Hostname: page-component-848d4c4894-wzw2p Total loading time: 0 Render date: 2024-05-27T11:51:37.463Z Has data issue: false hasContentIssue false

Dietary nano-Se supplementation regulates lipid deposition, protein synthesis and muscle fibre formation in grass carp fed with high-fat diet

Published online by Cambridge University Press:  31 March 2023

Sha Liu
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling 712100, People’s Republic of China
Haibo Yu*
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling 712100, People’s Republic of China
Lingwei Zhu
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling 712100, People’s Republic of China
Xiaotian Zhang
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling 712100, People’s Republic of China
Pengju Li
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling 712100, People’s Republic of China
Chi Wang
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling 712100, People’s Republic of China
Guohao Liu
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling 712100, People’s Republic of China
Pan He
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling 712100, People’s Republic of China
Cheng Zhang
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling 712100, People’s Republic of China
Hong Ji
Affiliation:
College of Animal Science and Technology, Northwest A&F University, Yangling 712100, People’s Republic of China
*
*Corresponding author: Haibo Yu, email yuhaiboper@nwsuaf.edu.cn

Abstract

The current study aims to confirm the positive effects of dietary nano-Se on nutrients deposition and muscle fibre formation in grass carp fed with high-fat diet (HFD) before overwintering and to reveal its possible molecular mechanism. The lipid deposition, protein synthesis and muscle fibre formation in grass carp fed with regular diet (RD), HFD or HFD supplemented with nano-Se (0·3 or 0·6 mg/kg) for 60 d were tested. Results show that nano-Se significantly reduced lipid content, dripping loss and fibre diameter (P < 0·05), but increased protein content, post-mortem pH24 h and muscle fibre density (P < 0·05) in muscle of grass carp fed with HFD. Notably, dietary nano-Se decreased lipid deposition in the muscle by regulating amp-activated protein kinase activity and increased protein synthesis and fibre formation in muscle by activating target of rapamycin and myogenic determining factors pathways. In summary, dietary nano-Se can regulate the nutrients deposition and muscle fibre formation in grass carp fed with HFD, which exhibit potential benefit for improving flesh quality of grass carp fed with HFD.

Type
Research Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Han, F, Huang, X & Mahunu, GK (2016) Exploratory review on safety of edible raw fish per the hazard factors and their detection methods. Trends Food Sci Technol 59, 3748.10.1016/j.tifs.2016.11.004CrossRefGoogle Scholar
Lv, HB, Ma, YY, Hu, CT, et al. (2021) The individual and combined effects of hypoxia and high-fat diet feeding on nutrient composition and flesh quality in Nile tilapia (Oreochromis niloticus). Food Chem 343, 128479.10.1016/j.foodchem.2020.128479CrossRefGoogle ScholarPubMed
Jia, R, Cao, LP, Du, JL, et al. (2020) Effects of high-fat diet on steatosis, endoplasmic reticulum stress and autophagy in liver of tilapia (Oreochromis niloticus). Front Marine Sci 7, 363.10.3389/fmars.2020.00363CrossRefGoogle Scholar
Du, ZY, Liu, YJ, Tian, L, et al. (2005) Effect of dietary lipid level on growth, feed utilization and body composition by juvenile grass carp (Ctenopharyngodon idella). Aquacult Nutr 11, 139146.10.1111/j.1365-2095.2004.00333.xCrossRefGoogle Scholar
Tang, T, Hu, Y, Peng, M, et al. (2019) Effects of high-fat diet on growth performance, lipid accumulation and lipid metabolism-related MicroRNA/gene expression in the liver of grass carp (Ctenopharyngodon idella). Comp Biochem Physiol B Biochem Mol Biol 234, 3440.10.1016/j.cbpb.2019.04.006CrossRefGoogle ScholarPubMed
Morgan, I (2002) The influence of life-history strategy on lipid metabolism in overwintering juvenile Atlantic salmon. J Fish Biol 60, 674686.10.1111/j.1095-8649.2002.tb01693.xCrossRefGoogle Scholar
Sun, J, Wu, W & Ji, H (2021) Effect of overwintering on body composition, antioxidant enzyme activities, fatty acid composition, glucose and lipid-metabolic related gene expression of grass carp (Ctenopharyngodon idellus). Aquaculture 545, 737125.10.1016/j.aquaculture.2021.737125CrossRefGoogle Scholar
Zhang, ZY, Limbu, SM, Zhao, SH, et al. (2022) Dietary l-carnitine supplementation recovers the increased pH and hardness in fillets caused by high-fat diet in Nile tilapia (Oreochromis niloticus). Food Chem 382, 132367.10.1016/j.foodchem.2022.132367CrossRefGoogle ScholarPubMed
Yu, E, Fu, B, Wang, G, et al. (2020. Proteomic and metabolomic basis for improved textural quality in crisp grass carp (Ctenopharyngodon idellus C.et V) fed with a natural dietary pro-oxidant. Food Chem 325, 126906.10.1016/j.foodchem.2020.126906CrossRefGoogle ScholarPubMed
Jiang, WD, Chen, L, Liu, Y, et al. (2019) Impact and consequences of dietary riboflavin deficiency treatment on flesh quality loss in on-growing grass carp (Ctenopharyngodon idella). Food Funct 10, 33963409.10.1039/C8FO01943FCrossRefGoogle ScholarPubMed
Ma, XZ, Feng, L, Wu, P, et al. (2020) Enhancement of flavor and healthcare substances, mouthfeel parameters and collagen synthesis in the muscle of on-growing grass carp (Ctenopharyngodon idella) fed with graded levels of glutamine. Aquaculture 528, 735486.10.1016/j.aquaculture.2020.735486CrossRefGoogle Scholar
Rayman, MP (2000) The importance of selenium to human health. Lancet 356, 233241.10.1016/S0140-6736(00)02490-9CrossRefGoogle ScholarPubMed
Zheng, L, Jiang, WD, Feng, L, et al. (2018) Selenium deficiency impaired structural integrity of the head kidney, spleen and skin in young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 82, 408420.10.1016/j.fsi.2018.08.038CrossRefGoogle ScholarPubMed
Liu, G, Yu, H, Wang, C, et al. (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, 736580.10.1016/j.aquaculture.2021.736580CrossRefGoogle Scholar
Liu, S, Yu, H, Li, P, et al. (2021) 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, 235248.10.1016/j.aninu.2021.07.001CrossRefGoogle ScholarPubMed
Wang, L, Wang, L, Zhang, D, et al. (2021) Effect of dietary selenium on postprandial protein deposition in the muscle of juvenile rainbow trout (Oncorhynchus mykiss). Br J Nutr 125, 721731.10.1017/S000711452000313XCrossRefGoogle ScholarPubMed
Saffari, S, Keyvanshokooh, S, Zakeri, M, et al. (2016) Effects of different dietary selenium sources (sodium selenite, selenomethionine and nanoselenium) on growth performance, muscle composition, blood enzymes and antioxidant status of common carp (Cyprinus carpio). Aquacult Nutr 23, 611617.10.1111/anu.12428CrossRefGoogle Scholar
Yang, MT, Li, F, Wang, YC, et al. (2014) Synthesis of selenium nanoparticles in the presence of oyster polysaccharides and the antioxidant activity. Appl Mech Mater 522, 11431146.10.4028/www.scientific.net/AMM.522-524.1143CrossRefGoogle Scholar
Horwitz, W & Latimer, GW (2007) Official Methods of Analysis of the Association of Analytical Chemists, 18th ed. Maryland: AOAC.Google Scholar
Wang, B, Liu, Y, Feng, L, et al. (2015) Effects of dietary arginine supplementation on growth performance, flesh quality, muscle antioxidant capacity and antioxidant-related signalling molecule expression in young grass carp (Ctenopharyngodon idella). Food Chem 167, 9199.10.1016/j.foodchem.2014.06.091CrossRefGoogle ScholarPubMed
Wang, L, Li, XL, Lu, KL, et al. (2021) Dietary hydroxyl methionine selenium supplementation enhances growth performance, antioxidant ability and nitrite tolerance of Litopenaeus vannamei . Aquaculture 537, 736513.10.1016/j.aquaculture.2021.736513CrossRefGoogle Scholar
Folch, J, Lees, M & Stanley, GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497509.10.1016/S0021-9258(18)64849-5CrossRefGoogle ScholarPubMed
Ye, Z, Li, R, Cao, C, et al. (2019) Fatty acid profiles of typical dietary lipids after gastrointestinal digestion and absorbtion: a combination study between in-vitro and in-vivo. Food Chem 280, 3444.10.1016/j.foodchem.2018.12.032CrossRefGoogle ScholarPubMed
Ali, S, Rajput, N, Li, C, et al. (2016) Effect of freeze-thaw cycles on lipid oxidation and myowater in broiler chickens. Braz J Poult Sci 18, 3540.10.1590/1516-635x1801035-040CrossRefGoogle Scholar
Jiang, WD, Wen, HL, Liu, Y, et al. (2016) Enhanced muscle nutrient content and flesh quality, resulting from tryptophan, is associated with anti-oxidative damage referred to the Nrf2 and TOR signalling factors in young grass carp (Ctenopharyngodon idella): avoid tryptophan deficiency or excess. Food Chem 199, 210219.10.1016/j.foodchem.2015.12.003CrossRefGoogle ScholarPubMed
Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402408.10.1006/meth.2001.1262CrossRefGoogle Scholar
Bjørnevik, M, Espe, M, Beattie, C, et al. (2010) Temporal variation in muscle fibre area, gaping, texture, colour and collagen in triploid and diploid Atlantic salmon (Salmo salar L). J Sci Food Agr 84, 530540.10.1002/jsfa.1656CrossRefGoogle Scholar
Zhao, H, Chong, J, Tang, R, et al. (2018) Metabolomics investigation of dietary effects on flesh quality in grass carp (Ctenopharyngodon idellus). GigaScience 7, giy111.10.1093/gigascience/giy111CrossRefGoogle ScholarPubMed
Yuan, X, Liang, XF, Liu, L, et al. (2016) Fat deposition pattern and mechanism in response to dietary lipid levels in grass carp, Ctenopharyngodon idellus . Fish Physiol Biochem 42, 15571569.10.1007/s10695-016-0240-4CrossRefGoogle ScholarPubMed
He, S, Guo, X, Tan, W, et al. (2016) Effect of selenium deficiency on phosphorylation of the AMPK pathway in rats. Biol Trace Elem Res 169, 254260.10.1007/s12011-015-0427-zCrossRefGoogle ScholarPubMed
Sun, J, Yang, Z, Xiao, P, et al. (2017) Two isoforms of hormone-sensitive lipase b are generated by alternative exons usage and transcriptional regulation by insulin in grass carp (Ctenopharyngodon idella). Fish Physiol Biochem 43, 539547.10.1007/s10695-016-0308-1CrossRefGoogle ScholarPubMed
Kaneko, G, Shirakami, H, Yamada, T, et al. (2016) Short-term fasting increases skeletal muscle lipid content in association with enhanced mRNA levels of lipoprotein lipase 1 in lean juvenile red seabream (Pagrus major). Aquaculture 452, 160168.10.1016/j.aquaculture.2015.10.030CrossRefGoogle Scholar
Lee, WJ, Kim, M, Park, HS, et al. (2006) AMPK activation increases fatty acid oxidation in skeletal muscle by activating PPARαand PGC-1. Biochem Biophys Res Comm 340, 291295.10.1016/j.bbrc.2005.12.011CrossRefGoogle Scholar
Zhao, Z, Barcus, M, Kim, J, et al. (2016) High dietary selenium intake alters lipid metabolism and protein synthesis in liver and muscle of pigs. J Nutr 146, 16251633.10.3945/jn.116.229955CrossRefGoogle ScholarPubMed
Li, S, Fu, Y, Pang, Y, et al. (2019) GRP94 promotes muscle differentiation by inhibiting the PI3K/AKT/mTOR signaling pathway. J Cell Physiol 234, 2121121223.10.1002/jcp.28727CrossRefGoogle ScholarPubMed
Wang, J, Jiang, H, Alhamoud, Y, et al. (2022) Integrated metabolomic and gene expression analyses to study the effects of glycerol monolaurate on flesh quality in large yellow croaker (Larimichthys crocea). Food Chem 367, 130749.10.1016/j.foodchem.2021.130749CrossRefGoogle Scholar
Fauconneau, B, Andre, S, Chmaitilly, J, et al. (1997) Control of skeletal muscle fibres and adipose cells size in the flesh of rainbow trout. J Fish Biol 50, 296314.10.1111/j.1095-8649.1997.tb01360.xCrossRefGoogle Scholar
Hurling, R, Rodell, JB & Hunt, HD (1996) Research note: fiber diameter and fish texture. J Texture Stud 27, 679685.10.1111/j.1745-4603.1996.tb01001.xCrossRefGoogle Scholar
Liang, XF, Hu, L, Dong, YC, et al. (2017) Substitution of fish meal by fermented soybean meal affects the growth performance and flesh quality of Japanese seabass (Lateolabrax japonicus). Anim Feed Sci Technol 229, 112.10.1016/j.anifeedsci.2017.03.006CrossRefGoogle Scholar
Wirth-Dzicioowska, E, Zimowska, M, Gajewska, M, et al. (2011) Differential growth of skeletal muscle in mice selected divergently over 108 generations for low and high body weight. Animal Sci Pap Rep 29, 161177.Google Scholar
Rant, W, Radzik-Rant, A, Swiatek, M, et al. (2019) The effect of aging and muscle type on the quality characteristics and lipid oxidation of lamb meat. Arch Animal Breed 62, 383391.10.5194/aab-62-383-2019CrossRefGoogle ScholarPubMed
Hultmann, L, Phu, TM, Tobiassen, T, et al. (2012) Effects of pre-slaughter stress on proteolytic enzyme activities and muscle quality of farmed Atlantic cod (Gadus morhua). Food Chem 134, 13991408.10.1016/j.foodchem.2012.03.038CrossRefGoogle ScholarPubMed
Supplementary material: File

Liu et al. supplementary material

Tables S1-S4

Download Liu et al. supplementary material(File)
File 24.8 KB