L (2017) Effects of heat stress on the renal and branchial carbohydrate metabolism and antioxidant system of Antarctic fish. J Comp Physiol B 187(8):1137–1154. https://doi.org/10.1007/s00360-017-1088-3
Habibian M, Ghazi S, Moeini MM, Abdolmohammadi A (2014) Effects of dietary selenium and vitamin E on immune response and biological blood parameters of broilers reared under thermoneutral or heat stress conditions. Int J Biometeorol 58(5):741–752. https://doi.org/10.1007/s00484-013-0654-y
He SJ, Zhao SJ, Dai SF, Liu DY, Bokhari SG (2015) Effects of dietary betaine on growth performance, fat deposition and serum lipids in broilers subjected to chronic heat stress. Anim Sci J 86(10):897–903. https://doi.org/10.1111/asj.12372
Huang DY, Ren MC, Liang HL, Ge XP, Xu H, Wu LH (2022) Transcriptome analysis of the effect of high-temperature on nutrient metabolism in juvenile grass carp (Ctenopharyngodon idellus). Gene 809:146035. https://doi.org/10.1016/j.gene.2021.146035
Jia R, Cao LP, Du JL, He Q, Gu ZY, Jeney G, Xu P, Yin GJ (2020) Effects of high-fat diet on antioxidative status, apoptosis and inflammation in liver of tilapia (Oreochromis niloticus) via Nrf2, TLRs and JNK pathways. Fish Shellfish Immunol 104:391–401. https://doi.org/10.1016/j.fsi.2020.06.025
Kursvietiene L, Mongirdiene A, Bernatoniene J, Sulinskiene J, Staneviciene I (2020) Selenium anticancer properties and impact on cellular redox status. Antioxidants 9(1):80. https://doi.org/10.3390/antiox9010080
Li XF, Jiang YY, Liu WB, Ge XP (2012) Protein-sparing effect of dietary lipid in practical diets for blunt snout bream (Megalobrama amblycephala) fingerlings: effects on digestive and metabolic responses. Fish Physiol Biochem 38(2):529–541. https://doi.org/10.1007/s10695-011-9533-9
Li YH, Wei L, Cao JR, Qiu LG, Jiang X, Li P, Song QQ, Zhou HL, Han Q, Diao XP (2016) Oxidative stress, DNA damage and antioxidant enzyme activities in the pacific white shrimp (Litopenaeus vannarnei) when exposed to hypoxia and reoxygenation. Chemosphere 144:234–240. https://doi.org/10.1016/j.chemosphere.2015.08.051
Li LY, Li JM, Qiao F, Chen LQ, Zhang ML, Du ZY (2020a) Inhibited carnitine synthesis impairs adaptation to high-fat diet in Nile tilapia (Oreochromis niloticus). Aquac Rep 16:100249. https://doi.org/10.1016/j.aqrep.2019.100249
Li RB, Toan S, Zhou H (2020b) Role of mitochondrial quality control in the pathogenesis of nonalcoholic fatty liver disease. Aging 12(7):6467–6485. https://doi.org/10.18632/aging.102972
Li LL, Liu Z, Quan JQ, Lu JH, Zhao GY, Sun J (2022) Metabonomics analysis reveals the protective effect of nano-selenium against heat stress of rainbow trout (Oncorhynchus mykiss). J Proteomics 259:104545. https://doi.org/10.1016/j.jprot.2022.104545
Liang HL, Ge XP, Xia D, Ren MC, Mi HF, Pan LK (2022) The role of dietary chromium supplementation in relieving heat stress of juvenile blunt snout bream (Megalobrama amblycephala). Fish Shellfish Immunol 120:23–30. https://doi.org/10.1016/j.fsi.2021.11.012
Liu GH, Yu HB, Wang C, Li PJ, Liu S, Zhang XT, Zhang C, Qi M, Ji H (2021) Nano-selenium supplements in high-fat diets relieve hepatopancreas injury and improve survival of grass carp (Ctenopharyngodon Idella) by reducing lipid deposition. Aquaculture 538:736580. https://doi.org/10.1016/j.aquaculture.2021.736580
Liu S, Yu HB, Li PJ, Wang C, Liu GH, Zhang XT, Zhang C, Qi M, Ji H (2022) Dietary nano-selenium alleviated intestinal damage of juvenile grass carp (Ctenopharyngodon idella) induced by high-fat diet: insight from intestinal morphology, tight junction, inflammation, anti-oxidization and intestinal microbiota. Anim Nutr 8:235–248. https://doi.org/10.1016/j.aninu.2021.07.001
Lu KL, Xu WN, Li JY, Li XF, Huang GQ, Liu WB (2013) Alterations of liver histology and blood biochemistry in blunt snout bream (Megalobrama amblycephala) fed high-fat diets. Fish Sci 79(4):661–671. https://doi.org/10.1007/s12562-013-0635-4
Lu KL, Xu WN, Wang LN, Zhang DD, Zhang CN, Liu WB (2014) Hepatic beta-oxidation and regulation of carnitine palmitoyltransferase (CPT) I in blunt snout bream (Megalobrama amblycephala) fed a high-fat diet. PLoS One 9(3):e93135. https://doi.org/10.1371/journal.pone.0093135
Ma YM, Ibeanu G, Wang LY, Zhang JZ, Chang Y, Dong JD, Li PA, Jing L (2017) Selenium suppresses glutamate-induced cell death and prevents mitochondrial morphological dynamic alterations in hippocampal HT22 neuronal cells. BMC Neurosci 18(1):1–14. https://doi.org/10.1186/s12868-017-0337-4
Ma Q, Li LY, Le JY, Lu DL, Qiao F, Zhang ML, Du ZY, Li DL (2018) Dietary microencapsulated oil improves immune function and intestinal health in Nile tilapia fed with high-fat diet. Aquaculture 496:19–29. https://doi.org/10.1016/j.aquaculture.2018.06.080
Mahanty A, Mohanty S, Mohanty BP (2017) Dietary supplementation of curcumin augments heat stress tolerance through upregulation of nrf-2-mediated antioxidative enzymes and hsps in Puntius sophore. Fish Physiol Biochem 43(4):1131–1141. https://doi.org/10.1007/s10695-017-0358-z
Malyar RM, Li H, Liu DD, Abdulrahim Y, Farid RA, Gan F, Ali W, Enayatullah H, Banuree SAH, Huang KH, Chen XX (2020) Selenium/zinc-enriched probiotics improve serum enzyme activity, antioxidant ability, inflammatory factors and related gene expression of Wistar rats inflated under heat stress. Life Sci 248:117464. https://doi.org/10.1016/j.lfs.2020.117464
Manoli I, Alesci S, Blackman MR, Su YA, Rennert OM, Chrousos GP (2007) Mitochondria as key components of the stress response. Trends Endocrinol Metab 18(5):190–198. https://doi.org/10.1016/j.tem.2007.04.004
Mehta SL, Kumari S, Mendelev N, Li PA (2012) Selenium preserves mitochondrial function, stimulates mitochondrial biogenesis, and reduces infarct volume after focal cerebral ischemia. BMC Neurosci 13(1):1–12. https://doi.org/10.1186/1471-2202-13-79
Ming JH, Xie J, Xu P, Ge XP, Liu WB, Ye JY (2012) Effects of emodin and vitamin C on growth performance, biochemical parameters and two hsp70s mRNA expression of Wuchang bream (Megalobrama amblycephala Yih) under high temperature stress. Fish Shellfish Immunol 32(5):651–661. https://doi.org/10.1016/j.fsi.2012.01.008
Nasar MF, Shah SZH, Aftab K, Fatima M, Bilal M, Hussain M (2021) Dietary vitamin C requirement of juvenile grass carp (Ctenopharyngodon idella) and its effects on growth attributes, organ indices, whole-body composition and biochemical parameters. Aquacult Nutr 27(6):1903–1911. https://doi.org/10.1111/anu.13327
Ni HM, Williams JA, Ding WX (2015) Mitochondrial dynamics and mitochondrial quality control. Redox Biol 4:6–13. https://doi.org/10.1016/j.redox.2014.11.006
Pant R, Sharma N, Kabeer SW, Sharma S, Tikoo K (2022) Selenium-enriched probiotic alleviates western diet-induced non-alcoholic fatty liver disease in rats via modulation of autophagy through AMPK/SIRT-1 pathway. Biol Trace Elem Res. https://doi.org/10.1007/s12011-022-03247-x
Qiao L, Guo Z, Liu H, Liu J, Lin X, Deng H, Liu X, Zhao Y, Xiao X, Lei J, Han J (2022) Protective effect of mitophagy regulated by mTOR signaling pathway in liver fibrosis associated with selenium. Nutrients 14(12):2410. https://doi.org/10.3390/nu14122410
Qiu J, Wang WN, Wang LJ, Liu YF, Wang AL (2011) Oxidative stress, DNA damage and osmolality in the pacific white shrimp, Litopenaeus vannamei exposed to acute low temperature stress. Comp Biochem Physiol C 154(1):36–41. https://doi.org/10.1016/j.cbpc.2011.02.007
Rhoads RP, Baumgard LH, Suagee JK, Sanders SR (2013) Nutritional interventions to alleviate the negative consequences of heat stress. Adv Nutr 4(3):267–276. https://doi.org/10.3945/an.112.003376
Rub C, Wilkening A, Voos W (2017) Mitochondrial quality control by the Pink1/Parkin system. Cell Tissue Res 367(1):111–123. https://doi.org/10.1007/s00441-016-2485-8
Sarkar B, Bhattacharjee S, Daware A, Tribedi P, Krishnani KK, Minhas PS (2015) Selenium nanoparticles for stress-resilient fish and livestock. Nanoscale Res Lett 10(1):1–14. https://doi.org/10.1186/s11671-015-1073-2
Sedlackova L, Korolchuk VI (2019) Mitochondrial quality control as a key determinant of cell survival. Biochim Biophys Acta Mol Cell Res 1866(4):575–587. https://doi.org/10.1016/j.bbamcr.2018.12.012
Serano M, Paolini C, Michelucci A, Pietrangelo L, Guarnier FA, Protasi F (2022) High-fat diet impairs muscle function and increases the risk of environmental heatstroke in mice. Int J Mol Sci 23(9):5286. https://doi.org/10.3390/ijms23095286
Simoes ICM, Fontes A, Pinton P, Zischka H, Wieckowski MR (2018) Mitochondria in non-alcoholic fatty liver disease. Int J Biochem Cell Biol 95:93–99. https://doi.org/10.1016/j.biocel.2017.12.019
Stotland A, Gottlieb RA (2015) Mitochondrial quality control: easy come, easy go. Biochim Biophys Acta Mol Cell Res 1853(10):2802–2811. https://doi.org/10.1016/j.bbamcr.2014.12.041
Sun J, Liu Z, Quan JQ, Li LL, Zhao GY, Lu JH (2022) Protective effects of different concentrations of selenium nanoparticles on rainbow trout (Oncorhynchus mykiss) primary hepatocytes under heat stress. Ecotoxicol Environ Saf 230:113121. https://doi.org/10.1016/j.ecoenv.2021.113121
Venditti P, Di Meo S (2020) The role of reactive oxygen species in the life cycle of the mitochondrion. Int J Mol Sci 21(6):2173. https://doi.org/10.3390/ijms21062173
Vial G, Dubouchaud H, Couturier K, Cottet-Rousselle C, Taleux N, Athias A, Galinier A, Casteilla L, Leverve XM (2011) Effects of a high-fat diet on energy metabolism and ROS production in rat liver. J Hepatol 54(2):348–356. https://doi.org/10.1016/j.jhep.2010.06.044
Wang XD, Shen ZH, Wang CL, Li EC, Qin JG, Chen LQ (2019a) Dietary supplementation of selenium yeast enhances the antioxidant capacity and immune response of juvenile Eriocheir Sinensis under nitrite stress. Fish Shellfish Immunol 87:22–31. https://doi.org/10.1016/j.fsi.2018.12.076
Wang YF, Li CJ, Pan CL, Liu EG, Zhao XQ, Ling QF (2019b) Alterations to transcriptomic profile, histopathology, and oxidative stress in liver of pikeperch (Sander lucioperca) under heat stress. Fish Shellfish Immunol 95:659–669. https://doi.org/10.1016/j.fsi.2019.11.014
Wang Y, Liu BB, Wu PX, Chu Y, Gui SS, Zheng YZ, Chen XD (2022) Dietary selenium alleviated mouse liver oxidative stress and NAFLD induced by obesity by regulating the KEAP1/NRF2 pathway. Antioxidants 11(2):349. https://doi.org/10.3390/antiox11020349
Wei CC, Luo Z, Hogstrand C, Xu YH, Wu LX, Chen GH, Pan YX, Song YF (2018) Zinc reduces hepatic lipid deposition and activates lipophagy via Zn2+/MTF-1/PPARα and Ca2+/CaMKKβ/AMPK pathways. Faseb J 32(12):6666–6680. https://doi.org/10.1096/fj.201800463
Willis JR, Hickey AJR, Devaux JBL (2021) Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress. Sci Rep 11(1):1–10. https://doi.org/10.1038/s41598-021-90575-y
Wu CX, Zhao FY, Zhang Y, Zhu YJ, Ma MS, Mao HL, Hu CY (2012) Overexpression of hsp90 from grass carp (Ctenopharyngodon idella) increases thermal protection against heat stress. Fish Shellfish Immunol 33(1):42–47. https://doi.org/10.1016/j.fsi.2012.03.033
Xiao PZ, Ji H, Ye YT, Zhang BT, Chen YS, Tian JJ, Liu P, Chen LQ, Du ZY (2017) Dietary silymarin supplementation promotes growth performance and improves lipid metabolism and health status in grass carp (Ctenopharyngodon idellus) fed diets with elevated lipid levels. Fish Physiol Biochem 43(1):245–263. https://doi.org/10.1007/s10695-016-0283-6
Xie SW, Yin P, Tian LX, Yu YY, Liu YJ, Niu J (2020) Dietary supplementation of astaxanthin improved the growth performance, antioxidant ability and immune response of juvenile largemouth bass (Micropterus salmoides) fed high-fat diet. Mar Drugs 18(12):642. https://doi.org/10.3390/md18120642
Xu DN, Li WY, Li BX, Tian YB, Huang YM (2017) The effect of selenium and polysaccharide of Atractylodes macrocephala Koidz. (PAMK) on endoplasmic reticulum stress and apoptosis in chicken spleen induced by heat stress. Rsc Adv 7(13):7519–7525. https://doi.org/10.1039/c6ra27730f
Yu T, Dohl J, Chen Y, Gasier HG, Deuster PA (2019) Astaxanthin but not quercetin preserves mitochondrial integrity and function, ameliorates oxidative stress, and reduces heat-induced skeletal muscle injury. J Cell Physiol 234(8):13292–13302. https://doi.org/10.1002/jcp.28006
Yu HB, Zhang C, Zhang XT, Wang C, Li PJ, Liu GH, Yan XF, Xiong XF, Zhang L, Hou JY, Liu S, Zhou JS, Ji H (2020) Dietary nano-selenium enhances antioxidant capacity and hypoxia tolerance of grass carp (Ctenopharyngodon idella) fed with high-fat diet. Aquac Nutr 26(2):545–557. https://doi.org/10.1111/anu.13016
Zhang JF, Hu ZP, Lu CH, Yang MX, Zhang LL, Wang T (2015) Dietary curcumin supplementation protects against heat-stress-impaired growth performance of broilers possibly through a mitochondrial pathway. J Anim Sci 93(4):1656–1665. https://doi.org/10.2527/jas.2014-8244
Zhang SQ, Xu JL, He ZS, Xue F, Jiang TB, Xu MZ (2019) Sodium selenate ameliorates cardiac injury developed from high-fat diet in mice through regulation of autophagy activity. Sci Rep 9(1):1–13. https://doi.org/10.1038/s41598-019-54985-3
Zhou WH, Rahimnejad S, Lu KL, Wang LN, Liu WB (2019) Effects of berberine on growth, liver histology, and expression of lipid-related genes in blunt snout bream (Megalobrama amblycephala) fed high-fat diets. Fish Physiol Biochem 45(1):83–91. https://doi.org/10.1007/s10695-018-0536-7
Funding
This work was supported by the National Key Research and Development Program of China (Project No. 2019YFD0901002), the Northwest A&F University Young Talent Training Program (2452018030), and the National Natural Science Foundation of China (31602180).
Author information
Authors and Affiliations
Contributions
Xiaotian Zhang, methodology, investigation, data curation, writing original draft, formal analysis; Haibo Yu, conceptualization, methodology, resources, supervision, project administration, funding acquisition, writing—review and editing; Xianfang Yan, methodology, investigation, and data curation; Pengju Li, methodology, investigation, and data curation; Chi Wang, investigation; Cheng Zhang, investigation; Hong Ji, resources; Qinfeng Gao, resources; Shuanglin Dong, resources.
Corresponding author
Ethics declarations
Ethics approval
The experiment procedures were conducted in compliance with the Guidelines for Animal Research which was approved by the Animal Care Committee of Northwest A&F University, Yangling, China (Permit number: DKXT20210308).
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, X., Yu, H., Yan, X. et al. Selenium improved mitochondrial quality and energy supply in the liver of high-fat diet-fed grass carp (Ctenopharyngodon idella) after heat stress. Fish Physiol Biochem 48, 1701–1716 (2022). https://doi.org/10.1007/s10695-022-01140-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-022-01140-x