Hepatic Glucose Metabolism and Its Disorders in Fish.

Carbohydrate metabolism Disorders Fish Glucose Liver diseases

Journal

Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103

Informations de publication

Date de publication:
2022
Historique:
entrez: 22 11 2021
pubmed: 23 11 2021
medline: 25 11 2021
Statut: ppublish

Résumé

Carbohydrate, which is the most abundant nutrient in plant-sourced feedstuffs, is an economically indispensable component in commercial compound feeds for fish. This nutrient can enhance the physical quality of diets and allow for pellet expansion during extrusion. There is compelling evidence that an excess dietary intake of starch causes hepatic disorders, thereby further reducing the overall food consumption and growth performance of fish species. Among the severe metabolic disturbances are glycogenic hepatopathy (hepatomegaly caused by the excessive accumulation of glycogen in hepatocytes) and hepatic steatosis (the accumulation of large vacuoles of triacylglycerols in hepatocytes). The development of those disorders is mainly due to the limited ability of fish to oxidize glucose and control blood glucose concentration. The prolonged elevations of blood glucose increase glucose intake by the liver, and excess glucose is stored either as glycogen through glycogenesis in hepatocytes or as triglycerides via lipogenesis in tissues, depending on the species. In some fish species (e.g., largemouth bass), the liver has a low ability to regulate glycolysis, gluconeogenesis, and glycogen breakdown in response to high starch intake. For most species of fish, the liver size increases with lipid or glycogen accumulation when they have a high starch intake. It is a challenge to develop the same set of diagnostic criteria for all fish species as their physiology or metabolic patterns differ. Although glycogenic hepatopathy appears to be a common disease in carnivorous fish, it has been under-recognized in many studies. As a result, understanding these diseases and their pathogeneses in different fish species is crucial for manufacturing cost-effective pellet diets to promote the health, growth, survival, and feed efficiency of fish in future.

Identifiants

pubmed: 34807444
doi: 10.1007/978-3-030-85686-1_11
doi:

Substances chimiques

Dietary Carbohydrates 0
Glycogen 9005-79-2
Glucose IY9XDZ35W2

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

207-236

Informations de copyright

© 2022. Springer Nature Switzerland AG.

Références

Adeva-Andany M, López-Ojén M, Funcasta-Calderón R, Ameneiros-Rodríguez E, Donapetry-García C, Vila-Altesor M, Rodríguez-Seijas J (2014) Comprehensive review on lactate metabolism in human health. Mitochondrion 17:76–100
pubmed: 24929216
Akiyoshi H, Inoue A (2004) Comparative histological study of teleost livers in relation to phylogeny. Zool Sci 21:841–850
Ali A, Al-Asgah NA (2001) Effect of feeding different carbohydrate to lipid ratios on the growth performance and body composition of nile tilapia (Oreochromis niloticus) fingerlings. Anim Res 50:91–100
Ali MZ, Jauncey K (2004) Optimal dietary carbohydrate to lipid ratio in African catfish Clarias gariepinus (Burchell 1822). Aquacult Int 12:169–180
Alvarez MJ, Lopez-Bote CJ, Diez A, Corraze G, Arzel J, Dias J, Kaushik SJ, Bautista JM (1999) The partial substitution of digestible protein with gelatinized starch as an energy source reduces susceptibility to lipid oxidation in rainbow trout (Oncorhynchus mykiss) and sea bass (Dicentrarchus labrax) muscle. J Anim Sci 77:3322–3329
pubmed: 10641880
Amoah A, Coyle SD, Webster CD, Durborow RM, Bright LA, Tidwell JH (2008) Effects of graded levels of carbohydrate on growth and survival of largemouth bass, Micropterus salmoides. J World Aquacult Soc 39:397–405
Anderson RJ, Kienholz EW, Flickinger SA (1981) Protein requirements of smallmouth bass and largemouth bass. Nutr J 111:1085–1097
Arrese M, Cabrera D, Kalergis AM, Feldstein AE (2016) Innate immunity and inflammation in NAFLD/NASH. Digest Dis Sci 61:1294–1303
pubmed: 26841783
Bernardes CL, Navarro RD, Guerra-Santos B, Fortes-Silva R (2016) Effects of dietary carbohydrate/lipid ratios on growth, body composition, and nutrient utilization of hybrid catfish (Pseudoplatystoma reticulatum x Leiarius marmoratus). Rev Colomb Cienc Pec 29:58–65
Blasco Ferna´ndez-Borra´s J, Marimon I, Requena A, J (1996) Plasma glucose kinetics and tissue uptake in brown trout in vivo: effect of an intravascular glucose load. J Comp Physiol B 165:534–541
Brauge C, Medale F, Corraze G (1994) Effect of dietary carbohydrate levels on growth, body composition and glycaemia in rainbow trout, Oncorhynchus mykiss, reared in seawater. Aquaculture 123:109–120
Brauge C, Corraze G, Médale F (1995) Effects of dietary levels of carbohydrate and lipid on glucose oxidation and lipogenesis from glucose in rainbow trout, Oncorhynchus mykiss, reared in freshwater or in seawater. Comp Biochem Physiol A 111:117–124
Bright LA, Coyle SD, Tidwell JH (2005) Effect of dietary lipid level and protein energy ratio on growth and body composition of largemouth bass Micropterus salmoides. J World Aquacult Soc 36:129–134
Brooks GA (2018) The science and translation of lactate shuttle theory. Cell Metab 27:757–785
pubmed: 29617642
Brusle J, Anadon GG (1996) The structure and function of fish liver. In: Munshi JSD, Dutta HM (eds) Fish Morphology, CRC Press, Boca Raton. pp 77–93
Buchinger TJ, Li W, Johnson NS (2014) Bile salts as semiochemicals in fish. Chem Senses 39:647–654
pubmed: 25151152
Byrne CD (2010) Fatty liver: role of inflammation and fatty acid nutrition. Prostaglandins Leukot Ess Fat Acids 82:265–271
Cabezas J, Mayorga M, Crespo J (2012) Nonalcoholic fatty liver disease: a pathological view. In: Tagaya N (ed) Liver biopsy—indications, procedures, results. InTechOpen, Croatia, pp 161–188
Cai W, Liang XF, Yuan X, Liu L, He S, Li J, Li B, Xue M (2018) Different strategies of grass carp (Ctenopharyngodon idella) responding to insufficient or excessive dietary carbohydrate. Aquaculture 497:292–298
Capilla E, Díaz M, Albalat A, Navarro I, Pessin JE, Keller K, Planas JV (2004) Functional characterization of an insulin-responsive glucose transporter (GLUT4) from fish adipose tissue. Am J Physiol 287:E348–E357
Castillo J, Crespo D, Capilla E, Diaz M, Chauvigne F, Cerda J, Planas JV (2009) Evolutionary structural and functional conservation of an ortholog of the GLUT2 glucose transporter gene (SLC2A2) in zebrafish. Am J Physiol 297:R1570–R1581
Castro C, Diógenes AF, Coutinho F, Panserat S, Corraze G, Pérez-Jiménez A, Peres H, Oliva-Teles A (2016) Liver and intestine oxidative status of gilthead sea bream fed vegetable oil and carbohydrate rich diets. Aquaculture 464:665–672
Castro C, Pérez-Jiménez A, Guerreiro I, Peres H, Castro-Cunha M, Oliva-Teles A (2012) Effects of temperature and dietary protein level on hepatic oxidative status of Senegalese sole juveniles (Solea senegalensis). Comp Biochem Physiol A 163:372–378
Chandel A, Scarpato B, Camacho J, McFarland M, Mok S (2017) Glycogenic hepatopathy: resolution with minimal glucose control. Case Rep Hepatol 2017:7651387
Che DS, Nyingwa PS, Ralinala KM, Maswanganye GMT, Wu G (2021) Amino acids in the nutrition, metabolism, and health of domestic cats. Adv Exp Med Biol 1285:217–231
pubmed: 33770409
Chen YJ, Tian LX, Yang HJ, Chen PF, Yuan Y, Liu YJ, Liang GY (2012a) Effect of protein and starch level in practical extruded diets on growth, feed utilization, body composition, and hepatic transaminases of juvenile grass carp, Ctenopharyngodon idella. J World Aquacult Soc 43:187–197
Chen YJ, Liu YJ, Yang HJ, Yuan Y, Liu FJ, Tian LX, Liang GY, Yuan RM (2012b) Effect of dietary oxidized fish oil on growth performance, body composition, antioxidant defence mechanism and liver histology of juvenile largemouth bass Micropterus salmoides. Aquac Nutr 18:321–331
Chen YJ, Liu YJ, Tian LX, Niu J, Liang GY, Yang HJ, Yuan Y, Zhang YQ (2013) Effect of dietary vitamin E and selenium supplementation on growth, body composition, and antioxidant defense mechanism in juvenile largemouth bass (Micropterus salmoide) fed oxidized fish oil. Fish Physiol Biochem 39:593–604
pubmed: 23053606
Chen YJ, Yuan RM, Liu YJ, Yang HJ, Liang GY, Tian LX (2015) Dietary vitamin C requirement and its effects on tissue antioxidant capacity of juvenile largemouth bass, Micropterus salmoides. Aquaculture 435:431–436
Chinnaswamy R, Bhattacharya KR (1984) Relationship between amylose content and expansion characteristics of parboiled rice. J Cereal Sci 2:273–279
Dai W, Panserat S, Kaushik S, Terrier F, Plagnes-Juan E, Seiliez I, Skiba-Cassy S (2016) Hepatic fatty acid biosynthesis is more responsive to protein than carbohydrate in rainbow trout during acute stimulations. Am J Physiol 310:R74–86
Dairiki JK, Dias CTD, Cyrino JEP (2007) Lysine requirements of largemouth bass, Micropterus salmoides: a comparison of methods of analysis of dose-response trials data. J Appl Aquacult 19:1–27
Davies SJ (1985) The role of dietary fibre in fish nutrition. In: Roberts RJ (ed) Recent advances in aquaculture (Muir JF. Croom Helm, London, United Kingdom, pp 219–249
Díaz M, Antonescu CN, Capilla E, Klip A, Planas JV (2007) Fish glucose transporter (GLUT)-4 differs from rat GLUT4 in its traffic characteristics but can translocate to the cell surface in response to insulin in skeletal muscle cells. Endocrinology 148:5248–5257
pubmed: 17702851
Deng DF, Ju ZY, Dominy W, Murashige R, Wilson RP (2011) Optimal dietary protein levels for juvenile Pacific threadfin (Polydactylus sexfilis) fed diets with two levels of lipid. Aquaculture 316:25–30
Dentin R, Girard J, Postic C (2005) Carbohydrate responsive element binding protein (ChREBP) and sterol regulatory element binding protein-1c (SREBP-1c): two key regulators of glucose metabolism and lipid synthesis in liver. Biochimie 87:81–86
pubmed: 15733741
Dias J, Alvarez MJ, Arzel J, Corraze G, Diez A, Bautista JM, Kaushik SJ (2005) Dietary protein source affects lipid metabolism in the European seabass (Dicentrarchus labrax). Comp Biochem Physiol A 142:19–31
Enes P, Panserat S, Kaushik S, Oliva-Teles A (2006) Effect of normal and waxy maize starch on growth, food utilization and hepatic glucose metabolism in European sea bass (Dicentrarchus labrax) juveniles. Comp Biochem Physiol A 143:89–96
Enes P, Panserat S, Kaushik S, Oliva-Teles A (2009) Nutritional regulation of hepatic glucose metabolism in fish. Fish Physiol Biochem 35:519–539
pubmed: 18791853
Farrell GC, Larter CZ (2006) Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology 43(S1):S99-112
pubmed: 16447287
Fabbrini E, Sullivan S, Klein S (2010) Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 51:679–689
pubmed: 20041406
Faccioli CK, Chedid RA, Bombonato MTS, Vicentini CA, Vicentini IBF (2014) Morphology and histochemistry of the liver of carnivorous fish Hemisorubim platyrhynchos. Int J Morphol 715–720
Fang YZ, Yang S, Wu G (2002) Free radicals, antioxidants, and nutrition. Nutrition 18:872–879
doi: 10.1016/S0899-9007(02)00916-4 pubmed: 12361782
FAO (2020) The state of world fisheries and aquaculture 2020. Food and Agriculture Organization of the United Nations, Rome
Fu WJ, Haynes TE, Kohli R, Hu J, Shi W, Spencer TE, Carroll RJ, Meininger CJ, Wu G (2005) Dietary L-arginine supplementation reduces fat mass in Zucker diabetic fatty rats. J Nutr 135:714–721
pubmed: 15795423
Fynn-Aikins K, Hung SS, Liu W, Li H (1992) Growth, lipogenesis and liver composition of juvenile white sturgeon fed different levels of D-glucose. Aquaculture 105:61–72
Gong Y, Yang F, Hu J, Liu C, Liu H, Han D, Jin J, Yang Y, Zhu X, Yi J, Xie S (2019) Effects of dietary yeast hydrolysate on the growth, antioxidant response, immune response and disease resistance of largemouth bass (Micropterus salmoides). Fish Shellfish Immun 94:548–557
Groussard C, Morel I, Chevanne M, Monnier M, Cillard J, Delamarche A (2020) Free radical scavenging and antioxidant effects of lactate ion: an in vitro study. J Appl Physiol 89:169–175
Guo JL, Kuang WM, Zhong YF, Zhou YL, Chen YJ, Lin SM (2020) Effects of supplemental dietary bile acids on growth, liver function and immunity of juvenile largemouth bass (Micropterus salmoides) fed high-starch diet. Fish Shellfish Immun 97:602–607
Hagey LR, Møller PR, Hofmann AF, Krasowski MD (2010) Diversity of bile salts in fish and amphibians: evolution of a complex biochemical pathway. Physiol Biochem Zool 83:308–321
pubmed: 20113173 pmcid: 2845723
Hall JR, Short CE, Driedzic WR (2006) Sequence of Atlantic cod (Gadus morhua) GLUT4, GLUT2 and GPDH: developmental stage expression, tissue expression and relationship to starvation-induced changes in blood glucose. J Exp Biol 209:4490–4502
pubmed: 17079719
Hemre GI, Mommsen TP, Krogdahl A (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8:175–194
Hilton JW, Plisetskaya EM, Leatherland JF (1987) Does oral 3,5,3¢-triiodo-L-thyronine affect dietary glucose utilization and plasma insulin levels in rainbow trout (Salmo gairdneri). Fish Physiol Biochem 4:113–120
pubmed: 24226258
Hilton JW, Atkinson JL, Slinger SJ (2011) Effect of increased dietary fiber on the growth of rainbow trout (Salmo gairdneri). Can J Fish Aquatic Sci 40:81–85
Hofmann AF, Hagey LR, Krasowski MD (2010) Bile salts of vertebrates: structural variation and possible evolutionary significance. J Lipid Res 51:226–246
pubmed: 19638645 pmcid: 2803226
Hou Y, He W, Hu S, Wu G (2019) Composition of polyamines and amino acids in plant-source foods for human consumption. Amino Acids 51:1153–1165
doi: 10.1007/s00726-019-02751-0 pubmed: 31197570
Hou YQ, Hu SD, Li XY, He WL, Wu G (2020) Amino acid metabolism in the liver: nutritional and physiological significance. Adv Exp Med Biol 1265:21–37
pubmed: 32761568
Jia S, Li X, Zheng S, Wu G (2017) Amino acids are major energy substrates for tissues of hybrid striped bass and zebrafish. Amino Acids 49:2053–2063
pubmed: 28852872
Jia SC, Li XY, He WL, Wu G (2021) Oxidation of energy substrates in tissues of fish: metabolic significance and implications for gene expression and carcinogenesis. Adv Exp Med Biol 1332:67–83
pubmed: 34251639
Jia SC, Li XY, He WL, Wu G (2022) Protein-sourced feedstuffs for aquatic animals in nutrition research and aquaculture. Adv Exp Med Biol 1354:237–261
Jiang L, Wu H, Huang K, Ma Y, Yang Q, Yu D, Zhong L (2013) Effects of dietary carbohydrate levels on growth performance and liver metabolism functions of juvenile tilapia (Oreochromis niloticus). J Fish China 37:245–255
Jin M, Pan T, Cheng X, Zhu TT, Sun P, Zhou F, Ding X, Zhou Q (2019a) Effects of supplemental dietary L-carnitine and bile acids on growth performance, antioxidant and immune ability, histopathological changes and inflammatory response in juvenile black seabream (Acanthopagrus schlegelii) fed high-fat diet. Aquaculture 504:199–209
Jin M, Pan T, Tocher DR, Betancor MB, Monroig Ó, Shen Y, Zhu T, Sun P, Jiao L, Zhou Q (2019b) Dietary choline supplementation attenuated high-fat diet-induced inflammation through regulation of lipid metabolism and suppression of NFκB activation in juvenile black seabream (Acanthopagrus schlegelii). J Nutr Sci 8:e38
Jin M, Zhu T, Tocher DR, Luo J, Shen Y, Li X, Pan T, Yuan Y, Betancor MB, Jiao L, Sun P (2020) Dietary fenofibrate attenuated high-fat-diet-induced lipid accumulation and inflammation response partly through regulation of pparα and sirt1 in juvenile black seabream (Acanthopagrus schlegelii). Dev Comp Immunol 109:103691
Jobgen WJ, Meininger CJ, Jobgen SC, Li P, Lee MJ, Smith SB, Spencer TE, Fried SK, Wu G (2009) Dietary L-arginine supplementation reduces white-fat gain and enhances skeletal muscle and brown fat masses in diet-induced obese rats. J Nutr 139:230–237
pubmed: 19106310 pmcid: 3151442
Jobling M (1994) Book of fish bioenergetics- fish and fisheries series 13, 1st edn. Chapman & Hall, London, United Kingdom
Kamalam BS, Medale F, Panserat S (2017) Utilization of dietary carbohydrates in farmed fishes: new insights on influencing factors, biological limitations and future strategies. Aquaculture 467:3–27
Krogdahl Å, HEMRE GI, Mommsen TP, (2005) Carbohydrates in fish nutrition: digestion and absorption in postlarval stages. Aquac Nutr 11:103–122
Leung LY, Woo NY (2012) Influence of dietary carbohydrate level on endocrine status and hepatic carbohydrate metabolism in the marine fish Sparus sarba. Fish Physiol Biochem 38:543–554
pubmed: 21701819
Li XF, Wang Y, Liu WB, Jiang GZ, Zhu J (2013) Effects of dietary carbohydrate/lipid ratios on growth performance, body composition and glucose metabolism of fingerling blunt snout bream Megalobrama amblycephala. Aquac Nutr 19:701–708
Li X, Zhu X, Han D, Yang Y, Jin J, Xie S (2014) 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). Aquac Res 47:128–139
Li XY, Wang JT, Han T, Hu SX, Jiang YD (2015) Effects of dietary carbohydrate level on growth and body composition of juvenile giant croaker Nibea japonica. Aquac Res 46:2851–2858
Li XY, Wu G (2019) Oxidation of energy substrates in tissues of largemouth bass (Micropterus salmoides). J Anim Sci 97(Suppl 3):68–69
pmcid: 6898196
Li XF, Xu C, Zhang DD, Jiang GZ, Liu WB (2016) Molecular characterization and expression analysis of glucokinase from herbivorous fish Megalobrama amblycephala subjected to a glucose load after the adaption to dietary carbohydrate levels. Aquaculture 459:89–98
Li S, Lian X, Chen N, Wang M, Sang C (2018) Effects of dietary vitamin E level on growth performance, feed utilization, antioxidant capacity and nonspecific immunity of largemouth bass, Micropterus salmoides. Aquac Nutr 24:1679–1688
Li S, Li Z, Zhang J, Sang C, Chen N (2019a) The impacts of dietary carbohydrate levels on growth performance, feed utilization, glycogen accumulation and hepatic glucose metabolism in hybrid grouper (Epinephelus fuscoguttatus♀× E. lanceolatus♂). Aquaculture 512:734351
Li S, Sang C, Wang A, Zhang J, Chen N (2019b) Effects of dietary carbohydrate sources on growth performance, glycogen accumulation, insulin signaling pathway and hepatic glucose metabolism in largemouth bass, Micropterus salmoides. Aquaculture 513:734391
Li P, He WL, Wu G (2021e) Composition of amino acids in foodstuffs for humans and animals. Adv Exp Med Biol 1332:189–210
pubmed: 34251645
Li P, Wu G (2020) Composition of amino acids and related nitrogenous nutrients in feedstuffs for animal diets. Amino Acids 52:523–542
pubmed: 32162082
Li P, Wu G (2022) Functional molecules of intestinal mucosal products in animal nutrition and health. Adv Exp Med Biol 1354:263–277
Li P, Mai K, Trushenski J, Wu G (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37:43–53
pubmed: 18751871
Li SL, Zhang YC, Liu N, Chen JQ, Guo LN, Dai ZL, Wang C, Wu ZL, Wu G (2020a) Dietary L-arginine supplementation reduces lipid accretion by regulating fatty acid metabolism in Nile tilapia (Oreochromis niloticus). J Anim Sci Biotechnol 11:82
pubmed: 32817790 pmcid: 7427058
Li XY, Zheng SX, Ma XK, Cheng KM, Wu G (2020b) Effects of dietary starch and lipid levels on the protein retention and growth of largemouth bass (Micropterus salmoides). Amino Acids 52:999–1016
pubmed: 32648068
Li XY, Zheng SX, Ma XK, Cheng KM, Wu G (2020c) Effects of dietary protein and lipid levels on growth performance, feed utilization, and liver histology of largemouth bass (Micropterus salmoides). Amino Acids 52:1043–1061
pubmed: 32683495
Li XL, Zheng SX, Jia SC, Song F, Zhou CP, Wu G (2020d) Oxidation of energy substrates in tissues of largemouth bass (Micropterus salmoides). Amino Acids 52:1017–1032
pubmed: 32656621
Li XY, Zheng SX, Han T, Song F, Wu G (2020) Effects of dietary protein intake on the oxidation of glutamate, glutamine, glucose and palmitate in tissues of largemouth bass (Micropterus salmoides). Amino Acids 52:1491–1503
pubmed: 33161445
Li XL, Zheng SX, Wu G (2020f) Nutrition and metabolism of glutamate and glutamine in fish. Amino Acids 52:671–691
pubmed: 32405703
Li XY, Zheng SX, Wu G (2020g) Amino acid metabolism in the kidneys: nutritional and physiological significance. Adv Exp Med Biol 1265:71–95
pubmed: 32761571
Li XY, Zheng SX, Ma XK, Cheng KM, Wu G (2021a) Use of alternative protein sources for fishmeal replacement in the diet of largemouth bass (Micropterus salmoides). Part I: effects of poultry by-product meal and soybean meal on growth, feed utilization, and health. Amino Acids 53:33–47
pubmed: 33236255
Li XY, Zheng SX, Cheng KM, Ma XK, Wu G (2021b) Use of alternative protein sources for fishmeal replacement in the diet of largemouth bass (Micropterus salmoides). Part II: effects of supplementation with methionine or taurine on growth, feed utilization, and health. Amino Acids 53:49–62
pubmed: 33398521
Li XY, Zheng SX, Wu G (2021c) Nutrition and functions of amino acids in fish. Adv Exp Med Biol 1285:133–168
pubmed: 33770406
Li XY, Han T, Zheng SX, Wu G (2021d) Nutrition and functions of amino acids in aquatic crustaceans. Adv Exp Med Biol 1285:169–198
pubmed: 33770407
Liao Z, Sun B, Zhang Q, Jia L, Wei Y, Liang M, Xu H (2020) Dietary bile acids regulate the hepatic lipid homeostasis in tiger puffer fed normal or high-lipid diets. Aquaculture 519:734935
Lin YC, Kao CH (2012) Glycogenic hepatopathy in type 1 diabetes mellitus. Liver Int 32:1294
pubmed: 22731940
Lin SM, Shi CM, Mu MM, Chen YJ, Luo L (2018) Effect of high dietary starch levels on growth, hepatic glucose metabolism, oxidative status and immune response of juvenile largemouth bass, Micropterus salmoides. Fish Shellfish Immun 78:121–126
Liu XH, Ye CX, Zheng LM, Ou CC, Wang AL, Ye JD, Kong JH (2015) Dietary maize starch influences growth performance, apparent digestibility coefficient, and hepatic enzyme activities of carbohydrate metabolism in obscure puffer, Takifugu obscurus (Abe). J World Aquac Soc 46:102–113
doi: 10.1111/jwas.12168
Luo Y, Wu X, Li W, Jiang S, Lu S, Wu M (2016) Effects of different corn starch levels on growth, protein input, and feed utilization of juvenile hybrid grouper (male Epinephelus lanceolatus× female E. fuscoguttatus). N Am J Aquacult 78:168–173
Lygren B, Hemre GI (2001) Influence of dietary carbohydrate on antioxidant enzyme activities in liver of Atlantic salmon (Salmo salar L.). Aquacult Int 9:421–427
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
Maharaj V, Fitz M, Ding X (2017) Drug-induced liver injury in the setting of glycogenic hepatopathy. J Gen Intern Med 32:714–717
pubmed: 28224373 pmcid: 5442014
Marchesini G, Bugianesi E, Forlani G, Cerrelli F, Lenzi M, Manini R, Natale S, Vanni E, Villanova N, Melchionda N, Rizzetto M (2003) Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 37:917–923
pubmed: 12668987
Marín-Juez R, Diaz M, Morata J, Planas JV (2013) Mechanisms regulating GLUT4 transcription in skeletal muscle cells are highly conserved across vertebrates. PLoS One 8:e80628
Marín-Juez R, Capilla E, Carvalho-Simoes F, Camps M, Planas JV (2014) Structural and functional evolution of glucose transporter 4 (GLUT4): a look at GLUT4 in fish. In: Szablewski L (ed) Glucose homeostasis. IntechOpen, London, pp 37–67
Martínez-Palacios CA, Ríos-Durán MG, Ambriz-Cervantes L, Jauncey KJ, Ross LG (2007) Dietary protein requirement of juvenile Mexican Silverside (Menidia estor Jordan 1879), a stomachless zooplanktophagous fish. Aquac Nutr 13:304–310
Martos-Sitcha JA, Bermejo-Nogales A, Calduch-Giner JA, Jaume Pérez-Sánchez J (2017) Gene expression profiling of whole blood cells supports a more efficient mitochondrial respiration in hypoxia-challenged gilthead sea bream (Sparus aurata). Front Zool 14:34
Maas RM, Verdegem MC, Wiegertjes GF, Schrama JW (2020) Carbohydrate utilisation by tilapia: a meta-analytical approach. Rev Aquacult 12:1851–1866
Milligan LC, Pagnotta A (1991) The role of blood glucose in the restoration of muscle glycogen during recovery from exhaustive exercise in rainbow trout (Oncorhynchus mykiss) and winter flounder (Pseudopleuronectes americanus). J Exp Biol 161:489–508
pubmed: 1757776
Mohanta KN, Mohanty SN, Jena J, Sahu NP, Patro B (2009) Carbohydrate level in the diet of silver barb, Puntius gonionotus (Bleeker) fingerlings: effect on growth, nutrient utilization and whole body composition. Aquac Res 40:927–937
Mokhtar DM (2017) Fish histology: from cells to organs. Apple Academic Press, Palm Bay, Florida
Moreira IS, Peres H, Couto A, Enes P, Oliva-Teles A (2008) Temperature and dietary carbohydrate level effects on performance and metabolic utilisation of diets in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 274:153–160
Moon TW, Foster GD (1995) Tissue carbohydrate metabolism, gluconeogenesis and hormonal and environmental influences. Biochem Mol Biol Fish 4:65–100
National Research Council (NRC) (2011) Nutrient requirements of fish and shrimp. National Academies Press, Washington DC
Oberbauer AM, Larsen JA (2021) Amino acids in dog nutrition and health. Adv Exp Med Biol 1285:199–216
pubmed: 33770408
Palmer TN, Ryman BE (1972) Studies on oral glucose intolerance in fish. J Fish Biol 4:311–319
Panserat S, Plagnes-Juan E, Kaushik S (2001a) Nutritional regulation and tissue specificity of gene expression for proteins involved in hepatic glucose metabolism in rainbow trout (Oncorhynchus mykiss). J Exp Biol 204:2351–2360
pubmed: 11507117
Panserat S, Plagnes-Juan E, Breque J, Kaushik S (2001b) Hepatic phosphoenolpyruvate carboxykinase gene expression is not repressed by dietary carbohydrates in rainbow trout (Oncorhynchus mykiss). J Exp Biol 204:359–365
pubmed: 11136621
Panserat S, Plagnes-Juan E, Kaushik S (2002) Gluconeogenic enzyme gene expression is decreased by dietary carbohydrates in common carp (Cyprinus carpio) and gilthead seabream (Sparus aurata). Biochim Biophys Acta 1579:35–42
pubmed: 12401217
Panserat S, Rideau N, Polakof S (2014) Nutritional regulation of glucokinase: a cross-species story. NutrRes Rev 27:21–47
Pérez-Jiménez A, Abellán E, Arizcun M, Cardenete G, Morales AE, Hidalgo MC (2017) Dietary carbohydrates improve oxidative status of common dentex (Dentex dentex) juveniles, a carnivorous fish species. Comp Biochem Physiol A 203:17–23
Prisingkorn W, Prathomya P, Liu H, Deng FY, Zhao YH, Wang WM (2017) Transcriptomic and metabolomics analyses show that high carbohydrate induces fatty liver in blunt snout bream (Megalobrama amblycephala). Preprints 2017:2017010117
Polakof S, Medale F, Larroquet L, Vachot C, Corraze G, Panserat S (2011) Regulation of de novo hepatic lipogenesis by insulin infusion in rainbow trout fed a high-carbohydrate diet. J Anim Sci 89:3079–3088
pubmed: 21571891
Rawles SD, Smith SB, Gatlin DM (2008) Hepatic glucose utilization and lipogenesis of hybrid striped bass (Morone chrysops× Morone saxatilis) in response to dietary carbohydrate level and complexity. Aquac Nutr 14:40–50
Ren MC, Ai QH, Mai K, Ma HM, Wang XJ (2011) Effect of dietary carbohydrate level on growth performance, body composition, apparent digestibility coefficient and digestive enzyme activities of juvenile cobia, Rachycentron canadum L. Aquac Res 42:1467–1475
Riaz MN, Rokey GJ (2011) Extrusion problems solved: food, pet food and feed. Elsevier, New York, NY
Russell DW (2003) The enzymes, regulation, and genetics of bile acid synthesis. Annu Rev Biochem 72:137–174
pubmed: 12543708
Satapati S, Kucejova B, Duarte JA, Fletcher JA, Reynolds L, Sunny NE, He T, Nair LA, Livingston K, Fu X, Merritt ME (2015) Mitochondrial metabolism mediates oxidative stress and inflammation in fatty liver. J Clin Invest 125:4447–4462
pubmed: 26571396 pmcid: 4665800
Saunier E, Benelli C, Bortoli S (2016) The pyruvate dehydrogenase complex in cancer: an old metabolic gatekeeper regulated by new pathways and pharmacological agents. Int J Cancer 138:809–817
pubmed: 25868605
Saxena P, Turner I, McIndoe R (2010) Hepatobiliary and pancreatic: glycogenic hepatopathy: a reversible condition. J Gastroenterol Hepatol 25:646–646
pubmed: 20370736
Sherigar JM, De Castro J, Yin YM, Guss D, Mohanty SR (2018) Glycogenic hepatopathy: a narrative review. World J Hepatol 10:172
pubmed: 29527255 pmcid: 5838438
Shimeno S, Kheyyali D, Shikata T (1995) Metabolic response to dietary carbohydrate to protein rations in carp. Fish Sci 61:277–281
Siddiqui RA, Xu Z, Harvey KA, Pavlina TM, Becker MJ, Zaloga GP (2015) Comparative study of the modulation of fructose/sucrose-induced hepatic steatosis by mixed lipid formulations varying in unsaturated fatty acid content. Nutr Metab 12:41
Skilleter DN, Kun E (1972) The oxidation of L-lactate by liver mitochondria. Arch Biochem Biophys 152:92–104
pubmed: 4342115
Skiba-Cassy S, Lansard M, Panserat S, Médale F (2009) Rainbow trout genetically selected for greater muscle fat content display increased activation of liver TOR signaling and lipogenic gene expression. Am J Phys 297:R1421–R1429
doi: 10.1152/ajpregu.00312.2009
Skiba-Cassy S, Panserat S, Larquier M, Dias K, Surget A, Plagnes-Juan E, Kaushik S, Seiliez I (2013) Apparent low ability of liver and muscle to adapt to variation of dietary carbohydrate: protein ratio in rainbow trout (Oncorhynchus mykiss). Br J Nutr 109:1359–1372
pubmed: 22951215
Stier A, Bize P, Schull Q, Zoll J, Singh F, Geny B, Gros F, Royer C, Massemin S, Criscuolo F (2013) Avian erythrocytes have functional mitochondria, opening novel perspectives for birds as animal models in the study of ageing. Front Zool 10:33
doi: 10.1186/1742-9994-10-33
Stone D, Allan G, Anderson A (2003) Carbohydrate utilization by juvenile silver perch, Bidyanus bidyanus (Mitchell). III. The protein-sparing effect of wheat starch-based carbohydrates. Aquac Res 34:123–134
Subhadra B, Lochmann R, Rawles S, Chen R (2006) Effect of dietary lipid source on the growth, tissue composition and hematological parameters of largemouth bass (Micropterus salmoides). Aquaculture 255:210–222
Sulaiman MA, Kamarudin MS, Romano N, Syukri F (2020) Effects of increasing dietary carbohydrate level on feed utilisation, body composition, liver glycogen, and intestinal short chain fatty acids of hybrid lemon fin barb (Barbonymus gonionotus♀ Hypsibarbus wetmorei male♂). Aquacul Rep 16:100250
Szabo G, Saha B, Ambade A (2018) The Liver as an immune organ. In: Boyer TD, Terrault NA, Lindor KD (eds) Zakim and Boyer’s Hepatology (Sanyal AJ. Elsevier, New York, pp 66–76
Szczesna-Kaczmarek A (1990) L-lactate oxidation by skeletal muscle mitochondria. Int J Biochem 22:617–620
pubmed: 2379665
Tammar AR (1974) Bile salts in fishes. Chem Zool 8:595–612
Tan Q, Xie S, Zhu X, Lei W, Yang Y (2007) Effect of dietary carbohydrate-to-lipid ratios on growth and feed utilization in Chinese longsnout catfish (Leiocassis longirostris Günther). J Appl Ich 23:605–610
Terova G, Rimoldi S, Brambilla F, Gornati R, Bernardini G, Saroglia M (2009) In vivo regulation of GLUT2 mRNA in sea bass (Dicentrarchus labrax) in response to acute and chronic hypoxia. Comp Biochem Physiol B 152:306–316
pubmed: 19162213
Tang Y, Boutilier RG (1991) White muscle intracellular acid base and lactate status following exhaustive exercise: a comparison between freshwater- and seawater-adapted rainbow trout. J Exp Biol 156:153–171
Tian LX, Liu YJ, Yang HJ, Liang GY, Niu J (2012) Effects of different dietary wheat starch levels on growth, feed efficiency and digestibility in grass carp (Ctenopharyngodon idella). Aquacult Int 20:283–293
Tidwell JH, Coyle SD, Bright LA, Yasharian D (2005) Evaluation of plant and animal source proteins for replacement of fish meal in practical diets for the largemouth bass Micropterus salmoides. J World Aquacult Soc 36:454–463
Tidwell JH, Coyle S, Bright LA (2007) Effects of different types of dietary lipids on growth and fatty acid composition of largemouth bass. North Am. J Aquacult 69:257–264
Torbenson M, Chen YY, Brunt E, Cummings OW, Gottfried M, Jakate S, Liu YC, Yeh MM, Ferrell L (2006) Glycogenic hepatopathy: an underrecognized hepatic complication of diabetes mellitus. Am J Surg Pathol 30:508–513
pubmed: 16625098
Torfi Mozanzadeh M, Yavari V, Marammazi JG, Agh N, Gisbert E (2017) Optimal dietary carbohydrate-to-lipid ratios for silvery-black porgy (Sparidentex hasta) juveniles. Aquac Nutr 23:470–483
Torres DM, Williams CD, Harrison SA (2012) Features, diagnosis, and treatment of nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 10:837–858
pubmed: 22446927
Tranulis MA, Christophersen B, Blom AK, Borrebaek B (1991) Glucose dehydrogenase, glucose-6-phosphate dehydrogenase and hexokinase in liver of rainbow trout (Salmo gairdneri). effects of starvation and temperature variations. Comp Biochem Physiol B 99:687–691
pubmed: 1769217
Tucker JW Jr (1999) Grouper aquaculture. South Reg Aquac Cent Publ 721:1–11
Viegas IDDSM (2012) Sources of blood glucose and liver glycogen in the seabass (Dicentrarchus labrax L.): implications to carbohydrate metabolism in fish. PhD Dissertation, Universidade de Coimbra, Portugal
Viegas I, Rito J, Jarak I, Leston S, Caballero-Solares A, Metón I, Pardal MA, Baanante IV, Jones JG (2015) Contribution of dietary starch to hepatic and systemic carbohydrate fluxes in European seabass (Dicentrarchus labrax L.). Br J Nutr 113:1345–1354
pubmed: 25989995
Waagbø R, Glette J, Sandnes K, Hemre GI (1994) Influence of dietary carbohydrate on blood chemistry, immunity and disease resistance in Atlantic salmon, Salmo salar L. J Fish Dis 17:245–258
Wang XF, Perez E, Liu R, Yan LJ, Mallet RT, Yang SU (2007) Pyruvate protects mitochondria from oxidative stress in human neuroblastoma SK-N-SH cells. Brain Res 1132:1–9
pubmed: 17174285
Wang Y, Liu YJ, Tian LX, Du ZY, Wang JT, Wang S, Xiao WP (2005) Effects of dietary carbohydrate level on growth and body composition of juvenile tilapia, Oreochromis niloticus× O. aureus. Aquac Res 36:1408–1413
Wang LN, Liu WB, Lu KL, Xu WN, Cai DS, Zhang CN, Qian Y (2014) Effects of dietary carbohydrate/lipid ratios on non-specific immune responses, oxidative status and liver histology of juvenile yellow catfish Pelteobagrus fulvidraco. Aquaculture 426:41–48
Wang J, Li X, Han T, Yang Y, Jiang Y, Yang M, Xu Y, Harpaz S (2016a) Effects of different dietary carbohydrate levels on growth, feed utilization and body composition of juvenile grouper Epinephelus akaara. Aquaculture 459:143–147
Wang J, Jiang Y, Li X, Han T, Yang Y, Hu S, Yang M (2016b) Dietary protein requirement of juvenile red spotted grouper (Epinephelus akaara). Aquaculture 450:289–294
Watanabe T (2002) Strategies for further development of aquatic feeds. Fish Sci 68:242–252
Welker TL, Overturf K, Snyder S, Liu K, Abernathy J, Frost J, Barrows FT (2018) Effects of feed processing method (extrusion and expansion-compression pelleting) on water quality and growth of rainbow trout in a commercial setting. J Appl Aquac 30:97–124
Wilkins Benjamin J, Pack M (2013) Zebrafish models of human liver development and disease. Compr Physiol 3:1213–1230
pubmed: 23897685 pmcid: 4784975
Wilson RP (1994) Utilization of dietary carbohydrate by fish. Aquaculture 124:67–80
Wilson RP, Halver JE (1986) Protein and amino acid requirements of fishes. Annu Rev Nutr 6:225–244
pubmed: 3089240
Wu G, Meininger CJ, McNeal CJ, Bazer FW, Rhoads JM (2021) Role of L-arginine in nitric oxide synthesis and health in humans. Adv Exp Med Biol 1332:167–187
pubmed: 34251644
Wu XY, Liu YJ, Tian LX, Mai KS, Yang HJ, Liang GY (2007) Effects of raw corn starch levels on growth, feed utilization, plasma chemical indices and enzyme activities in juvenile yellowfin seabream Sparus latus Houttuyn. Aquac Res 38:1330–1338
Wu G (2018) Principles of animal nutrition. CRC Press, Boca Raton, Florida
Wu G (2020a) Management of metabolic disorders (including metabolic diseases) in ruminant and nonruminant animals. In: Lamb GC, Wu G (eds) Animal agriculture: challenges, innovations, and sustainability (Bazer FW). Elsevier, New York, pp 471–492
Wu G (2020b) Important roles of dietary taurine, creatine, carnosine, anserine and hydroxyproline in human nutrition and health. Amino Acids 52:329–360
pubmed: 32072297 pmcid: 7088015
Wu G (2021) Amino Acids: biochemistry and Nutrition, 2nd edition. CRC Press, Boca Raton, Florida
Wu G (2022) Nutrition and metabolism: Foundations for animal growth, development, reproduction, and health. Adv Exp Med Biol 1354:1–24
Xie D, Yang L, Yu R, Chen F, Lu R, Qin C, Nie G (2017) Effects of dietary carbohydrate and lipid levels on growth and hepatic lipid deposition of juvenile tilapia, Oreochromis niloticus. Aquaculture 479:696–703
Yamamoto T, Konishi K, Shima T, Furuita H, Suzuki N, Tabata M (2001) Influence of dietary fat and carbohydrate levels on growth and body composition of rainbow trout Oncorhynchus mykiss under selffeeding conditions. Fish Sci 67:221–227
Yang SD, Lin TS, Liou CH, Peng HK (2003) Influence of dietary protein levels on growth performance, carcass composition and liver lipid classes of juvenile Spinibarbus hollandi (Oshima). Aquac Res 34:661–666
Yang Y, Han T, Xiao J, Li X, Wang J (2018) Transcriptome analysis reveals carbohydrate-mediated liver immune responses in Epinephelus akaara. Sci Rep 8:1
Yin P, Xie S, Huo Y, Guo T, Fang H, Zhang Y, Liu Y, Tian L, Niu J (2019) Effects of dietary oxidized fish oil on growth performance, antioxidant defense system, apoptosis and mitochondrial function of juvenile largemouth bass (Micropterus salmoides). Aquaculture 500:347–358
Yu LL, Yu HH, Liang XF, Li N, Wang X, Li FH, Wu XF, Zheng YH, Xue M (2018) Dietary butylated hydroxytoluene improves lipid metabolism, antioxidant and anti-apoptotic response of largemouth bass (Micropterus salmoides). Fish Shellfish Immun 72:220–229
Yuan L, Bambha K (2015) Bile acid receptors and nonalcoholic fatty liver disease. World J Hepatol 7:2811
Zamora-Sillero J, Ramos LRV, Romano LA, Monserrat JM, Tesser MB (2013) Effect of dietary dextrin levels on the growth performance, blood chemistry, body composition, hepatic triglicerides and glycogen of Lebranche mullet juveniles (Mugilliza Valenciennes 1836, Mugilidae). J Appl Ichthyol 29:1342–1347
Zhang J, Zhou F, Wang LL, Shao Q, Xu Z, Xu J (2010) Dietary protein requirement of juvenile black sea bream, Sparus macrocephalus. J World Aquac Soc 41:151–164
Zhang W, Tan B, Liu K, Dong X, Yang Q, Chi S, Liu H, Zhang S, Wang H (2019) Effects of different dietary lipids on growth, body composition and lipid metabolism-related enzymes and genes in juvenile largemouth bass, Micropterus salmoides. Aquac Nutr 25:1318–1326
Zhou H, Chen N, Qiu X, Zhao M, Jin L (2012) Arginine requirement and effect of arginine intake on immunity in largemouth bass, Micropterus salmoides. Aquac Nutr 18:107–116
Zhou CP, Liu B, Xie J, Ge XP, Xu P, Zhou QL, Pan LK, Chen RL (2013a) Effect of dietary carbohydrate level on growth performance, blood chemistry, hepatic enzyme activity, and growth hormone gene expression in Wuchang bream (Megalobrama amblycephala). Isr J Aquac 65:882–890
Zhou C, Liu B, Ge X, Xie J, Xu P (2013b) Effect of dietary carbohydrate on the growth performance, immune response, hepatic antioxidant abilities and heat shock protein 70 expression of Wuchang bream, Megalobrama amblycephala. J Appl Ich 29:1348–1356
Zhou C, Ge X, Niu J, Lin H, Huang Z, Tan X (2015) Effect of dietary carbohydrate levels on growth performance, body composition, intestinal and hepatic enzyme activities, and growth hormone gene expression of juvenile golden pompano, Trachinotus ovatus. Aquaculture 437:390–397
Zhou M, Liang R, Mo J, Yang S, Gu N, Wu Z, Babu VS, Li J, Huang Y, Lin L (2018) Effects of brewer’s yeast hydrolysate on the growth performance and the intestinal bacterial diversity of largemouth bass (Micropterus salmoides). Aquaculture 484:139–144
Zhou P, Wang M, Xie F, Deng DF, Zhou Q (2016) Effects of dietary carbohydrate to lipid ratios on growth performance, digestive enzyme and hepatic carbohydrate metabolic enzyme activities of large yellow croaker (Larmichthys crocea). Aquaculture 452:45–51
Zhu Y, Che Y, Liu Y, Yang H, Liang G, Tian L (2012) Effect of dietary selenium level on growth performance, body composition and hepatic glutathione peroxidase activities of largemouth bass Micropterus salmoide. Aquac Res 43:1660–1668
Zivkovic AM, German JB, Sanyal AJ (2007) Comparative review of diets for the metabolic syndrome: implications for nonalcoholic fatty liver disease. Am J Clin Nutr 86:285–300
pubmed: 17684197

Auteurs

Xinyu Li (X)

Department of Animal Science, Texas A&M University, College Station, TX, 77843, USA.

Tao Han (T)

Department of Animal Science, Texas A&M University, College Station, TX, 77843, USA.
Department of Aquaculture, Zhejiang Ocean University, Zhoushan, 316022, Zhejiang, China.

Shixuan Zheng (S)

Guangdong Yuehai Feeds Group Co., Ltd., Zhanjiang, 524017, Guangdong, China.

Guoyao Wu (G)

Department of Animal Science, Texas A&M University, College Station, TX, 77843, USA. g-wu@tamu.edu.

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