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The preferential utilization of hepatic glycogen as energy substrates in largemouth bass (Micropterus salmoides) under short-term starvation

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Abstract

To elucidate the underlying mechanism of the energy metabolism in largemouth bass (Micropterus salmoides), cultured fish (initial body weight: 77.57 ± 0.75 g) in the present study were starved for 0 h, 12 h, 24 h, 48 h, 96 h and 192 h, respectively. The proximate composition analysis showed that short-term starvation induced a significant up-regulation in crude protein proportion in hepatic of cultured fish (P < 0.05). However, short-term starvation significantly decreased the hepatosomatic index and the viscerosomatic index of cultured fish (P < 0.05). The exact hepatic glycogen content in the group starved for 92 h presented remarkable decrease (P < 0.05). Meanwhile, compared with the weight change of lipid and protein (mg) in hepatic (y = 0.0007x2 − 0.2827x + 49.402; y = 0.0013x2 − 0.5666x + 165.31), the decreasing trend of weight in glycogen (mg) was more pronounced (y = 0.0032x2 − 1.817x + 326.52), which suggested the preferential utilization of hepatic glycogen as energy substrates under short-term starvation. Gene expression analysis revealed that the starvation down-regulated the expression of insulin-like growth factor 1 and genes of TOR pathway, such as target of rapamycin (tor) and ribosomal protein S6 (s6) (P < 0.05). In addition, the starvation significantly enhanced expression of lipolysis-related genes, including hormone-sensitive lipase (hsl) and carnitine palmitoyl transferase I (cpt1), but down-regulated lipogenesis as indicated by the inhibited expression of fatty acids synthase (fas), acetyl-CoA carboxylase 1 (acc1) and acetyl-CoA carboxylase 2 (acc2) (P < 0.05). Starvation of 24 h up-regulated the expression of glycolysis genes, glucokinase (gk), phosphofructokinase liver type (pfkl) and pyruvate kinase (pk), and then their expression returned to the normal level. Meanwhile, the expression of gluconeogenesis genes, such as glucose-6-phosphatase catalytic subunit (g6pc), fructose-1,6-bisphosphatase-1 (fbp1) and phosphoenolpyruvate carboxy kinase (pepck), was significantly inhibited with the short-term starvation (P < 0.05). In conclusion, short-term starvation induced an overall decline in growth performance, but it could deplete the hepatic glycogen accumulation and mobilize glycogen for energy effectively.

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References

  • Alliot E, Djabali M, Pastoureaud A, Thebault H (1984) Changes in the biochemical composition of tissues in juvenile sea bass during forced starvation. Biochem Syst Ecol 12:209–213

    Article  CAS  Google Scholar 

  • AOAC Association of Official Analytical Chemist (2003) Official methods of analysis, 17th edn. AOAC Inc, Arlington VA

    Google Scholar 

  • Barcellos LJG, Marqueze A, Trapp M, Quevedo RM, Ferreira D (2010) The effects of fasting on cortisol, blood glucose and liver and muscle glycogen in adult jundiá Rhamdia quelen. Aquaculture 300:231–236

    Article  CAS  Google Scholar 

  • Caseras A, Metón I, Fernández F, Baanante IV (2000) Glucokinase gene expression is nutritionally regulated in liver of gilthead sea bream (Sparus aurata). Bba-Gene Struct Expr 1493:135–141

    Article  CAS  Google Scholar 

  • Caseras A, Metón I, Vives C, Egea M, Fernández F, Baanante AI (2002) Nutritional regulation of glucose-6-phosphatase gene expression in liver of the gilthead sea bream (Sparus aurata). Brit J Nutr 88:607–614

    Article  CAS  PubMed  Google Scholar 

  • Castilho BA, Shanmugam R, Silva RC, Ramesh R, Himme BM, Sattlegger E (2014) Keeping the eIF2 alpha kinase Gcn2 in check. BBA-Mol Cell Res 1843:1948–1968

    CAS  Google Scholar 

  • China Fishery Statistics Yearbook (2023) Ministry of Agriculture and Rural Affairs China Agriculture Press Beijing China

  • Black D, Love RM (1986) The sequential mobilisation and restoration of energy reserves in tissues of Atlantic cod during starvation and refeeding. J Comp Physiol B 156:469–479

    Article  CAS  Google Scholar 

  • Bradbury MW (2006) Lipid metabolism and liver inflammation. I. Hepatic fatty acid uptake: possible role in steatosis. Am J Physiol-Gastr L 290:G194–G198

    CAS  Google Scholar 

  • Bychek EA, Dobson GA, Harwood JL, Guschina IA (2005) Daphnia magna can tolerate short-term starvation without major changes in lipid metabolism. Lipids 40:599–608

    Article  CAS  PubMed  Google Scholar 

  • Chen N, Jin L, Zhou H, Qiu X (2012) Effects of dietary arginine levels and carbohydrate-to-lipid ratios on mRNA expression of growth-related hormones in largemouth bass, Micropterus salmoides. Gen Comp Endocrinol 179:121–127

    Article  CAS  PubMed  Google Scholar 

  • Collins AL, Anderson TA (1995) The regulation of endogeneous energy stores during starvation and refeeding in the somatic tissues of the golden perch. J Fish Biol 47:1004–1015

    Article  Google Scholar 

  • Coyle SD, Tidwell JH, Webster CD (2000) Response of largemouth bass Micropterus salmoides to dietary supplementation of lysine, methionine, and highly unsaturated fatty acids. J World Aquacult Soc 31:89–95

    Article  Google Scholar 

  • Davis KB, Gaylord TG (2011) Effect of fasting on body composition and responses to stress in sunshine bass. Comp Biochem Phys A 158:30–36

    Article  Google Scholar 

  • Dar SA, Srivastava PP, Varghese T, Gupta S, Gireesh-Babu P, Krishna G (2018) Effects of starvation and refeeding on expression of ghrelin and leptin gene with variations in metabolic parameters in Labeo rohita fingerlings. Aquaculture 484:219–227

    Article  CAS  Google Scholar 

  • De Pedro N, Delgado MJ, Gancedo B, Alonso-Bedate M (2003) Changes in glucose, glycogen, thyroid activity and hypothalamic catecholamines in tench by starvation and refeeding. J Comp Physiol B 173:475–481

    Article  PubMed  Google Scholar 

  • Dubois W, Callard GV (1993) Culture of intact Sertoli/germ cell units and isolated Sertoli cells from Squalus testis. II. Stimulatory effects of insulin and IGF-I on DNA synthesis in premeiotic stages. J Exp Zool 267:233–244

    Article  CAS  PubMed  Google Scholar 

  • Drew RE, Rodnick KJ, Settles M, Wacyk J, Churchill E, Powell MS, Hardy RW, Murdoch GK, Hill RA, Robison BD (2008) Effect of starvation on transcriptomes of brain and liver in adult female zebrafish (Danio rerio). Physiol Genomics 35:283–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Einen O, Waagan B, Thomassen MS (1998) Starvation prior to slaughter in Atlantic salmon (Salmo salar): I. Effects on weight loss, body shape, slaughter-and fillet-yield, proximate and fatty acid composition. Aquaculture 166:85–104

    Article  Google Scholar 

  • Folch J (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226(1):497–509

    Article  CAS  PubMed  Google Scholar 

  • Gominho-Rosa MC, Rodrigues APO, Mattioni B, de Francisco A, Moraes G, Fracalossi DM (2015) Comparison between the omnivorous jundiá catfish (Rhamdia quelen) and Nile tilapia (Oreochromis niloticus) on the utilization of dietary starch sources: digestibility, enzyme activity and starch microstructure. Aquaculture 435:92–99

    Article  CAS  Google Scholar 

  • Goodwin AE, Lochmann RT, Tieman DM, Mitchell AJ (2002) Massive hepatic necrosis and nodular regeneration in largemouth bass fed diets high in available carbohydrate. J World Aquacult Soc 33(4):466–477

    Article  Google Scholar 

  • Gong Y, Chen W, Han D, Zhu X, Yang Y, Jin J, Liu HK, Xie S (2017) Effects of food restriction on growth, body composition and gene expression related in regulation of lipid metabolism and food intake in grass carp. Aquaculture 469:28–35

    Article  CAS  Google Scholar 

  • Guo F, Cavener DR (2007) The GCN2 eIF2α kinase regulates fatty-acid homeostasis in the liver during deprivation of an essential amino acid. Cell Metab 5(2):103–114

    Article  CAS  PubMed  Google Scholar 

  • He W, Li P, Yan H, Han D (2022) Long-term fasting leads to preferential catabolism of His, Arg, and branched-chain amino acids in the dorsal muscle of gibel carp (Carassius auratus gibelio): potential preferential use of amino acids as energy substrates. Aquaculture 552:737967

    Article  CAS  Google Scholar 

  • Huang Y, Wang S, Meng X, Chen N, Li S (2021) Molecular cloning and characterization of sirtuin 1 and its potential regulation of lipid metabolism and antioxidant response in largemouth bass (Micropterus salmoides). Front Physiol 12:726877

    Article  PubMed  PubMed Central  Google Scholar 

  • Jafri AK (1995) Protein-sparing effect of dietary carbohydrate in diets for fingerling Labeo rohita. Aquaculture 136(3-4):331–339

    Article  Google Scholar 

  • Jin HO, Seo SK, Woo SH, Kim ES, Lee HC, Yoo DH, Choe TB, Hong SII, Kim JII, Park IC (2009) SP600125 negatively regulates the mammalian target of rapamycin via ATF4 - induced REDD1 expression. FEBS Lett 583(1):123–127

    Article  CAS  PubMed  Google Scholar 

  • Kimball SR, Jefferson LS (2002) Control of protein synthesis by amino acid availability. Curr Opin Clin Nutr 5(1):63–67

    Article  CAS  Google Scholar 

  • Kilberg MS, Pan YX, Chen H, Leung-Pineda V (2005) Nutritional control of gene expression: how mammalian cells respond to amino acid limitation. Annu Rev Nutr 25:59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kilberg MS, Shan J, Su N (2009) ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrinol Metab 20(9):436–443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Zhu X, Han D, Yang Y, Jin J, Xie S (2016) Carbohydrate utilization by herbivorous and omnivorous freshwater fish species: a comparative study on gibel carp (Carassius auratus gibelio var CAS III) and grass carp (Ctenopharyngodon idellus). Aquacult Res 47:128–139

    Article  CAS  Google Scholar 

  • Li S, Li J, Zhao Y, Zhang Q, Wang Q (2017) Nutrient sensing signaling integrates nutrient metabolism and intestinal immunity in grass carp, Ctenopharyngodon idellus after prolonged starvation. Fish Shellfish Immunol 71:50–57

    Article  CAS  PubMed  Google Scholar 

  • Li H, Xu W, Jin J, Yang Y, Zhu X, Han D, Liu HK, Xie S (2018) Effects of starvation on glucose and lipid metabolism in gibel carp (Carassius auratus gibelio var. CAS III). Aquaculture 496:166–175

    Article  CAS  Google Scholar 

  • Li S, Sang C, Turchini GM, Wang A, Zhang J, Chen N (2020) Starch in aquafeeds: the benefits of a high amylose to amylopectin ratio and resistant starch content in diets for the carnivorous fish, largemouth bass (Micropterus salmoides). Brit J Nutr 124(11):1145–1155

    Article  CAS  PubMed  Google Scholar 

  • Liang XF, Wang J, Gong G, Xue M, Dong YC, Wu XF, Wang X, Chen CS, Liang XF, Qin YC (2017) Gluconeogenesis during starvation and refeeding phase is affected by previous dietary carbohydrates levels and a glucose stimuli during early life in Siberian sturgeon (Acipenser baerii). Anim Nutr 3(3):284–294

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Liu N, Wang A, Chen N, Li S (2022a) Resveratrol inclusion alleviated high-dietary-carbohydrate-induced glycogen deposition and immune response of largemouth bass, Micropterus salmoides. Brit J Nutr 127(2):165–176

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Guo HY, Liu BS, Zhang N, Yang JW, Guo L, Jiang SG, Zhang DC (2022b) Starvation and refeeding influence the growth, biochemical index, intestinal microbiota, and transcriptomic profiles of golden pompano Trachinotus ovatus (Linnaeus 1758). Front Mar Sci 9:998190

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Lowery MS, Roberts SJ, Somero GN (1987) Effects of starvation on the activities and localization of glycolytic enzymes in the white muscle of the barred sand bass Paralabrax nebulifer. Physiol Zool 60(5):538–549

    Article  CAS  Google Scholar 

  • Lu DL, Ma Q, Wang J, Li LY, Han SL, Limbu SM, Li DL, Chen LQ, Zhang ML, Du ZY (2019) Fasting enhances cold resistance in fish through stimulating lipid catabolism and autophagy. J Physiol 597(6):1585–1603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo Z, Tan XY, Wang WM, Fan QX (2009) Effects of long-term starvation on body weight and body composition of juvenile channel catfish, Ictalurus punctatus, with special emphasis on amino acid and fatty acid changes. J Appl Ichthyol 25(2):184–189

    Article  CAS  Google Scholar 

  • Ma HJ, Mou MM, Pu DC, Lin SM, Chen YJ, Luo L (2019) Effect of dietary starch level on growth, metabolism enzyme and oxidative status of juvenile largemouth bass, Micropterus salmoides. Aquaculture 498:482–487

    Article  CAS  Google Scholar 

  • Machado CR, Garofaloj MAR, Roselino JES, Kettelhut IDC, Migliorini RH (1988) Effects of starvation, refeeding, and insulin on energy-linked metabolic processes in catfish (Rhamdia hilarii) adapted to a carbohydrate-rich diet. Gen Comp Endocrinol 71(3):429–437

    Article  CAS  PubMed  Google Scholar 

  • Martin SA, Douglas A, Houlihan DF, Secombes CJ (2010) Starvation alters the liver transcriptome of the innate immune response in Atlantic salmon (Salmo salar). BMC Genomics 11(1):1–20

    Article  Google Scholar 

  • Metón I, Fernández F, Baanante AI (2003) Short-and long-term effects of refeeding on key enzyme activities in glycolysis–gluconeogenesis in the liver of gilthead seabream (Sparus aurata). Aquaculture 225(1-4):99–107

    Article  Google Scholar 

  • Morata P, Vargas AM, Sanchez-Medina F, Garcia M, Cardenete G, Zamora S (1982) Evolution of gluconeogenic enzyme activities during starvation in liver and kidney of the rainbow trout (Salmo gairdneri). Comp Biochem Physiol B 71(1):65–70

    Article  CAS  PubMed  Google Scholar 

  • Morais S, Knoll-Gellida A, André M, Barthe C, Babin PJ (2007) Conserved expression of alternative splicing variants of peroxisomal acyl-CoA oxidase 1 in vertebrates and developmental and nutritional regulation in fish. Physiol Genomics 28(3):239–252

    Article  CAS  PubMed  Google Scholar 

  • Mohapatra S, Chakraborty T, Shimizu S, Urasaki S, Matsubara T, Nagahama Y, Ohta K (2015) Starvation beneficially influences the liver physiology and nutrient metabolism in Edwardsiella tarda infected red sea bream (Pagrus major). Comp Biochem Phys A 189:1–10

    Article  CAS  Google Scholar 

  • Nagai M, Ikeda S (1971) Carbohydrate metabolism in fish. I. Effects of starvation and dietary composition on the blood glucose level and the hepatopancreatic glycogen and lipid contents in carp. Bull Chem Soc Jpn 37(5):404–409

    CAS  Google Scholar 

  • Navarro I, Gutierrez J (1995) Fasting and starvation. Biochem Mol Biol Fishes 4:393–434

    Article  CAS  Google Scholar 

  • NRC (2011) Carbohydrates and fibre, in: Nutrient requirements of fish and shrimp. The National Academies Press, Washington DC, pp 135–162

    Google Scholar 

  • Pérez-Jiménez A, Guedes MJ, Morales AE, Oliva-Teles A (2007) Metabolic responses to short starvation and refeeding in Dicentrarchus labrax. Effect of dietary composition. Aquaculture 265(1-4):325–335

    Article  Google Scholar 

  • Polakof S, Panserat S, Soengas JL, Moon TW (2012) Glucose metabolism in fish: a review. J Comp Physiol B 182:1015–1045

    Article  CAS  PubMed  Google Scholar 

  • Rawles SD, Smith SB, Gatlin Iii DM (2008) Hepatic glucose utilization and lipogenesis of hybrid striped bass (Morone chrysops × Morone saxatilis) in response to dietary carbohydrate level and complexity. Aquacult Nutr 14(1):40–50

    Article  Google Scholar 

  • Reinitz G (1983) Relative effect of age, diet, and feeding rate on the body composition of young rainbow trout (Salmo gairdneri). Aquaculture 35:19–27

    Article  Google Scholar 

  • Rios FSA, Moraes G, Oba ET, Fernandes MN, Donatti L, Kalinin AL, Rantin FT (2006) Mobilization and recovery of energy stores in traíra, Hoplias malabaricus Bloch (Teleostei, Erythrinidae) during long-term starvation and after re-feeding. J Comp Physiol B 176(7):721–728

    Article  PubMed  Google Scholar 

  • Romano N, Fischer H, Rubio-Benito MM, Overtuf K, Sinha AK, Kumar V (2022) Different dietary combinations of high/low starch and fat with or without bile acid supplementation on growth, liver histopathology, gene expression and fatty acid composition of largemouth bass, Micropterus salmoides. Comp Biochem Phys A 266:111157

    Article  CAS  Google Scholar 

  • Roques S, Deborde C, Richard N, Skiba-Cassy S, Moing A, Fauconneau B (2020) Metabolomics and fish nutrition: a review in the context of sustainable feed development. Rev Aquacult 12(1):261–282

    Article  Google Scholar 

  • Salem M, Silverstein J, Rexroad CE, Yao J (2007) Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss). BMC Genomics 8(1):1–16

    Article  Google Scholar 

  • Seifter S, Dayton S, Novic B, Muntwyler E (1950) The estimation of glycogen with the anthrone reagent. Arch Biochem 25:191–200

    CAS  PubMed  Google Scholar 

  • Sheng Z, Turchini GM, Xu J, Fang Z, Chen N, Xie R, Zhang H, Li S (2022) Functional properties of protein hydrolysates on growth, digestive enzyme activities, protein metabolism, and intestinal health of larval largemouth bass (Micropterus salmoides). Front Immunol 13:913024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheng Z, Xu J, Zhang Y, Wang Z, Chen N, Li S (2023) Dietary protein hydrolysate effects on growth, digestive enzymes activity, and expression of genes related to amino acid transport and metabolism of larval snakehead (Channa argus). Aquaculture 563:738896

    Article  CAS  Google Scholar 

  • Soengas JL, Strong EF, Fuentes J, Veira JAR, Andrés MD (1996) Food deprivation and refeeding in Atlantic salmon, Salmo salar: effects on brain and liver carbohydrate and ketone bodies metabolism. Fish Physiol Biochem 15:491–511

    Article  CAS  PubMed  Google Scholar 

  • Song F, Xu D, Mai K, Zhou H, Xu W, He G (2016) Comparative study on the cellular and systemic nutrient sensing and intermediary metabolism after partial replacement of fishmeal by meat and bone meal in the diet of turbot (Scophthalmus maximus L.). PloS One 11(11):e0165708

    Article  PubMed  PubMed Central  Google Scholar 

  • Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ (2004) The IGF-1/PI3K/Akt pathway prevents short article expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14:395–403

    Article  CAS  PubMed  Google Scholar 

  • Sørensen M, Nguyen G, Storebakken T, Øverland M (2010) Starch source, screw configuration and injection of steam into the barrel affect the physical quality of extruded fish feed. Aquacult Res 41(3):419–432

    Article  Google Scholar 

  • Storebakken T, Austreng E (1987) Ration level for salmonids: II. Growth, feed intake, protein digestibility, body composition, and feed conversion in rainbow trout weighing 0.5–1.0 kg. Aquaculture 60(3-4):207–221

    Article  Google Scholar 

  • Stone DA (2003) Dietary carbohydrate utilization by fish. Rev Fish Sci 11:337–369

    Article  CAS  Google Scholar 

  • Tao J, Wang S, Qiu H, Xie R, Zhang H, Chen N, Li S (2022) Modulation of growth performance, antioxidant capacity, non-specific immunity and disease resistance in largemouth bass (Micropterus salmoides) upon compound probiotic cultures inclusion. Fish Shellfish Immunol 127:804–812

    Article  CAS  PubMed  Google Scholar 

  • Tian J, He G, Mai K, Liu C (2015) Effects of postprandial starvation on mRNA expression of endocrine-, amino acid and peptide transporter-, and metabolic enzyme-related genes in zebrafish (Danio rerio). Fish Physiol Biochem 41(3):773–787

    Article  CAS  PubMed  Google Scholar 

  • Tian J, Peng D, Wen H, Wang G, Li P, Chen J, Sun Y, Lu X, Wu F, Li Q (2020) A comparative study on protein-sparing effects among juvenile Erythroculter ilishaeformis line, Ancherythroculter nigrocauda line and their hybrid F1 fed diets with different protein to carbohydrate ratios. Aquacult Nutr 26(4):993–1006

    Article  CAS  Google Scholar 

  • Tran NT, Xiong F, Hao YT, Zhang J, Wu SG, Wang GT (2018) Starvation influences the microbiota assembly and expression of immunity-related genes in the intestine of grass carp (Ctenopharyngodon idellus). Aquaculture 489:121–129

    Article  CAS  Google Scholar 

  • Van de Pol I, Flik G, Gorissen M (2017) Comparative physiology of energy metabolism: fishing for endocrine signals in the early vertebrate pool. Front Endocrinol 8:36

    Google Scholar 

  • Wang S, Zhang Y, Xie R, Zhang N, Zhang H, Chen N, Li S (2022) Effects of dietary phospholipids on growth performance, fatty acid composition and lipid metabolism of early juvenile largemouth bass (Micropterus salmoides). Aquacult Res 53(16):5628–5637

    Article  CAS  Google Scholar 

  • Wang J, Li X, Han T, Yang Y, Jiang Y, Yang M, Xu Y, Harpaz S (2016) Effects of different dietary carbohydrate levels on growth, feed utilization and body composition of juvenile grouper Epinephelus akaara. Aquaculture 459:143–147

    Article  CAS  Google Scholar 

  • Whitney ML, Jefferson LS, Kimball SR (2009) ATF4 is necessary and sufficient for ER stress-induced upregulation of REDD1 expression. Biochem Bioph Res Co 379(2):451–455

    Article  CAS  Google Scholar 

  • Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124(3):471–484

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Chen N, Liu Z, Gou S, Yin J (2016) Effects of dietary starch sources and levels on liver histology in largemouth bass, Micropterus salmoides. J Shanghai Ocean Univ 25(1):61–70

    Google Scholar 

  • Xu W, Li H, Wu L, Jin J, Zhu X, Han D, Liu H, Yang Y, Xu X, Xie S (2020) Dietary Scenedesmus ovalternus improves disease resistance of overwintering gibel carp (Carassius gibelio) by alleviating toll-like receptor signaling activation. Fish Shellfish Immunol 97:351–358

    Article  CAS  PubMed  Google Scholar 

  • Zou JM, Zhu QS, Liang H, Lu HL, Liang XF, He S (2022) Lysine deprivation regulates npy Expression via GCN2 signaling pathway in mandarin fish (Siniperca chuatsi). Int J Mol Sci 23(12):6727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was financially supported by the “Chenguang program” supported by the Shanghai Education Development Foundation and Shanghai Municipal Education Commission (19CG56), the China Agriculture Research System of MOF and MARA (CARS-46), the National Natural Science Foundation of China (31802308) and the Shanghai talent development fund (2019097).

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  1. Research Centre of the Ministry of Agriculture and Rural Affairs on Environmental Ecology and Fish Nutrition, Shanghai Ocean University, Shanghai, 20136, China

    Nihe Zhang, Xiaoyuan Wang, Zhihao Han, Ye Gong, Xuxiong Huang, Naisong Chen & Songlin Li

  2. National Demonstration Center on Experiment Teaching of Fisheries Science, Shanghai Ocean University, Shanghai, 201306, China

    Xuxiong Huang, Naisong Chen & Songlin Li

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  1. Nihe Zhang
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  2. Xiaoyuan Wang
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Contributions

Nihe Zhang: Investigation, Data curation, Formal analysis, Writing-Original Draft; Xiaoyuan Wang, Zhihao Han and Ye Gong: Investigation, Methodology; Xuxiong Huang and Naisong Chen: Conceptualization, Project administration; Songlin Li: Conceptualization, Supervision, Writing - Review & Editing, Funding acquisition. All authors commented on previous versions of the manuscript and approved the final manuscript.

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Zhang, N., Wang, X., Han, Z. et al. The preferential utilization of hepatic glycogen as energy substrates in largemouth bass (Micropterus salmoides) under short-term starvation. Fish Physiol Biochem 50, 785–796 (2024). https://doi.org/10.1007/s10695-023-01285-3

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