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Role of creatine supplementation on the myofibre characteristics and muscle protein synthesis of grass carp (Ctenopharyngodon idellus)

Published online by Cambridge University Press:  05 May 2022

Juan Tian Open the ORCID record for Juan Tian [Opens in a new window] ,
Xiaoli Cheng ,
Lijuan Yu ,
Ming Jiang ,
Weihua Gao ,
Xing Lu ,
Wenbing Zhang  and
Hua Wen
Juan Tian
Affiliation:
Key Laboratory of Freshwater Biodiversity Conservation, the Ministry of Agriculture and Rural Affairs, Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan, 430223, People’s Republic of China
Xiaoli Cheng
Affiliation:
Key Laboratory of Freshwater Biodiversity Conservation, the Ministry of Agriculture and Rural Affairs, Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan, 430223, People’s Republic of China College of Animal Science, Yangtze University, Jingzhou, People’s Republic of China
Lijuan Yu
Affiliation:
Key Laboratory of Freshwater Biodiversity Conservation, the Ministry of Agriculture and Rural Affairs, Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan, 430223, People’s Republic of China
Ming Jiang
Affiliation:
Key Laboratory of Freshwater Biodiversity Conservation, the Ministry of Agriculture and Rural Affairs, Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan, 430223, People’s Republic of China
Weihua Gao
Affiliation:
College of Animal Science, Yangtze University, Jingzhou, People’s Republic of China
Xing Lu
Affiliation:
Key Laboratory of Freshwater Biodiversity Conservation, the Ministry of Agriculture and Rural Affairs, Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan, 430223, People’s Republic of China
Wenbing Zhang
Affiliation:
College of Animal Science, Yangtze University, Jingzhou, People’s Republic of China
Hua Wen*
Affiliation:
Key Laboratory of Freshwater Biodiversity Conservation, the Ministry of Agriculture and Rural Affairs, Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan, 430223, People’s Republic of China
*
*Corresponding author: Dr H. Wen, fax +86 27 81780157, email wenhua.hb@163.com
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Abstract

To assess the role of dietary creatine on myofibre characteristics and protein synthesis in muscle, we fed grass carp (Ctenopharyngodon idellus, initial body weight: 88·47 ± 1·44 g) creatine-supplemented diets (1·84, 5·91, 8·48 and 15·44 g/kg diet) for 8 weeks. Creatine supplementation did not affect growth performance, but significantly increased creatine contents in muscle and liver. At 8·48 g/kg, creatine decreased the activities of alanine transaminase and aspartate aminotransferase in serum and improved hardness and chewiness of muscle due to shorter myofibre mean diameter, higher myofibre density and the frequencies of the diameters of classes I and III and collagen content, longer sarcomere length and upregulated mRNA levels of slow myosin heavy chains. Creatine supplementation upregulated the mRNA expressions of myogenic regulatory factors. The 8·48 g/kg creatine-supplemented diet significantly increased the contents of protein, total amino acids (AA), essential AA and free flavour AAs in muscle, the protein levels of insulin-like growth factor I, myogenic differentiation antigen and PPAR-γ coactlvator-1α in muscle and stimulated the phosphorylation of target of rapamycin (TOR) pathway in muscle. In summary, 8·48 mg/kg creatine improved fish health and skeletal muscle growth and increased hardness and protein synthesis in muscle of grass carp by affecting myofibre characteristics and the TOR signalling pathway. A second-order regression model revealed that the optimal dietary creatine supplementation of grass carp ranges between 8·48 and 12·04 g/kg.

Keywords

CreatineGrass carpFlesh qualityMyofibreTOR
Type
Research Article
Information
British Journal of Nutrition , Volume 130 , Issue 2 , 28 July 2023 , pp. 185 - 201
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Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Nutrition Society

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References

Thurstan, RH & Roberts, CM (2014) The past and future of fish consumption: can supplies meet healthy eating recommendations? Mar Pollut Bull 89, 5–11.CrossRefGoogle ScholarPubMed
Wang, Q, Cheng, L, Liu, J, et al. (2015) Freshwater aquaculture in PR China: trends and prospects. Rev Aquacult 7, 283–302.CrossRefGoogle Scholar
FAO (2020) The State of World Fisheries and Aquaculture 2020. Rome: FAO.Google Scholar
Ashraf, M, Zafar, A, Rauf, A, et al. (2011) Nutritional values of wild and cultivated silver carp (Hypophthalmichthys molitrix) and grass carp (Ctenopharyngodon idella). Int J Agric Biol 13, 1560–8530.Google Scholar
Choi, YM & Kim, BC (2009) Muscle fiber characteristics, myofibrillar protein isoforms, and meat quality. Livest Sci 122, 105–118.CrossRefGoogle Scholar
Lie, Ø (2001) Flesh quality – the role of nutrition. Aquacult Res 32, 341–348.CrossRefGoogle Scholar
Ayoola, MO (2016) Application of Dietary Bentonite Clay as Feed Addictive on Feed Quality, Water Quality and Production Performance of African Catfish (Clarias gariepinus). Stellenbosch: Stellenbosch University.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, 91–99.CrossRefGoogle ScholarPubMed
Alami-Durante, H, Wrutniak-Cabello, C, Kaushik, SJ, et al. (2010) Skeletal muscle cellularity and expression of myogenic regulatory factors and myosin heavy chains in rainbow trout (Oncorhynchus mykiss): effects of changes in dietary plant protein sources and amino acid profiles. Comp Biochem Physiol A Mol Integr Physiol 156, 561–568.CrossRefGoogle ScholarPubMed
Negro, M, Avanzato, I & D’Antona, G (2019) Creatine in skeletal muscle physiology. In Nonvitamin and Nonmineral Nutritional Supplements, pp. 59–68 [Nabavi, SM and Silva, AS, editors]. London: Academic Press.Google Scholar
Gualano, B, Artioli, GG, Poortmans, JR, et al. (2010) Exploring the therapeutic role of creatine supplementation. Amino Acids 38, 31–44.CrossRefGoogle ScholarPubMed
Mcfarlane, WJ, Heigenhauser, G & Mcdonald, DG (2001) Creatine supplementation affects sprint endurance in juvenile rainbow trout. Comp Biochem Physiol A Mol Integr Physiol 130, 857–866.CrossRefGoogle ScholarPubMed
Cheng, X, Li, M, Leng, X, et al. (2021) Creatine improves the flesh quality of Pacific white shrimp (Litopenaeus vannamei) reared in freshwater. Food Chem 354, 129498.CrossRefGoogle ScholarPubMed
Cunha, MP, Budni, J, Ludka, FK, et al. (2016) Involvement of PI3K/Akt signaling pathway and its downstream intracellular targets in the antidepressant-like effect of creatine. Mol Neurobiol 53, 2954–2968.CrossRefGoogle ScholarPubMed
Aguiar, AF, Aguiar, DH, Felisberto, AD, et al. (2010) Effects of creatine supplementation during resistance training on myosin heavy chain (MHC) expression in rat skeletal muscle fibers. J Strength Cond Res 24, 88–96.CrossRefGoogle ScholarPubMed
Ceddia, RB & Sweeney, G (2004) Creatine supplementation increases glucose oxidation and AMPK phosphorylation and reduces lactate production in L6 rat skeletal muscle cells. J Physiol 555, 409–421.CrossRefGoogle ScholarPubMed
Morita, M, Gravel, SP, Hulea, L, et al. (2015) mTOR coordinates protein synthesis, mitochondrial activity and proliferation. Cell Cycle 14, 473–480.CrossRefGoogle ScholarPubMed
Ramos-Pinto, L, Lopes, G, Sousa, V, et al. (2019) Dietary creatine supplementation in gilthead seabream (Sparus aurata) increases dorsal muscle area and the expression of myod1 and capn1 genes. Front Endocrinol 10, 161.CrossRefGoogle ScholarPubMed
Schrama, D, Cerqueira, M, Raposo, CS, et al. (2018) Dietary creatine supplementation in gilthead seabream (Sparus aurata): comparative proteomics analysis on fish allergens, muscle quality, and liver. Front Physiol 9, 1844.CrossRefGoogle ScholarPubMed
Burns, AF & Gatlin, DM III (2019) Dietary creatine requirement of red drum (Sciaenops ocellatus) and effects of water salinity on responses to creatine supplementation. Aquaculture 506, 320–324.CrossRefGoogle Scholar
Zhao, HH, Xia, JG, Zhang, X, et al. (2018) Diet affects muscle quality and growth traits of grass carp (Ctenopharyngodon idellus): a comparison between grass and artificial feed. Front Physiol 9, 283.CrossRefGoogle ScholarPubMed
NRC (2011) Nutrient Requirements of Fish and Shrimp. Washington, DC: National Academies Press.Google Scholar
Du, Z-Y, Liu, Y-J, Tian, L-X, et al. (2006) The influence of feeding rate on growth, feed efficiency and body composition of juvenile grass carp (Ctenopharyngodon idella). Aquacult Int 14, 247–257.CrossRefGoogle Scholar
AOAC (2005) Official Methods of Analysis, 18th ed. Arlington, VA: AOAC.Google Scholar
Zhang, KK, Ai, QH, Mai, KS, et al. (2013) Effects of dietary hydroxyproline on growth performance, body composition, hydroxyproline and collagen concentrations in tissues in relation to prolyl 4-hydroxylase α(I) gene expression of juvenile turbot, Scophthalmus maximus L. fed high plant protein diets. Aquaculture 404–405, 77–84.CrossRefGoogle Scholar
Wu, F, Wen, H, Tian, J, et al. (2018) Effect of stocking density on growth performance, serum biochemical parameters, and muscle texture properties of genetically improved farm tilapia, Oreochromis niloticus . Aquacult Int 26, 1247–1259.CrossRefGoogle Scholar
Nihei, Y, Kobiyama, A, Ikeda, D, et al. (2006) Molecular cloning and mRNA expression analysis of carp embryonic, slow and cardiac myosin heavy chain isoforms. J Exp Biol 209, 188.CrossRefGoogle ScholarPubMed
Shi, XC, Jin, A, Sun, J, et al. (2018) The protein-sparing effect of α-lipoic acid in juvenile grass carp, Ctenopharyngodon idellus: effects on lipolysis, fatty acid β-oxidation and protein synthesis. Br J Nutr 120, 977–987.CrossRefGoogle ScholarPubMed
Tian, J, Lu, X, Jiang, M, et al. (2020) AMPK activation by dietary AICAR affects the growth performance and glucose and lipid metabolism in juvenile grass carp. Aquacult Nutr 26, 3–14.CrossRefGoogle Scholar
Borchel, A, Verleih, M, Rebl, A, et al. (2014) Creatine metabolism differs between mammals and rainbow trout (Oncorhynchus mykiss). SpringerPlus 3, 510.CrossRefGoogle ScholarPubMed
Wagner, T & Congleton, J (2011) Blood chemistry correlates of nutritional condition, tissue damage, and stress in migrating juvenile Chinook salmon (Oncorhynchus tshawytscha). Can J Fish AquatSci 61, 1066–1074.CrossRefGoogle Scholar
Ohgo, H, Yokoyama, H, Hirose, H, et al. (2009) Significance of ALT/AST ratio for specifying subjects with metabolic syndrome in its silent stage. Diabetes Metab Syndr 3, 3–6.CrossRefGoogle Scholar
da Silva, RP, Leonard, K-A & Jacobs, RL (2017) Dietary creatine supplementation lowers hepatic triacylglycerol by increasing lipoprotein secretion in rats fed high-fat diet. J Nutr Biochem 50, 46–53.CrossRefGoogle ScholarPubMed
Brosnan, ME & Brosnan, JT (2016) The role of dietary creatine. Amino Acids 48, 1785–1791.Google ScholarPubMed
Ejiofor, E, Ebhohon, S & Ndukaku, OY (2015) Effect of fermented and unfermented cocoa bean on some liver enzymes, creatinine and antioxidant in wistar albino rats. Carpathian J Food Sci Technol 7, 132–138.Google Scholar
James, BW, Goodband, RD, Unruh, JA, et al. (2002) A review of creatine supplementation and its potential to improve pork quality. J Appl Anim Res 21, 1–16.CrossRefGoogle Scholar
Johnston, IA (1999) Muscle development and growth: potential implications for flesh quality in fish. Aquaculture 177, 99–115.CrossRefGoogle Scholar
Lin, WL, Zeng, QX & Zhu, ZW (2009) Different changes in mastication between crisp grass carp (Ctenopharyngodon idellus C.et V) and grass carp (Ctenopharyngodon idellus) after heating: The relationship between texture and ultrastructure in muscle tissue. Food Res Int 42, 271–278.CrossRefGoogle Scholar
Periago, MJ, Ayala, MD, López-Albors, O, et al. (2005) Muscle cellularity and flesh quality of wild and farmed sea bass, Dicentrarchus labrax L . Aquaculture 249, 175–188.CrossRefGoogle Scholar
Sun, WT, Xu, XY, Li, XQ, et al. (2018) Effects of dietary geniposidic acid on growth performance, flesh quality and collagen gene expression of grass carp, Ctenopharyngodon idella . Aquacult Nutr 24, 1112–1121.CrossRefGoogle Scholar
Hurling, R, Rodell, JB & Hunt, HD (1996) Fiber diameter and fish texture. J Texture Stud 27, 679–685.CrossRefGoogle Scholar
Listrat, A, Lebret, B, Louveau, I, et al. (2016) How muscle structure and composition influence meat and flesh quality. Sci World J 2016, 1–14.CrossRefGoogle ScholarPubMed
Guzek, D, Głąbski, K, Głąbska, D, et al. (2012) Comparison of sarcomere length for two types of meat from animal family Suidae–analysis of measurements carried out by microscopic technique. Adv Sci Technol Res J 6, 13–17.CrossRefGoogle Scholar
Wei, YL, Li, BX, Xu, HG, et al. (2020) Fish protein hydrolysate in diets of turbot affects muscle fibre morphometry, and the expression of muscle growth-related genes. Aquacult Nutr 26, 1780–1791.CrossRefGoogle Scholar
Ertbjerg, P & Puolanne, E (2017) Muscle structure, sarcomere length and influences on meat quality: a review. Meat Sci 132, 139–152.CrossRefGoogle ScholarPubMed
Medler, S & Mykles, DL (2015) Muscle structure, fiber types, and physiology. Nat Hist Crust 4, 103–133.Google Scholar
Mònica, RF, Laura, A, Vanesa, JA, et al. (2011) Differential effects on proliferation of GH and IGFs in sea bream (Sparus aurata) cultured myocytes. Gen Comp Endocrinol 172, 44–49.Google Scholar
Kraemer, WJ, Luk, HY, Lombard, JR, et al. (2013) Physiological basis for creatine supplementation in skeletal muscle. In Nutrition and Enhanced Sports Performance, pp. 385–394 [Bagchi, D, Nair, S and Sen, CK, editors]. San Diego: Academic Press.CrossRefGoogle Scholar
Willoughby, DS & Rosene, JM (2003) Effects of oral creatine and resistance training on myogenic regulatory factor expression. Med Sci Sports Exerc 35, 923.CrossRefGoogle ScholarPubMed
Nikolić, N, Rhedin, M, Rustan, AC, et al. (2012) Overexpression of PGC-1α increases fatty acid oxidative capacity of human skeletal muscle cells. Biochem Res Int 2012, 714074.CrossRefGoogle ScholarPubMed
Louis, M, Van Beneden, R, Dehoux, M, et al. (2004) Creatine increases IGF-I and myogenic regulatory factor mRNA in C2C12 cells. FEBS Lett 557, 243–247.CrossRefGoogle Scholar
Liang, HL, Ren, MC, Habte-Tsion, HM, et al. (2016) Dietary arginine affects growth performance, plasma amino acid contents and gene expressions of the TOR signaling pathway in juvenile blunt snout bream, Megalobrama amblycephala . Aquaculture 461, 1–8.Google Scholar
Azizi, S, Nematollahi, MA, Mojazi Amiri, B, et al. (2016) Lysine and leucine deficiencies affect myocytes development and IGF signaling in gilthead sea bream (Sparus aurata). PLOS ONE 11, E0147618.Google ScholarPubMed
Um, SH, D’Alessio, D & Thomas, G (2006) Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab 3, 393–402.CrossRefGoogle ScholarPubMed
Mohanty, B, Mahanty, A, Ganguly, S, et al. (2014) Amino acid compositions of 27 food fishes and their importance in clinical nutrition. J Amino Acids 2014, 269797.CrossRefGoogle ScholarPubMed
Li, P, Mai, KS, Trushenski, J, et al. (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37, 43–53.CrossRefGoogle ScholarPubMed
Sarma, D, Akhtar, MS, Das, P, et al. (2013) Nutritional quality in terms of amino acid and fatty acid of five coldwater fish species: implications to human health. Natl Acad Sci Lett 36, 385–391.CrossRefGoogle Scholar
Hong, H, Regenstein, JM & Luo, Y (2017) The importance of ATP-related compounds for the freshness and flavor of post-mortem fish and shellfish muscle: a review. Crit Rev Food Sci Nutr 57, 1787–1798.Google 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.CrossRefGoogle Scholar
Wallimann, T, Wyss, M, Brdiczka, D, et al. (1992) Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the ‘phosphocreatine circuit’ for cellular energy homeostasis. Biochem J 281, 21–40.CrossRefGoogle ScholarPubMed
Speer, O, Neukomm, L, Murphy, R, et al. (2004) Creatine transporters: a reappraisal. Mol Cell Biochem 256–257, 407–424.CrossRefGoogle Scholar