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Interactions between dietary carbohydrate and thiamine: implications on the growth performance and intestinal mitochondrial biogenesis and function of Megalobrama amblycephala

Published online by Cambridge University Press:  22 March 2021

Chao Xu
Affiliation:
College of Marine Sciences, South China Agricultural University, Guangzhou510642, People’s Republic of China
Yuan-You Li
Affiliation:
College of Marine Sciences, South China Agricultural University, Guangzhou510642, People’s Republic of China
Paul B. Brown
Affiliation:
Purdue University, Department of Forestry and Natural Resources, West Lafayette, IN, 47907, USA
Wen-Bin Liu
Affiliation:
Key Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, Nanjing210095, People’s Republic of China
Liu-Ling Gao
Affiliation:
College of Marine Sciences, South China Agricultural University, Guangzhou510642, People’s Republic of China
Zhi-Rong Ding
Affiliation:
College of Marine Sciences, South China Agricultural University, Guangzhou510642, People’s Republic of China
Xiang-Fei Li*
Affiliation:
Key Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, Nanjing210095, People’s Republic of China
Di-Zhi Xie*
Affiliation:
College of Marine Sciences, South China Agricultural University, Guangzhou510642, People’s Republic of China
*
*Corresponding authors: Xiang-Fei Li, email xfli@njau.edu.cn; Di-Zhi Xie, email xiedizhi@scau.edu.cn
*Corresponding authors: Xiang-Fei Li, email xfli@njau.edu.cn; Di-Zhi Xie, email xiedizhi@scau.edu.cn

Abstract

A12-week experiment was conducted to evaluate the influences of thiamine ongrowth performance, and intestinal mitochondrial biogenesis and function of Megalobramaamblycephala fed a high-carbohydrate (HC) diet. Fish (24·73 (sem 0·45) g) were randomly assigned to one of four diets: two carbohydrate (CHO) levels (30 and 45 %) and two thiamine levels (0 and 1·5 mg/kg). HC diets significantly decreased DGC, GRMBW, FIMBW, intestinal activities of amylase, lipase, Na+, K+-ATPase, CK, complexes I, III and IV, intestinal ML, number of mitochondrial per field, ΔΨm, the P-AMPK: T-AMPK ratio, PGC-1β protein expression as well as the transcriptions of AMPKα1, AMPKα2, PGC-1β, mitochondrial transcription factor A, Opa-1, ND-1 and COX-1 and 2, while the opposite was true for ATP, AMP and reactive oxygen species, and the transcriptions of dynamin-related protein-1, fission-1 and mitochondrial fission factor. Dietarythiamine concentrations significantly increased DGC, GRMBW, intestinal activities of amylase, Na+, K+-ATPase, CK, complexes I and IV, intestinal ML, number of mitochondrial per field, ΔΨm, the P-AMPK:T-AMPK ratio, PGC-1β protein expression as well as the transcriptions of AMPKα1, AMPKα2, PGC-1β, Opa-1, ND-1, COX-1 and 2, SGLT-1 and GLUT-2. Furthermore, a significant interaction between dietary CHO and thiamine was observed in DGC, GRMBW, intestinal activities of amylase, CK, complexes I and IV, ΔΨm, the AMP:ATP ratio, the P-AMPK:T-AMPK ratio, PGC-1β protein expression as well as the transcriptions of AMPKα1, AMPKα2, PGC-1β, Opa-1, COX-1 and 2, SGLT-1 and GLUT-2. Overall, thiamine supplementation improved growth performance, and intestinal mitochondrial biogenesis and function of M. amblycephala fed HC diets.

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Full Papers
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of The Nutrition Society

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References

Hemre, GI, Mommsen, TP & Krogdahl, A (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8, 175194.CrossRefGoogle Scholar
Enes, P, Panserat, S, Kaushik, S, et al. (2009) Nutritional regulation of hepatic glucose metabolism in fish. Fish Physiol Biochem 35, 519539.CrossRefGoogle ScholarPubMed
Kamalam, BS, Medale, F, Panserat, S, et al. (2017) Utilisation of dietary carbohydrates in farmed fishes: new insights on influencing factors, biological limitations and future strategies. Aquaculture 467, 327.CrossRefGoogle Scholar
Chen, X, Eslamfam, S, Fang, L, et al. (2017) Maintenance of gastrointestinal glucose homeostasis by the gut-brain axis. Curr Protein Pept Sci 18(6), 541547.CrossRefGoogle ScholarPubMed
Mithieux, G, Rajas, F & Gautier-Stein, A (2004) A novel role for glucose 6-phosphatase in the small intestine in the control of glucose homeostasis. J Biol Chem 279(43), 4423144234.CrossRefGoogle ScholarPubMed
Pi, DG, Liu, YL, Shi, HF, et al. (2014) Dietary supplementation of aspartate enhances intestinal integrity and energy status in weanling piglets after lipopolysaccharide challenge. J Nutr Biochem 25, 456462.CrossRefGoogle ScholarPubMed
Marcu, R, Zheng, Y & Hawkins, BJ (2017) Mitochondria and angiogenesis. Adv Exp Med Biol 982, 371406.CrossRefGoogle ScholarPubMed
Li, XF, Wang, BK, Xu, C, et al. (2019) Regulation of mitochondrial biogenesis and function by dietary carbohydrate levels and lipid sources in juvenile blunt snout bream Megalobrama amblycephala . Comp Biochem Physiol A Mol Integr Physiol 227, 1424.CrossRefGoogle Scholar
Tang, X, Luo, YX, Chen, HZ, et al. (2014) Mitochondria, endothelial cell function, and vascular diseases. Front Physiol 5, 175.CrossRefGoogle ScholarPubMed
Bartolák-Suki, E & Suki, B (2020) Tuning mitochondrial structure and function to criticality by fluctuation-driven mechanotransduction. Sci Rep 10, 407.CrossRefGoogle ScholarPubMed
Fogarty, S & Hardie, DG (2010) Development of protein kinase activators: AMPK as a target in metabolic disorders and cancer. Biochim Biophys Acta 1804, 581591.CrossRefGoogle ScholarPubMed
Leick, L, Fentz, J, Biensø, RS, et al. (2010) PGC-1α is required for aicar-induced expression of GLUT4 and mitochondrial proteins in mouse skeletal muscle. Am J Physiol-Endoc M 299, E456.Google ScholarPubMed
Lu, KL, Tomas, P, Song, XJ, et al. (2020) Molecular characterization of PGC-1β (PPAR coactivator 1β) and its roles in mitochondrial biogenesis in blunt snout bream (Megalobrama amblycephala). Int J Mol Sci 21, 1935.CrossRefGoogle Scholar
Bremer, K, Kocha, KM, Snider, T, et al. (2016) Sensing and responding to energetic stress: the role of the AMPK-PGC1a-NRF1 axis in control of mitochondrial biogenesis in fish. Comp Biochem Phys B Biochem Mol Biol 199, 412.CrossRefGoogle ScholarPubMed
Papa, S & Skulachev, VP (1997) Reactive oxygen species, mitochondria, apoptosis and aging. Mol Cell Biochem 174, 305309.CrossRefGoogle Scholar
Korshunov, SS, Korkina, OV, Ruuge, EK, et al. (1998) Fatty acids as natural uncouplers preventing generation of O2 and H2O2 by mitochondria in the resting state. FEBS Lett 435, 215218.CrossRefGoogle ScholarPubMed
Eya, JC, Ashame, MF & Pomeroy, CF (2010) Influence of diet on mitochondrial complex activity in channel catfish, Ictalurus punctatus . N Am J Aquac 72, 225236.CrossRefGoogle Scholar
Depeint, F, Bruce, WR, Shangari, N, et al. (2006) Mitochondrial function and toxicity: role of the B vitamin family on mitochondrial energy metabolism. Chem Biol Interact 163, 94112.CrossRefGoogle Scholar
Gangolf, M, Wins, P, Thiry, M, et al. (2010) Thiamine triphosphate synthesis in rat brain occurs in mitochondria and is coupled to the respiratory chain. J Biol Chem 285, 583594.CrossRefGoogle Scholar
Mehta, R, Shangari, N & O’Brien, PJ (2008) Preventing cell death induced by carbonyl stress, oxidative stress or mitochondrial toxins with vitamin B anti-AGE agents. Mol Nutr Food Res 52, 379385.CrossRefGoogle ScholarPubMed
Huang, HH, Feng, L, Liu, Y, et al. (2011) Effects of dietary thiamin supplement on growth, body composition and intestinal enzyme activities of juvenile Jian carp (Cyprinus carpio var. Jian). Aquac Nutr 17, e233e240.CrossRefGoogle Scholar
Li, XF, Lu, KL, Liu, WB, et al. (2014) Effects of dietary lipid and carbohydrate and their interaction on growth performance and body composition of juvenile blunt snout bream, Megalobrama amblycephala . Isr J Aquacult Bamidgeh 66, 931.Google Scholar
Li, PF, Wang, Y, Jiang, GZ, et al. (2017) Effects of dietary thiamin levels on growth, hepatic thiamin contents and plasma biochemical indexes of juvenile blunt snout bream, Megalobrama amblycephala . Acta Hydrobiologica Sinica 4, 109113.Google Scholar
AOAC (1995) Official Methods of Analysis of Official Analytical Chemists International, 16th edn. Arlington, VA: Association of Official Analytical Chemists.Google Scholar
Nigam, VN (1962) An enzymatic method for the determination of pyruvate, phosphoenolpyruvate, 2- and 3-phosphoglyceric acids. Biochem Cell Biol 40, 836840.Google ScholarPubMed
Keppler, D, Decker, K (1974) Glycogen determination with amyloglucosidase. In Methods of Enzymatic Analysis, pp. 11271131 [Bergmeyer, HU, editor]. New York: Academic Press.Google Scholar
Folch, J, Lees, M & Sloane-Stanley, GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226, 497509.CrossRefGoogle ScholarPubMed
Merrifield, DL, Dimitroglou, A, Bradley, G, et al. (2009) Soybean meal alters autochthonous microbial populations, microvilli morphology and compromises intestinal enterocyte integrity of rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 32, 755766.CrossRefGoogle Scholar
Bradford, M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem 72, 248254.CrossRefGoogle Scholar
Bernfeld, P (1955) Amylase. In: Methods in Enzymology, pp. 149150, [Colowich, SP, editor]. New York: Academic Press.CrossRefGoogle Scholar
Iijima, N, Tanaka, S & Ota, Y (1998) Purification and characterization of bile salt-activated lipase from the hepatopancreas of red sea bream, Pagrus major . Fish Physiol Biochem 18, 5969.CrossRefGoogle Scholar
Gjellesvik, D, Lombardo, D & Walther, B (1992) Pancreatic bile salt dependent lipase from cod (Gadus morhua): purification and properties. Biochim Biophys Acta 1124, 123134.CrossRefGoogle ScholarPubMed
Mukhopadhyay, PK, Dehadrai, PV & Banerjee, SK (1978) Studies on intestinal protease: Isolation, purification and effect of dietary proteins on alkaline protease activity of the air-breathing fish, Clarias batrachus (Linn.). Hydrobiologia 57, 1115.CrossRefGoogle Scholar
Engstad, RE, Robertsen, B & Frivold, E (1992) Yeast glucan induces increase in lysozyme and complement-mediated haemolytic activity in Atlantic salmon blood. Fish Shellfish Immunol 2, 287297.CrossRefGoogle Scholar
Weng, CF, Chiang, CC, Gong, HY, et al. (2002) Acute changes in gill Na+, K+-ATPase and creatine kinase in response to salinity changes in the euryhaline teleost, tilapia (Oreochromis mossambicus). Physiol Biochem Zool 75, 2936.CrossRefGoogle Scholar
McCormick, SD (1993) Methods for nonlethal gill biopsy and measurement of Na+, K+-ATPase activity. Can J Fish Aquat Sci 50, 656658.CrossRefGoogle Scholar
Bergmeyer, HL (1983) Methods of Enzymatic Analysis. New York: Academic Press.Google Scholar
Adam, H (1965) Adenosine-5′-diphosphate and Adenosine-5′-monophosphate. Meth Enzymatic Anal 4, 573577.CrossRefGoogle Scholar
Liu, B, Cui, YT, Brown, PB, et al. (2015) Cytotoxic effects and apoptosis induction of enrofloxacin in hepatic cell line of grass carp (Ctenopharyngodon idellus). Fish Shellfish Immun 47, 639644.CrossRefGoogle Scholar
Bradford, HF & Dodd, PR (1977) Convulsions and activation of epileptic foci induced by monosodium glutamate and related compounds. Biochem Pharmacol 26, 253254.CrossRefGoogle ScholarPubMed
Jeejeebhoy, KN (2002) Nutritional assessment by measuring mitochondrial complex activity. United States Patent 6455243 (US Patent Issued accessed September 2002).Google Scholar
Kirby, DM, Thorburn, DR, Turnbull, DM, et al. (2007) Biochemical assays of respiratory chain complex activity. Methods Cell Biol 80, 93.CrossRefGoogle ScholarPubMed
Xu, C, Liu, WB, Remø, SC, et al. (2019) Feeding restriction alleviates high carbohydrate diet-induced oxidative stress and inflammation of Megalobrama amblycephala by activating the AMPK-SIRT1 pathway. Fish Shellfish Immun 92, 637648.CrossRefGoogle ScholarPubMed
Xu, C, Liu, WB, Zhang, DD, et al. (2018) Interactions between dietary carbohydrate and metformin: implications on energy sensing, insulin signaling pathway, glycolipid metabolism and glucose tolerance in blunt snout bream Megalobrama amblycephala . Aquaculture 483, 183195.CrossRefGoogle Scholar
Tang, R, Dodd, A, Lai, D, et al. (2007) Validation of Zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochim Biophys Sinica 39, 384390.CrossRefGoogle ScholarPubMed
Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2−ΔΔCt method. Methods 25, 402408.CrossRefGoogle Scholar
Gao, ZX, Luo, W, Liu, H, et al. (2012) Transcriptome analysis and SSR/SNP markers information of the blunt snout bream (Megalobrama amblycephala). PLOS ONE 7, e42637.CrossRefGoogle Scholar
Song, XJ, Samad, R, Zhou, WH, et al. (2019) Molecular characterization of peroxisome proliferator-activated receptor- coactivator-1α (PGC1α) and its role in mitochondrial biogenesis in blunt snout bream (Megalobrama amblycephala). Front Physiol 9, 1957.CrossRefGoogle Scholar
Lawn, RM, Efstratiadis, A, O’Connell, C, et al. (1980) The nucleotide sequence of the human β-globin gene. Cell 21, 647651.CrossRefGoogle ScholarPubMed
Sanchez-Muros, MJ, Garcia-Rejon, L & Lupianez, JA (1995) Long-term nutritional effects on the primary liver and kidney metabolism in rainbow trout, Oncorhynchus mykiss (Walbaum): adaptive response to a high-protein/non-carbohydrate diet and starvation of glucose 6-phosphate dehydrogenase activity. Aquac Nutr 1, 213220.CrossRefGoogle Scholar
Liu, M, Alimov, AP, Wang, H, et al. (2014) Thiamine deficiency induces anorexia by inhibiting hypothalamic AMPK. Neuroscience 267, 102113.CrossRefGoogle ScholarPubMed
Zakim, D, Pardini, RS, Herman, RH, et al. (1967) Mechanism for the differential effects of high carbohydrate diets on lipogenesis in rat liver. Biochim Biophys Acta 144, 242251.CrossRefGoogle ScholarPubMed
Babaei-Jadidi, R, Karachalias, N, Kupich, C, et al. (2004) High-dose thiamine therapy counters dyslipidaemia in streptozotocin-induced diabetic rats. Diabetologia 47, 22352246.CrossRefGoogle ScholarPubMed
Bakker, SJ, Hoogeveen, EK, Nijpels, G, et al. (1998) The association of dietary fibres with glucose tolerance is partly explained by concomitant intake of thiamine: the Hoorn Study. Diabetologia 41, 11681175.CrossRefGoogle ScholarPubMed
Moon, TW (2001) Glucose intolerance in teleost fish: fact or fiction? Comp Biochem Physiol B 129, 243249.CrossRefGoogle ScholarPubMed
Zhou, XQ, Zhao, CR & Lin, Y (2007) Compare the effect of diet supplementation with uncoated or coated lysine on juvenile Jian carp (Cyprinus carpio var. Jian). Aquacult Nutr 13, 457461.CrossRefGoogle Scholar
Suzer, C, Çoban, D, Kamaci, HO, et al. (2008) Lactobacillus spp. bacteria as probiotics in gilthead sea bream (Sparus aurata, L.) larvae: Effects on growth performance and digestive enzyme activities. Aquaculture 280, 140145.CrossRefGoogle Scholar
Tengjaroenkul, B, Smith, BJ, Caceci, T, et al. (2000) Distribution of intestinal enzyme activities along the intestinal tract of cultured Nile tilapia, Oreochromis niloticus L. Aquaculture 182, 317327.CrossRefGoogle Scholar
Wallimann, T & Hemmer, W (1994) Creatine-kinase in nonmuscle tissues and cells. Mol Cell Biochem 133, 193220.CrossRefGoogle Scholar
Harpaz, S, Hakim, Y, Barki, A, et al. (2005) Effects of different feeding levels during day and/or night on growth and brush-border enzyme activity in juvenile Lates calcarifer reared in freshwater re-circulating tanks. Aquaculture 248, 325335.CrossRefGoogle Scholar
Garcia-Berumen, CI, Alejandre-Buitron, A, Montoya-Perez, R, et al. (2016) Differential effects of diets rich in fats, carbohydrates and/or fructose on the development of hepatic steatosis and mitochondrial dysfunction. FASEB J 30, 1100.111100.11.Google Scholar
Roder, PV, Geillinger, KE, Zietek, TS, et al. (2014) The role of SGLT1 and GLUT2 in intestinal glucose transport and sensing. PLOS ONE 9, e89977.CrossRefGoogle Scholar
Chen, L, Huang, J, Li, XC, et al. (2019) High-glucose induced mitochondrial dynamics disorder of spinal cord neurons in diabetic rats and its effect on mitochondrial spatial distribution. Spine (Phila Pa 1976) 44, E715E722.CrossRefGoogle ScholarPubMed
Al-Kafaji, G, Sabry, MA & Skrypnyk, C (2016) Time-course effect of high-glucose-induced reactive oxygen species on mitochondrial biogenesis and function in human renal mesangial cells. Cell Biol Int 40, 3648.CrossRefGoogle ScholarPubMed
Kroemer, G (2003) Mitochondrial control of apoptosis: an introduction. Biochem Biophys Res Commun 304, 433435.CrossRefGoogle ScholarPubMed
Miranda, N, Tovar, AR, Palacios, B, et al. (2007) AMPK as a cellular energy sensor and its function in the organism. Rev Invest Clin 59, 458469.Google ScholarPubMed
Nesci, S, Ventrella, V, Trombetti, F, et al. (2014) Thiol oxidation of mitochondrial F0-c subunits: a way to switch off antimicrobial drug targets of the mitochondrial ATP synthase. Med Hypotheses 83, 160165.CrossRefGoogle ScholarPubMed
Marín-García, J, Akhmedov, AT (2016) Mitochondrial dynamics and cell death inheart failureHeart Fail Rev 21, 123136.CrossRefGoogle Scholar
Schmid, SL & Frolov, VA (2011) Dynamin: functional design of a membrane fission catalyst. Annu Rev Cell Dev Biol 27, 79105.CrossRefGoogle ScholarPubMed
Rutter, GA & Leclerc, I (2009) The AMP-regulated kinase family: enigmatic targets for diabetes therapy. Mol Cell Endocrinol 297, 4149.CrossRefGoogle ScholarPubMed
Zhuang, XY, Maimaitijiang, A, Li, Y, et al. (2017) Salidroside inhibits high-glucose-induced proliferation of vascular smooth muscle cells via inhibiting mitochondrial fission and oxidative stress. Exp Ther Med 14, 515524.CrossRefGoogle ScholarPubMed
Wu, Z, Puigserver, P, Andersson, U, et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115124.CrossRefGoogle ScholarPubMed
Lin, Z, Xue, YM, Sha, JP, et al. (2009) High glucose impairs mitochondrial respiratory chain function in pancreatic beta cells. J South Med Univ 29, 1251.Google ScholarPubMed
Zhou, J, Sun, A & Xing, D (2013) Modulation of cellular redox status by thiamine-activated NADPH oxidase confers Arabidopsis resistance to Sclerotinia sclerotiorum . J Exp Bot 64, 32613272.CrossRefGoogle ScholarPubMed
Eya, JC, Ashame, MF, Pomeroy, CF, et al. (2012) Genetic variation in feed consumption, growth, nutrient utilization efficiency and mitochondrial function within a farmed population of channel catfish (Ictalurus punctatus). Comp Biochem Physiol B Biochem Mol Biol 163, 211220.CrossRefGoogle Scholar
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