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Published in: European Journal of Nutrition 6/2017

01-09-2017 | Original Contribution

Benefits of l-alanine or l-arginine supplementation against adiposity and glucose intolerance in monosodium glutamate-induced obesity

Authors: Thiago R. Araujo, Israelle N. Freitas, Jean F. Vettorazzi, Thiago M. Batista, Junia C. Santos-Silva, Maria L. Bonfleur, Sandra L. Balbo, Antonio C. Boschero, Everardo M. Carneiro, Rosane A. Ribeiro

Published in: European Journal of Nutrition | Issue 6/2017

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Abstract

Purpose

l-alanine (Ala) and l-arginine (Arg) have been reported to regulate pancreatic β-cell physiology and to prevent body fat accumulation in diet-induced obesity. Here, we assessed growth and adiposity parameters, glucose tolerance, insulin secretion and the expression of insulin and nutrient-regulated proteins in monosodium glutamate (MSG)-obese mice supplemented with either Ala or Arg.

Methods

Male newborn C57Bl/6 mice received a daily subcutaneous injection of MSG or saline solution (CTL group), during the first 6 days of life. From 30 to 90 days of age, MSG and CTL mice received or not 2.55 % Ala (CAla or MArg groups) or 1.51 % Arg-HCl (CArg or MArg groups) in their drinking water.

Results

Adult MSG mice displayed higher adiposity associated with lower phosphorylation of the adipogenic enzyme, ACC, in adipose tissue. Glucose intolerance in MSG mice was linked to lower insulin secretion and to lower expression of IRβ in adipose tissue, as well as AS160 phosphorylation in skeletal muscle. Perigonadal fat depots were smaller in Ala and Arg mice, while retroperitoneal fat pads were decreased by Ala supplementation only. Both Ala and Arg improved fed-state glycemia as well as IRβ and pAS160 content, but only Ala led to improved glucose tolerance and insulin secretion. Adipostatic signals were increased in MAla mice, as indicated by enhanced AMPK phosphorylation and pACC content in fat depots.

Conclusions

Ala supplementation led to more pronounced metabolic improvements compared to Arg, possibly due to suppression of lipogenesis through activation of the AMPK/ACC pathway.
Literature
3.
go back to reference Wu G, Morris SM Jr (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336(Pt 1):1–17CrossRef Wu G, Morris SM Jr (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336(Pt 1):1–17CrossRef
4.
go back to reference Popov D, Costache G, Georgescu A, Enache M (2002) Beneficial effects of l-arginine supplementation in experimental hyperlipemia-hyperglycemia in the hamster. Cell Tissue Res 308(1):109–120. doi:10.1007/s00441-001-0509-4 CrossRef Popov D, Costache G, Georgescu A, Enache M (2002) Beneficial effects of l-arginine supplementation in experimental hyperlipemia-hyperglycemia in the hamster. Cell Tissue Res 308(1):109–120. doi:10.​1007/​s00441-001-0509-4 CrossRef
5.
go back to reference 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(4):714–721 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(4):714–721
6.
go back to reference Jobgen W, 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(2):230–237. doi:10.3945/jn.108.096362 CrossRef Jobgen W, 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(2):230–237. doi:10.​3945/​jn.​108.​096362 CrossRef
7.
go back to reference Monti LD, Setola E, Lucotti PC, Marrocco-Trischitta MM, Comola M, Galluccio E, Poggi A, Mammi S, Catapano AL, Comi G, Chiesa R, Bosi E, Piatti PM (2012) Effect of a long-term oral l-arginine supplementation on glucose metabolism: a randomized, double-blind, placebo-controlled trial. Diabetes Obes Metab 14(10):893–900. doi:10.1111/j.1463-1326.2012.01615.x CrossRef Monti LD, Setola E, Lucotti PC, Marrocco-Trischitta MM, Comola M, Galluccio E, Poggi A, Mammi S, Catapano AL, Comi G, Chiesa R, Bosi E, Piatti PM (2012) Effect of a long-term oral l-arginine supplementation on glucose metabolism: a randomized, double-blind, placebo-controlled trial. Diabetes Obes Metab 14(10):893–900. doi:10.​1111/​j.​1463-1326.​2012.​01615.​x CrossRef
11.
go back to reference Smith PA, Sakura H, Coles B, Gummerson N, Proks P, Ashcroft FM (1997) Electrogenic arginine transport mediates stimulus-secretion coupling in mouse pancreatic beta-cells. J Physiol 499(3):625–635CrossRef Smith PA, Sakura H, Coles B, Gummerson N, Proks P, Ashcroft FM (1997) Electrogenic arginine transport mediates stimulus-secretion coupling in mouse pancreatic beta-cells. J Physiol 499(3):625–635CrossRef
12.
go back to reference Krause MS, McClenaghan NH, Flatt PR, de Bittencourt PI, Murphy C, Newsholme P (2011) l-arginine is essential for pancreatic beta-cell functional integrity, metabolism and defense from inflammatory challenge. J Endocrinol 211(1):87–97. doi:10.1530/JOE-11-0236 CrossRef Krause MS, McClenaghan NH, Flatt PR, de Bittencourt PI, Murphy C, Newsholme P (2011) l-arginine is essential for pancreatic beta-cell functional integrity, metabolism and defense from inflammatory challenge. J Endocrinol 211(1):87–97. doi:10.​1530/​JOE-11-0236 CrossRef
13.
go back to reference Leiss V, Flockerzie K, Novakovic A, Rath M, Schonsiegel A, Birnbaumer L, Schurmann A, Harteneck C, Nurnberg B (2014) Insulin secretion stimulated by l-arginine and its metabolite l-ornithine depends on Galphai2. Am J Physiol Endocrinol Metab 307(9):E800–E812. doi:10.1152/ajpendo.00337.2014 CrossRef Leiss V, Flockerzie K, Novakovic A, Rath M, Schonsiegel A, Birnbaumer L, Schurmann A, Harteneck C, Nurnberg B (2014) Insulin secretion stimulated by l-arginine and its metabolite l-ornithine depends on Galphai2. Am J Physiol Endocrinol Metab 307(9):E800–E812. doi:10.​1152/​ajpendo.​00337.​2014 CrossRef
14.
go back to reference Mullooly N, Vernon W, Smith DM, Newsholme P (2014) Elevated levels of branched-chain amino acids have little effect on pancreatic islet cells, but l-arginine impairs function through activation of the endoplasmic reticulum stress response. Exp Physiol 99(3):538–551. doi:10.1113/expphysiol.2013.077495 CrossRef Mullooly N, Vernon W, Smith DM, Newsholme P (2014) Elevated levels of branched-chain amino acids have little effect on pancreatic islet cells, but l-arginine impairs function through activation of the endoplasmic reticulum stress response. Exp Physiol 99(3):538–551. doi:10.​1113/​expphysiol.​2013.​077495 CrossRef
15.
go back to reference Prada PO, Hirabara SM, de Souza CT, Schenka AA, Zecchin HG, Vassallo J, Velloso LA, Carneiro E, Carvalheira JB, Curi R, Saad MJ (2007) L-glutamine supplementation induces insulin resistance in adipose tissue and improves insulin signalling in liver and muscle of rats with diet-induced obesity. Diabetologia 50(9):1949–1959. doi:10.1007/s00125-007-0723-z CrossRef Prada PO, Hirabara SM, de Souza CT, Schenka AA, Zecchin HG, Vassallo J, Velloso LA, Carneiro E, Carvalheira JB, Curi R, Saad MJ (2007) L-glutamine supplementation induces insulin resistance in adipose tissue and improves insulin signalling in liver and muscle of rats with diet-induced obesity. Diabetologia 50(9):1949–1959. doi:10.​1007/​s00125-007-0723-z CrossRef
16.
go back to reference Freudenberg A, Petzke KJ, Klaus S (2013) Dietary l-leucine and l-alanine supplementation have similar acute effects in the prevention of high-fat diet-induced obesity. Amino Acids 44(2):519–528. doi:10.1007/s00726-012-1363-2 CrossRef Freudenberg A, Petzke KJ, Klaus S (2013) Dietary l-leucine and l-alanine supplementation have similar acute effects in the prevention of high-fat diet-induced obesity. Amino Acids 44(2):519–528. doi:10.​1007/​s00726-012-1363-2 CrossRef
17.
go back to reference McClenaghan NH, Barnett CR, Flatt PR (1998) Na+ cotransport by metabolizable and nonmetabolizable amino acids stimulates a glucose-regulated insulin-secretory response. Biochem Biophys Res Commun 249(2):299–303. doi:10.1006/bbrc.1998.9136 CrossRef McClenaghan NH, Barnett CR, Flatt PR (1998) Na+ cotransport by metabolizable and nonmetabolizable amino acids stimulates a glucose-regulated insulin-secretory response. Biochem Biophys Res Commun 249(2):299–303. doi:10.​1006/​bbrc.​1998.​9136 CrossRef
18.
go back to reference Sener A, Malaisse WJ (2002) The stimulus-secretion coupling of amino acid-induced insulin release. Insulinotropic action of l-alanine. Biochim Biophys Acta 1573(1):100–104CrossRef Sener A, Malaisse WJ (2002) The stimulus-secretion coupling of amino acid-induced insulin release. Insulinotropic action of l-alanine. Biochim Biophys Acta 1573(1):100–104CrossRef
19.
go back to reference Brennan L, Shine A, Hewage C, Malthouse JP, Brindle KM, McClenaghan N, Flatt PR, Newsholme P (2002) A nuclear magnetic resonance-based demonstration of substantial oxidative l-alanine metabolism and l-alanine-enhanced glucose metabolism in a clonal pancreatic beta-cell line: metabolism of l-alanine is important to the regulation of insulin secretion. Diabetes 51(6):1714–1721CrossRef Brennan L, Shine A, Hewage C, Malthouse JP, Brindle KM, McClenaghan N, Flatt PR, Newsholme P (2002) A nuclear magnetic resonance-based demonstration of substantial oxidative l-alanine metabolism and l-alanine-enhanced glucose metabolism in a clonal pancreatic beta-cell line: metabolism of l-alanine is important to the regulation of insulin secretion. Diabetes 51(6):1714–1721CrossRef
20.
go back to reference Cunningham GA, McClenaghan NH, Flatt PR, Newsholme P (2005) l-Alanine induces changes in metabolic and signal transduction gene expression in a clonal rat pancreatic beta-cell line and protects from pro-inflammatory cytokine-induced apoptosis. Clin Sci 109(5):447–455. doi:10.1042/CS20050149 CrossRef Cunningham GA, McClenaghan NH, Flatt PR, Newsholme P (2005) l-Alanine induces changes in metabolic and signal transduction gene expression in a clonal rat pancreatic beta-cell line and protects from pro-inflammatory cytokine-induced apoptosis. Clin Sci 109(5):447–455. doi:10.​1042/​CS20050149 CrossRef
21.
go back to reference Olney JW, Sharpe LG (1969) Brain lesions in an infant rhesus monkey treated with monsodium glutamate. Science 166(3903):386–388CrossRef Olney JW, Sharpe LG (1969) Brain lesions in an infant rhesus monkey treated with monsodium glutamate. Science 166(3903):386–388CrossRef
22.
go back to reference Matyskova R, Maletinska L, Maixnerova J, Pirnik Z, Kiss A, Zelezna B (2008) Comparison of the obesity phenotypes related to monosodium glutamate effect on arcuate nucleus and/or the high fat diet feeding in C57BL/6 and NMRI mice. Physiol Res/Acad Sci Bohemoslov 57(5):727–734 Matyskova R, Maletinska L, Maixnerova J, Pirnik Z, Kiss A, Zelezna B (2008) Comparison of the obesity phenotypes related to monosodium glutamate effect on arcuate nucleus and/or the high fat diet feeding in C57BL/6 and NMRI mice. Physiol Res/Acad Sci Bohemoslov 57(5):727–734
23.
go back to reference Hirata AE, Alvarez-Rojas F, Carvalheira JB, Carvalho CR, Dolnikoff MS, Abdalla Saad MJ (2003) Modulation of IR/PTP1B interaction and downstream signaling in insulin sensitive tissues of MSG-rats. Life Sci 73(11):1369–1381CrossRef Hirata AE, Alvarez-Rojas F, Carvalheira JB, Carvalho CR, Dolnikoff MS, Abdalla Saad MJ (2003) Modulation of IR/PTP1B interaction and downstream signaling in insulin sensitive tissues of MSG-rats. Life Sci 73(11):1369–1381CrossRef
24.
go back to reference Nardelli TR, Ribeiro RA, Balbo SL, Vanzela EC, Carneiro EM, Boschero AC, Bonfleur ML (2011) Taurine prevents fat deposition and ameliorates plasma lipid profile in monosodium glutamate-obese rats. Amino Acids 41(4):901–908. doi:10.1007/s00726-010-0789-7 CrossRef Nardelli TR, Ribeiro RA, Balbo SL, Vanzela EC, Carneiro EM, Boschero AC, Bonfleur ML (2011) Taurine prevents fat deposition and ameliorates plasma lipid profile in monosodium glutamate-obese rats. Amino Acids 41(4):901–908. doi:10.​1007/​s00726-010-0789-7 CrossRef
25.
go back to reference Lubaczeuski C, Balbo SL, Ribeiro RA, Vettorazzi JF, Santos-Silva JC, Carneiro EM, Bonfleur ML (2015) Vagotomy ameliorates islet morphofunction and body metabolic homeostasis in MSG-obese rats. Braz J Med Biol Res Revista brasileira de pesquisas medicas e biologicas/Sociedade Brasileira de Biofisica [et al] 0:0. doi:10.1590/1414-431X20144340 Lubaczeuski C, Balbo SL, Ribeiro RA, Vettorazzi JF, Santos-Silva JC, Carneiro EM, Bonfleur ML (2015) Vagotomy ameliorates islet morphofunction and body metabolic homeostasis in MSG-obese rats. Braz J Med Biol Res Revista brasileira de pesquisas medicas e biologicas/Sociedade Brasileira de Biofisica [et al] 0:0. doi:10.​1590/​1414-431X20144340
26.
go back to reference Lucinei Balbo S, Gravena C, Bonfleur ML, de Freitas Mathias PC (2000) Insulin secretion and acetylcholinesterase activity in monosodium l-glutamate-induced obese mice. Horm Res 54(4):186–191. doi:10.1159/000053257 Lucinei Balbo S, Gravena C, Bonfleur ML, de Freitas Mathias PC (2000) Insulin secretion and acetylcholinesterase activity in monosodium l-glutamate-induced obese mice. Horm Res 54(4):186–191. doi:10.​1159/​000053257
27.
go back to reference Balbo SL, Bonfleur ML, Carneiro EM, Amaral ME, Filiputti E, Mathias PC (2002) Parasympathetic activity changes insulin response to glucose and neurotransmitters. Diabetes Metab 28(6.2):3S13–3S17 (discussion 13S108-112) Balbo SL, Bonfleur ML, Carneiro EM, Amaral ME, Filiputti E, Mathias PC (2002) Parasympathetic activity changes insulin response to glucose and neurotransmitters. Diabetes Metab 28(6.2):3S13–3S17 (discussion 13S108-112)
28.
go back to reference Nagata M, Suzuki W, Iizuka S, Tabuchi M, Maruyama H, Takeda S, Aburada M, Miyamoto K (2006) Type 2 diabetes mellitus in obese mouse model induced by monosodium glutamate. Exp Anim/Jpn Assoc Lab Anim Sci 55(2):109–115 Nagata M, Suzuki W, Iizuka S, Tabuchi M, Maruyama H, Takeda S, Aburada M, Miyamoto K (2006) Type 2 diabetes mellitus in obese mouse model induced by monosodium glutamate. Exp Anim/Jpn Assoc Lab Anim Sci 55(2):109–115
29.
go back to reference Ribeiro RA, Balbo SL, Roma LP, Camargo RL, Barella LF, Vanzela EC, de Freitas Mathias PC, Carneiro EM, Boschero AC, Bonfleur ML (2013) Impaired muscarinic type 3 (M3) receptor/PKC and PKA pathways in islets from MSG-obese rats. Mol Biol Rep 40(7):4521–4528. doi:10.1007/s11033-013-2546-y CrossRef Ribeiro RA, Balbo SL, Roma LP, Camargo RL, Barella LF, Vanzela EC, de Freitas Mathias PC, Carneiro EM, Boschero AC, Bonfleur ML (2013) Impaired muscarinic type 3 (M3) receptor/PKC and PKA pathways in islets from MSG-obese rats. Mol Biol Rep 40(7):4521–4528. doi:10.​1007/​s11033-013-2546-y CrossRef
30.
go back to reference Duivenvoorden I, Teusink B, Rensen PC, Romijn JA, Havekes LM, Voshol PJ (2005) Apolipoprotein C3 deficiency results in diet-induced obesity and aggravated insulin resistance in mice. Diabetes 54(3):664–671CrossRef Duivenvoorden I, Teusink B, Rensen PC, Romijn JA, Havekes LM, Voshol PJ (2005) Apolipoprotein C3 deficiency results in diet-induced obesity and aggravated insulin resistance in mice. Diabetes 54(3):664–671CrossRef
31.
go back to reference Bernardis LL, Patterson BD (1968) Correlation between ‘Lee index’ and carcass fat content in weanling and adult female rats with hypothalamic lesions. J Endocrinol 40(4):527–528CrossRef Bernardis LL, Patterson BD (1968) Correlation between ‘Lee index’ and carcass fat content in weanling and adult female rats with hypothalamic lesions. J Endocrinol 40(4):527–528CrossRef
32.
go back to reference Carneiro EM, Latorraca MQ, Araujo E, Beltra M, Oliveras MJ, Navarro M, Berna G, Bedoya FJ, Velloso LA, Soria B, Martin F (2009) Taurine supplementation modulates glucose homeostasis and islet function. J Nutr Biochem 20(7):503–511. doi:10.1016/j.jnutbio.2008.05.008 CrossRef Carneiro EM, Latorraca MQ, Araujo E, Beltra M, Oliveras MJ, Navarro M, Berna G, Bedoya FJ, Velloso LA, Soria B, Martin F (2009) Taurine supplementation modulates glucose homeostasis and islet function. J Nutr Biochem 20(7):503–511. doi:10.​1016/​j.​jnutbio.​2008.​05.​008 CrossRef
33.
go back to reference Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRef Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRef
34.
go back to reference Ribeiro RA, Santos-Silva JC, Vettorazzi JF, Cotrim BB, Mobiolli DD, Boschero AC, Carneiro EM (2012) Taurine supplementation prevents morpho-physiological alterations in high-fat diet mice pancreatic beta-cells. Amino Acids 43(4):1791–1801. doi:10.1007/s00726-012-1263-5 CrossRef Ribeiro RA, Santos-Silva JC, Vettorazzi JF, Cotrim BB, Mobiolli DD, Boschero AC, Carneiro EM (2012) Taurine supplementation prevents morpho-physiological alterations in high-fat diet mice pancreatic beta-cells. Amino Acids 43(4):1791–1801. doi:10.​1007/​s00726-012-1263-5 CrossRef
36.
go back to reference Iwase M, Ichikawa K, Tashiro K, Iino K, Shinohara N, Ibayashi S, Yoshinari M, Fujishima M (2000) Effects of monosodium glutamate-induced obesity in spontaneously hypertensive rats vs. Wistar Kyoto rats: serum leptin and blood flow to brown adipose tissue. Hypertens Res 23(5):503–510CrossRef Iwase M, Ichikawa K, Tashiro K, Iino K, Shinohara N, Ibayashi S, Yoshinari M, Fujishima M (2000) Effects of monosodium glutamate-induced obesity in spontaneously hypertensive rats vs. Wistar Kyoto rats: serum leptin and blood flow to brown adipose tissue. Hypertens Res 23(5):503–510CrossRef
37.
go back to reference Leguisamo NM, Lehnen AM, Machado UF, Okamoto MM, Markoski MM, Pinto GH, Schaan BD (2012) GLUT4 content decreases along with insulin resistance and high levels of inflammatory markers in rats with metabolic syndrome. Cardiovas Diabetol 11:100. doi:10.1186/1475-2840-11-100 CrossRef Leguisamo NM, Lehnen AM, Machado UF, Okamoto MM, Markoski MM, Pinto GH, Schaan BD (2012) GLUT4 content decreases along with insulin resistance and high levels of inflammatory markers in rats with metabolic syndrome. Cardiovas Diabetol 11:100. doi:10.​1186/​1475-2840-11-100 CrossRef
38.
go back to reference Wang WF, Li SM, Ren GP, Zheng W, Lu YJ, Yu YH, Xu WJ, Li TH, Zhou LH, Liu Y, Li DS (2014) Recombinant murine fibroblast growth factor 21 ameliorates obesity-related inflammation in monosodium glutamate-induced obesity rats. Endocrine. doi:10.1007/s12020-014-0433-5 Wang WF, Li SM, Ren GP, Zheng W, Lu YJ, Yu YH, Xu WJ, Li TH, Zhou LH, Liu Y, Li DS (2014) Recombinant murine fibroblast growth factor 21 ameliorates obesity-related inflammation in monosodium glutamate-induced obesity rats. Endocrine. doi:10.​1007/​s12020-014-0433-5
39.
go back to reference Andreazzi AE, Scomparin DX, Mesquita FP, Balbo SL, Gravena C, De Oliveira JC, Rinaldi W, Garcia RM, Grassiolli S, Mathias PC (2009) Swimming exercise at weaning improves glycemic control and inhibits the onset of monosodium L-glutamate-obesity in mice. J Endocrinol 201(3):351–359. doi:10.1677/JOE-08-0312 CrossRef Andreazzi AE, Scomparin DX, Mesquita FP, Balbo SL, Gravena C, De Oliveira JC, Rinaldi W, Garcia RM, Grassiolli S, Mathias PC (2009) Swimming exercise at weaning improves glycemic control and inhibits the onset of monosodium L-glutamate-obesity in mice. J Endocrinol 201(3):351–359. doi:10.​1677/​JOE-08-0312 CrossRef
40.
go back to reference Roman-Ramos R, Almanza-Perez JC, Garcia-Macedo R, Blancas-Flores G, Fortis-Barrera A, Jasso EI, Garcia-Lorenzana M, Campos-Sepulveda AE, Cruz M, Alarcon-Aguilar FJ (2011) Monosodium glutamate neonatal intoxication associated with obesity in adult stage is characterized by chronic inflammation and increased mRNA expression of peroxisome proliferator-activated receptors in mice. Basic Clin Pharmacol Toxicol 108(6):406–413. doi:10.1111/j.1742-7843.2011.00671.x CrossRef Roman-Ramos R, Almanza-Perez JC, Garcia-Macedo R, Blancas-Flores G, Fortis-Barrera A, Jasso EI, Garcia-Lorenzana M, Campos-Sepulveda AE, Cruz M, Alarcon-Aguilar FJ (2011) Monosodium glutamate neonatal intoxication associated with obesity in adult stage is characterized by chronic inflammation and increased mRNA expression of peroxisome proliferator-activated receptors in mice. Basic Clin Pharmacol Toxicol 108(6):406–413. doi:10.​1111/​j.​1742-7843.​2011.​00671.​x CrossRef
41.
go back to reference Watanabe N, Kobayashi M, Maegawa H, Ishibashi O, Takata Y, Shigeta Y (1986) Long-term in vitro effects of insulin on insulin binding and glucose transport. Diabetes Res Clin Pract 2(1):1–8CrossRef Watanabe N, Kobayashi M, Maegawa H, Ishibashi O, Takata Y, Shigeta Y (1986) Long-term in vitro effects of insulin on insulin binding and glucose transport. Diabetes Res Clin Pract 2(1):1–8CrossRef
42.
go back to reference Cigolini M, Zancanaro C, Benati D, Cavallo E, Bosello O, Smith U (1987) Metformin enhances insulin binding to “in vitro” down regulated human fat cells. Diabete Metab 13(1):20–22 Cigolini M, Zancanaro C, Benati D, Cavallo E, Bosello O, Smith U (1987) Metformin enhances insulin binding to “in vitro” down regulated human fat cells. Diabete Metab 13(1):20–22
43.
go back to reference Sullivan JE, Brocklehurst KJ, Marley AE, Carey F, Carling D, Beri RK (1994) Inhibition of lipolysis and lipogenesis in isolated rat adipocytes with AICAR, a cell-permeable activator of AMP-activated protein kinase. FEBS Lett 353(1):33–36CrossRef Sullivan JE, Brocklehurst KJ, Marley AE, Carey F, Carling D, Beri RK (1994) Inhibition of lipolysis and lipogenesis in isolated rat adipocytes with AICAR, a cell-permeable activator of AMP-activated protein kinase. FEBS Lett 353(1):33–36CrossRef
44.
go back to reference Treebak JT, Glund S, Deshmukh A, Klein DK, Long YC, Jensen TE, Jorgensen SB, Viollet B, Andersson L, Neumann D, Wallimann T, Richter EA, Chibalin AV, Zierath JR, Wojtaszewski JF (2006) AMPK-mediated AS160 phosphorylation in skeletal muscle is dependent on AMPK catalytic and regulatory subunits. Diabetes 55(7):2051–2058. doi:10.2337/db06-0175 CrossRef Treebak JT, Glund S, Deshmukh A, Klein DK, Long YC, Jensen TE, Jorgensen SB, Viollet B, Andersson L, Neumann D, Wallimann T, Richter EA, Chibalin AV, Zierath JR, Wojtaszewski JF (2006) AMPK-mediated AS160 phosphorylation in skeletal muscle is dependent on AMPK catalytic and regulatory subunits. Diabetes 55(7):2051–2058. doi:10.​2337/​db06-0175 CrossRef
Metadata
Title
Benefits of l-alanine or l-arginine supplementation against adiposity and glucose intolerance in monosodium glutamate-induced obesity
Authors
Thiago R. Araujo
Israelle N. Freitas
Jean F. Vettorazzi
Thiago M. Batista
Junia C. Santos-Silva
Maria L. Bonfleur
Sandra L. Balbo
Antonio C. Boschero
Everardo M. Carneiro
Rosane A. Ribeiro
Publication date
01-09-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 6/2017
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-016-1245-6

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