Abstract
Lipoic acid (LA) is an antioxidant that also favors glucose uptake in mammals. Until now, there are no studies evaluating the potential effect of this molecule on glycemic control in fish. It was evaluated LA effects on glucose uptake in common carp Cyprinus carpio fed with carbohydrate diets from two carbohydrate sources: glucose (GLU) and starch (STA), and supplemented or not with LA, being the diets: +GLU/−LA (GLU); +GLU/+LA (GLU + LA); +STA/−LA (STA); and +STA/+LA (STA + LA). Carp juveniles (6.5 ± 0.1 g) were fed with each diet ad libitum 4 times a day, during 68 days. Muscle glycogen concentration was higher (p < 0.05) in GLU and GLU + LA than in STA and STA + LA groups. On fish fed with starch, muscle cholesterol and triglyceride concentrations were higher (p < 0.05) in fish fed diets supplemented with LA. Muscle protein levels were higher in fish fed with LA, independent of the diet carbohydrate source. Lipid peroxidation was significantly reduced (p < 0.05) in fish muscle on fish fed the STA + LA diets when compared with the STA diet. Our findings indicate that LA modulates lipid, proteins and carbohydrate metabolism together with the well-known antioxidant effect. Also, LA showed to enhance starch utilization taking into account muscle cholesterol and triglyceride levels.
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References
Amado LL, Garcia ML, Ramos PB, Yunes JS, Monserrat JM (2011) Influence of a toxic Microcystis aeruginosa strain on glutathione synthesis and glutathione-S-transferase activity in common carp Cyprinus carpio (Teleostei: Cyprinidae). Arch Environ Contam Toxicol 60:319–326
Association of the Official Analytical Chemists (AOAC) (1995) Official methods of analysis of the association of the official analytical chemists international, 16th edn. AOAC International, Arlington
Bauer W, Prentice-Hernandez C, Tesser MB, Wasielesky W, Poersch LHS (2012) Substitution of fish meal with microbial floc meal and soy protein concentrate in diets for the pacific white shrimp Litopenaeus vannamei. Aquaculture 342–343:112–116
Baynes JW, Thorpe SR (1999) Perspectives in diabetes—role of oxidative stress in diabetic complications. A new perspective on an old paradigm. Diabetes 48:1–10
Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820
Busserolles J, Rock E, Gueux E, Mazur A, Grolier P, Rayssiguier Y (2002) Short-term consumption of a high-sucrose diet has a pro-oxidant effect in rats. Br J Nutr 87:337–342
Carr RS, Neff JM (1984) Quantitative semiautomated enzymatic assay for tissue glycogen. Comp Biochem Physiol B 77:447–449
Castillo J, Codina M, Martínez ML, Navarro I, Martı L (2004) Metabolic and mitogenic effects of IGF-I and insulin on muscle cells of rainbow trout. Am J Physiol Regul Integr Comp Physiol 286:R935–R941
Coleman MD, Eason RC, Bailey CJ (2001) The therapeutic use of lipoic acid in diabetes: a current perspective. Environ Toxicol Pharmacol 10:167–172
Da Rocha AM, De Freitas DPS, Burns M, Vieira JP, de La Torre FR, Monserrat JM (2009) Seasonal and organ variations in antioxidant capacity, detoxifying competence and oxidative damage in freshwater and estuarine fishes from Southern Brazil. Comp Biochem Physiol C 150:512–520
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
Erfanullah, Jafri AK (1995) Protein-sparing effect of dietary carbohydrate in diets for fingerling Labeo rohita. Aquaculture 136:331–339
Estrada E, Ewart HH, Tsakiridis T, Volchuk A, Ramlal T, Tritschler H, Klip A (1996) Stimulation of glucose uptake by the natural co-enzyme α-lipoic acid/thioctic acid: participation of elements of the insulin signaling pathway. Diabetes 45:1798–1804
Food and Agriculture Organization of the United Nations (2014) The state of word fisheries and aquaculture- Opportunities and challenges. FAO, Rome
Furuichi M, Yone Y (1982) Availability of carbohydrate in nutrition of carp and red sea bream. Bull Jpn Soc Sci 48:945–948
Furuichi M, Taira H, Yone Y (1986) Availability of carbohydrate in nutrition of yellowtail. Bull Jpn Soc Sci 52:99–102
Haugaard N, Haugaard ES (1970) Stimulation of glucose utilization by thioctic acid in rat diaphragm incubated in vitro. Biochim Biophys Acta 222:583–586
Hemre G-I, Mommsen TP, Krogdahl A (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8:175–194
Henriksen EJ, Jacob S, Streeper RS, Fogtl DL, Hokama JY, Tritschler HJ (1997) Stimulation by alpha-lipoic acid of glucose transport activity in sketetal muscle of lean and obese zucker rats. Life Sci 61:805–812
Henry RR, Crapo PA, Thorburn AW (1991) Current issues in fructose metabolism. Ann Rev Nutr 11:21–39
Kaushik SJ (1995) Nutrient requirements, supply and utilization in the context of carp culture. Aquaculture 129:225–241
Kütter MT, Monserrat JM, Primel EG, Caldas SS, Tesser MB (2012) Effects of dietary α -lipoic acid on growth, body composition and antioxidant status in the Plata pompano Trachinotus marginatus (Pisces, Carangidae). Aquaculture 368–369:29–35
Kütter MT, Romano LA, Ventura-Lima J, Tesser MB, Monserrat JM (2014) Antioxidant and toxicological effects elicited by alpha-lipoic acid in aquatic organisms. Comp Biochem Physiol C 162:70–76
Laiz-Carrión R, Viana IR, Cejas JR, Ruiz-Jarabo I, Jerez S, Martos JA, Eduardo AB, Mancera JM (2012) Influence of food deprivation and high stocking density on energetic metabolism and stress response in red porgy, Pagrus pagrus L. Aquac Int 20:585–599
Lee S, Kim K, Lall SP (2003) Utilization of glucose, maltose, dextrin and cellulose by juvenile flounder (Paralichthys olivaceus). Aquaculture 221:427–438
Li JN, Xu CA, Wang LS, Wang ZG, Zhao ZG, Luo L (2016) Effects of dietary glucose and starch levels on the growth, haemotological indices and hepatic hexoquinase and glucokinase mRNA expression of juvenile mirror carp (Cyprinus carpio). Aquac Nutr 22:550–558
Lund SG, Phillips MCL, Moyes CD, Tufts BL (2000) The effects of cell ageing on protein synthesis in rainbow trout (Oncorhynchus mykiss) red blood cells. J Exp Biol 203:2219–2228
Martins ACS, Flores JA, Wasiliesky W Jr, Zanette J, Primel EG, Caldas SS, Monserrat JM (2014) Modulation of antioxidant and detoxification responses induced by lipoic acid in the Pacific white shrimp Litopenaeus vannamei (Boone, 1931) subjected to hypoxia and re-oxygenation. Mar Freshw Behav Physiol 47:335–348
Mommsen TP, Plisetskaya EM (1991) Insulin in fishes and agnathans: history, structure and metabolic regulation. Rev Aquat Sci 4:225–259
Monserrat JM, Ventura JL, Ferreira R, Acosta D, Garcia ML, Ramos PB, Moraes TB, Dos-Santos LC, Amado LL (2008) Modulation of antioxidant and detoxification responses mediated by lipoic acid in the fish Corydoras paleatus (Callychthyidae). Comp Biochem Physiol C 148:287–292
Moon TW (2001) Glucose intolerance in teleost fish: fact or fiction? Comp Biochem Physiol B 129:243–249
Murai T, Akiyama T, Nose T (1983) Effects of glucose chain length of various carbohydrates and frequency of feeding on their utilization by fingerling carp. Bull Jpn Soc Sci Fish 49:1607–1611
Nery LEM, Santos EA (1993) Carbohydrate metabolism during osmoregulation in Chasmagnathus granulata Dana, 1851 (Crustacea, Decapoda). Comp Biochem Physiol B 106:747–753
Oakes KD, Van der Kraak GJ (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat Toxicol 63:447–463
Packer L, Witt EH, Tritschler HJ (1995) Alpha-lipoic acid as a biological antioxidant. Free Rad Biol Med 19:227–250
Park KH, Terjesen BF, Tesser MB, Portella MC, Dabrowski K (2006) α-Lipoic acid-enrichment partially reverses tissue ascorbic acid depletion in pacu (Piaractus mesopotamicus) fed vitamin C-devoid diets. Fish Physiol Biochem 32:329–338
Párrizas M, Plisetskaya EM, Planas J, Gutiérrez J (1995) Abundant insulin-like growth factor-1 (IGF-1) receptor binding in fish skeletal muscle. Gen Comp Endocrinol 98:16–25
Polakof S, Moon TW, Aguirre P, Skiba-Cassy S, Panserat S (2010) Effects of insulin infusion on glucose homeostasis and glucose metabolism in rainbow trout fed a high-carbohydrate diet. J Exp Biol 213:4151–4157
Rains JL, Jain SK (2011) Oxidative stress, insulin signaling, and diabetes. Free Rad Biol Med 50:567–575
Robert L, Narcy A, Rayssiguier Y, Mazur A, Rémésy C (2008) Lipid metabolism and antioxidant status in sucrose vs. potato-fed rats. J Am Coll Nutr 27:109–116
Sá R, Pousão P, Oliva-Teles A (2008) Effect of dietary starch source (normal versus waxy) and protein levels on the performance of white sea bream Diplodus sargus (Linnaeus) juveniles. Aquac Res 39:1069–1076
Salze G, Mclean E, Battle PR, Schwarz MH, Craig SR (2010) Use of soy protein concentrate and novel ingredients in the total elimination of fish meal and fish oil in diets for juvenile cobia, Rachycentron canadum. Aquaculture 298:294–299
Satpathy BB, Ray AK (2009) Effect of dietary protein and carbohydrate levels on growth, nutrient utilization and body composition in fingerling rohu, Labeo rohita (Hamilton). J Appl Ichthyol 25:728–733
Shay KP, Moreau RF, Smith EJ, Smith AR, Hagen TM (2009) Alpha-lipoic acid as a dietary supplement: molecular mechanisms and therapeutic potential. Biochim Biophys Acta 1790:1149–1160
Silink M, Mbanya J (2007) Global standardization of the HbA 1c assay: the consensus committee recommendations. Diabetes Voice 52:33–34
Takeuchi T, Satoh S, Kiron V (2002) Common carp, Cyprinus carpio. In: Webster CD, Lim C (eds) Nutrient requirements and feeding of finfish for aquaculture. CAB, New York, pp 245–261
Tan Q, Wang F, Xie S, Zhu X, Lei W, Shen J (2009) Effect of high dietary starch levels on the growth performance, blood chemistry and body composition of gibel carp (Carassius auratus var. gibelio). Aquac Res 40:1011–1018
Ufodike EBC, Matty AJ (1983) Growth responses and nutrient digesibility in mirror carp (Cyprinus carpio) fed different levels of cassava and rice. Aquaculture 31:41–50
Wilson RP (1994) Utilization of dietary carbohydrate by fish. Aquaculture 124:67–80
Yaworsky K, Somwar R, Ramlal T, Tritschler HJ, Klip A (2000) Engagement of the insulin-sensitive pathway in the stimulation of glucose transport by a-lipoic acid in 3T3-L1 adipocytes. Diabetologia 43:294–303
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 (Mugil liza Valenciennes 1836, Mugilidae). J Appl Ichthyol 29:1342–1347
Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, New Jersey
Ziegler D, Hanfeld M, Ruhnau KJ, Meibner HP, Lobisch M, Schutte K, Gries FA (1995) Treatment of symptomatic diabetic peripheral neuropathy with the anti-oxidant a-lipoic acid. A 3-week multicentre randomized controlled trial (ALADIN Study). Diabetologia 38:1425–1433
Acknowledgments
The authors would like to thank Dr. Ricardo Roubax Robaldo of Federal University of Pelotas (UFPel). The authors also thank Dr. Luis Alberto Romano, M.Sc. Paola Milena, MSc. Juan Zamora-Sillero, Dr. Eduardo Martins Silva and oxidative stress and toxicology research group (EAOx) for sampling and analysis contributions. J. M. Monserrat; E. Pimentel and Marcelo B. Tesser are research fellows from Brazilian agency CNPq (process numbers PQ 307880/2013-3, DT 311605/2009-5 and PQ 308680/2014-6, respectively). R. A. Santos received support from the Brazilian Council of Research, CNPq.
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Santos, R.A., Caldas, S., Primel, E.G. et al. Effects of lipoic acid on growth and biochemical responses of common carp fed with carbohydrate diets. Fish Physiol Biochem 42, 1699–1707 (2016). https://doi.org/10.1007/s10695-016-0250-2
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DOI: https://doi.org/10.1007/s10695-016-0250-2