Abstract
The present study was undertaken to investigate the effect of the combination of soy protein, amylopectin, and chromium (SAC) on muscle protein synthesis and signal transduction pathways involved in protein synthesis (mTOR pathways, IGF-1, and AktSer473) and proteolysis (FOXO1Ser256; MURF1, MAFbx) after exercise. Thirty-five Wistar rats were randomly divided into five groups: (1) control (C); (2) exercise (E); (3) exercise + soy protein (3.1 g/kg/day) (E + S); (4) exercise + soy protein + chromium (E + S + Cr); (5) exercise + soy protein + amylopectin + chromium (E + S + A + Cr). Post-exercise ingestion of SAC significantly increased the fractional rate of protein synthesis (FSR), insulin, glycogen, and amino acid levels with the highest effect observed in E + S + A + Cr group (P ˂ 0.05). However, SAC supplementation decreased the lactic acid concentration (P ˂ 0.05). A reduction in forkhead box protein O1 (FOXO1) and forkhead box protein O3 (FOXO3) (regulators of ubiquitin-related proteolysis) and muscle atrophy F-box (MAFbx) levels was noted after treatment with SAC (P < 0.05). Insulin-like growth factor 1(IGF-1) level was increased in the E + S, E + S + Cr, and E + S + A + Cr groups (P < 0.05). While the phosphorylation of 4E-BP1Thr37/46, AktSer473, mTORSer2448, and S6K1Thr389 levels increased after SAC supplementation, phosphorylated muscle ring finger 1 (MuRF-1, an E3-ubiquitin ligase gene) was found to be significantly lower compared with the E group (P ˂ 0.05). These results indicate that SAC supplementation improves FSR, insulin, and glycogen levels after exercise. SAC improves protein synthesis by inhibiting the ubiquitin–proteasome pathway and inducing anabolic metabolism.
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Damas F, Libardi CA, Ugrinowitsch C (2018) The development of skeletal muscle hypertrophy through resistance training: the role of muscle damage and muscle protein synthesis. Eur J Appl Physiol 118(3):485–500. https://doi.org/10.1007/s00421-017-3792-9
Stokes T, Hector AJ, Morton RW, McGlory C, Phillips SM (2018) Recent perspectives regarding the role of dietary protein for the promotion of muscle hypertrophy with resistance exercise training. Nutrients 10(2):E180. https://doi.org/10.3390/nu10020180
Biolo G, Maggi SP, Williams BD, Tipton KD, Wolfe RR (1995) Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Phys 268(3):E514–E520
Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR (1997) Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Phys 273:E99–E107
Kanda A, Nakayama K, Fukasawa T, Koga J, Kanegae M, Kawanaka K, Higuchi M (2013) Post-exercise whey protein hydrolysate supplementation induces a greater increase in muscle protein synthesis than its constituent amino acid content. Br J Nutr 110:981–987. https://doi.org/10.1017/S0007114512006174
Koopman R, Walrand S, Beelen M, Gijsen AP, Kies AK, Boirie Y, Saris WH, van Loon LJ (2009) Dietary protein digestion and absorption rates and the subsequent postprandial muscle protein synthetic response do not differ between young and elderly men. J Nutr 139(9):1707–1713. https://doi.org/10.3945/jn.109.109173
Anthony JC, Anthony TG, Layman DK (1999) Leucine supplementation enhances skeletal muscle recovery in rats following exercise. J Nutr 129(6):1102–1106
Williamson DL, Kubica N, Kimball SR, Jefferson LS (2006) Exercise-induced alterations in extracellular signal-regulated kinase 1/2 and mammalian target of rapamycin (mTOR) signalling to regulatory mechanisms of mRNA translation in mouse muscle. J Physiol 573(2):497–510. https://doi.org/10.1113/jphysiol.2005.103481
Allen DL, Unterman TG (2007) Regulation of myostatin expression and myoblast differentiation by FOXO and SMAD transcription factors. Am J Physiol Cell Physiol 292(1):C188–C199. https://doi.org/10.1152/ajpcell.00542.2005
Nader GA (2005) Molecular determinants of skeletal muscle mass: getting the "AKT" together. Int J Biochem Cell Biol 37(10):1985–1996. https://doi.org/10.1016/j.biocel.2005.02.026
Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, Taniguchi T, Mochida K, Hata T, Matsuda J, Aburatani H, Nishino I, Ezaki O (2004) Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down regulated type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279(39):41114–41123. https://doi.org/10.1074/jbc.M400674200
Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL (2004) FOXO transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117(3):399–412
Lokireddy S, Wijesoma IW, Sze SK, McFarlane C, Kambadur R, Sharma M (2012) Identification of atrogin-1-targeted proteins during the myostatin-induced skeletal muscle wasting. Am J Physiol Cell Physiol 303(5):C512–C529. https://doi.org/10.1152/ajpcell.00402.2011
Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, Rakhilin SV, Stitt TN, Patterson C, Latres E, Glass DJ (2007) The E3 ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab 6(5):376–385. https://doi.org/10.1016/j.cmet.2007.09.009
Cohen S, Brault JJ, Gygi SP, Glass DJ, Valenzuela DM, Gartner C, Latres E, Goldberg AL (2009) During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol 185(6):1083–1095. https://doi.org/10.1083/jcb.200901052
Burke DG, Chilibeck PD, Davidson KS, Candow DG, Farthing J, Smith-Palmer T (2001) The effect of whey protein supplementation with and without creatine monohydrate combined with resistance training on lean tissue mass and muscle strength. Int J Sport Nutr Exerc Metab 11(3):349–364
Kanda A, Nakayama K, Sanbongi C, Nagata M, Ikegami S, Itoh H (2016) Effects of whey, caseinate, or milk protein ingestion on muscle protein synthesis after exercise. Nutrients 8(6):E339. https://doi.org/10.3390/nu8060339
Paul G, Mendelson GJ (2015) Evidence supports the use of soy protein to promote cardiometabolic health and muscle development. J Am Coll Nutr 34(1):56–59. https://doi.org/10.1080/07315724.2015.1080531
Shenoy S, Dhawan M, Sandhu JS (2016) Four weeks of supplementation with isolated soy protein attenuates exercise-induced muscle damage and enhances muscle recovery in well trained athletes: a randomized trial. Asian J Sports Med 7(3):e33528. https://doi.org/10.5812/asjsm.33528
Burke LM, Hawley JA, Ross ML, Moore DR, Phillips SM, Slater GR, Stellingwerff T, Tipton KD, Garnham AP, Coffey VG (2012) Preexercise aminoacidemia and muscle protein synthesis after resistance exercise. Med Sci Sports Exerc 44(10):1968–1977. https://doi.org/10.1249/MSS.0b013e31825d28fa
Norton LE, Layman DK (2006) Leucine regulates translation initiation of protein synthesis in skeletal muscle after exercise. J Nutr 136(2):533S–537S. https://doi.org/10.1093/jn/136.2.533S
Wang Q, Ge X, Tian X, Zhang Y, Zhang J, Zhang P (2013) Soy isoflavone: the multipurpose phytochemical (review). Biomed Rep 1(5):697–701. https://doi.org/10.3892/br.2013.129
Chen WY, Chen CJ, Liu CH, Mao FC (2008) Chromium supplementation enhances insulin signalling in skeletal muscle of obese KK/HlJ diabetic mice. Diabetes Obes Metab 11(4):293–303. https://doi.org/10.1111/j.1463-1326.2008.00936.x
Sahin K, Tuzcu M, Orhan C, Ali S, Sahin N, Gencoglu H, Ozkan Y, Hayirli A, Gozel N, Komorowski JR (2013) Chromium modulates expressions of neuronal plasticity markers and glial fibrillary acidic proteins in hypoglycemia-induced brain injury. Life Sci 93(25–26):1039–1048. https://doi.org/10.1016/j.lfs.2013.10.009
Ziegenfuss TN, Lopez HL, Kedia A, Habowski SM, Sandrock JE, Raub B, Kerksick CM, Ferrando AA (2017) Effects of an amylopectin and chromium complex on the anabolic response to a suboptimal dose of whey protein. J Int Soc Sports Nutr 14:6. https://doi.org/10.1186/s12970-017-0163-1
Bradstreet RB (1954) Kjeldahl method for organic nitrogen. Anal Chem 26(1):185–187. https://doi.org/10.1021/ac60085a028
Gautsch TA, Anthony JC, Kimball SR, Paul GL, Layman DK, Jefferson LS (1998) Availability of eIF4E regulates skeletal muscle protein synthesis during recovery from exercise. Am J Phys 274(2):406–414
Bark TH, McNurlan MA, Lang CH, Garlick PJ (1998) Increased protein synthesis after acute IGF-I or insulin infusion is localized to muscle in mice. Am J Phys 275:E118–E123
Takach E, O'Shea T, Liu H (2014) High-throughput quantitation of amino acids in rat and mouse biological matrices using stable isotope labeling and UPLC-MS/MS analysis. J Chromatogr B Anal Technol Biomed Life Sci 964:180–190. https://doi.org/10.1016/j.jchromb.2014.04.043
Bottiglieri T (1987) The effect of storage on rat tissues and human plasma amino acid levels determined by HPLC. Biomed Chromatogr 2(5):195–196
Tang JE, Moore DR, Kujbida GW, Tarnopolsky MA, Phillips SM (2009) Ingestion of whey hydrolysate, casein, or soy protein isolate: effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. J Appl Physiol 107(3):987–992. https://doi.org/10.1152/japplphysiol.00076.2009
Vincent JB (2004) Recent advances in the nutritional biochemistry of trivalent chromium. Proc Nutr Soc 63(1):41–47. https://doi.org/10.1079/PNS2003315
Wang H, Kruszewski A, Brautigan DL (2005) Cellular chromium enhances activation of insulin receptor kinase. Biochemistry 44(22):8167–8175. https://doi.org/10.1021/bi0473152
Hoffman NJ, Penque BA, Habegger KM, Sealls W, Tackett L, Elmendorf JS (2014) Chromium enhances insulin responsiveness via AMPK. J Nutr Biochem 25(5):565–572. https://doi.org/10.1016/j.jnutbio.2014.01.007
Evans GW, Bowman TD (1992) Chromium picolinate increases membrane fluidity and rate of insulin internalization. J Inorg Biochem 46(4):243–250
Brosnan JT, Brosnan ME (2006) The sulfur-containing amino acids: an overview. J Nutr 136(6):1636S–1640S. https://doi.org/10.1093/jn/136.6.1636S
Wu G, Fang YZ, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134(3):489–492. https://doi.org/10.1093/jn/134.3.489
Stuart MP (2014) A brief review of critical processes in exercise-induced muscular hypertrophy. Sports Med 44(1):71–77
Blomstrand E, Eliasson J, Karlsson HK, Köhnke R (2006) Branched-chain amino acids activate key enzymes in protein synthesis after physical exercise. J Nutr 136(1):269S–273S. https://doi.org/10.1093/jn/136.1.269S
Escobar J, Frank JW, Suryawan A, Nguyen HV, Kimball SR, Jefferson LS, Davis TA (2005) Physiological rise in plasma leucine stimulates muscle protein synthesis in neonatal pigs by enhancing translation initiation factor activation. Am J Physiol Endocrinol Metab 288(5):E914–E921. https://doi.org/10.1152/ajpendo.00510.2004
Connors MT, Poppi DP, Cant JP (2008) Protein elongation rates in tissues of growing and adult sheep. J Anim Sci 86(9):2288–2295. https://doi.org/10.2527/jas.2007-0159
Frank JW, Escobar J, Suryawan A, Nguyen HV, Kimball SR, Jefferson LS, Davis TA (2006) Dietary protein and lactose increase translation initiation factor activation and tissue protein synthesis in neonatal pigs. Am J Physiol Endocrinol Metab 290(2):E225–E233. https://doi.org/10.1152/ajpendo.00351.2005
Arden KC (2008) FOXO animal models reveal a variety of diverse roles for FOXO transcription factors. Oncogene 27(16):2345–2350. https://doi.org/10.1038/onc.2008.27
Bonaldo P, Sandri M (2013) Cellular and molecular mechanisms of muscle atrophy. Dis Model Mech 6(1):25–39. https://doi.org/10.1242/dmm.010389
Tang ED, Nuñez G, Barr FG, Guan KL (1999) Negative regulation of the forkhead transcription factor FKHR by Akt. J Biol Chem 274(24):16741–16746
Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M (2007) FOXO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6(6):458–471. https://doi.org/10.1016/j.cmet.2007.11.001
Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL (2007) FOXO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6(6):472–483. https://doi.org/10.1016/j.cmet.2007.11.004
Sanchez AM, Csibi A, Raibon A, Docquier A, Lagirand-Cantaloube J, Leibovitch MP, Leibovitch SA, Bernardi H (2013) EIF3f: a central regulator of the antagonism atrophy/hypertrophy in skeletal muscle. Int J Biochem Cell Biol 45(10):2158–2162. https://doi.org/10.1016/j.biocel.2013.06.001
Luo J, Chen D, Yu B (2010) Effects of different dietary protein sources on expression of genes related to protein metabolism in growing rats. Br J Nutr 104(10):1421–1428. https://doi.org/10.1017/S000711451000231X
Paula-Gomes S, Goncalves DA, Baviera AM, Zanon NM, Navegantes LC, Kettelhut IC (2013) Insulin suppresses atrophy- and autophagy related genes in heart tissue and cardiomyocytes through AKT/FOXO signaling. Horm Metab Res 45(12):849–855. https://doi.org/10.1055/s-0033-1347209
Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism 124(3):471–484. https://doi.org/10.1016/j.cell.2006.01.016
Greenhaff PL, Karagounis LG, Peirce N, Simpson EJ, Hazell M, Layfield R, Wackerhage H, Smith K, Atherton P, Selby A, Rennie MJ (2008) Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. Am J Physiol Endocrinol Metab 295(3):E595–E604. https://doi.org/10.1152/ajpendo.90411.2008
Anthony TG, McDaniel BJ, Knoll P, Bunpo P, Paul GL, McNurlan MA (2007) Feeding meals containing soy or whey protein after exercise stimulates protein synthesis and translation initiation in the skeletal muscle of male rats. J Nutr 37(2):357–362. https://doi.org/10.1093/jn/137.2.357
Gallagher P, Richmond S, Dudley K, Prewitt M, Gandy N, Kudrna B, Touchberry C (2007) Interaction of resistance exercise and BCAA supplementation on Akt and p70 s6 kinase phosphorylation in human skeletal muscle. FASEB J 21:895.10 https://www.fasebj.org/doi/abs/10.1096/fasebj.21.6.A1206
Shen WH, Boyle DW, Wisniowski P, Bade A, Liechty EA (2005) Insulin and IGF-I stimulate the formation of the eukaryotic initiation factor 4F complex and protein synthesis in C2C12 myotubes independent of availability of external amino acids. J Endocrinol 185(2):275–289. https://doi.org/10.1677/joe.1.06080
Hara K, Maruki Y, Long X, Yoshino K, Oshiro N, Hidayat S, Tokunaga C, Avruch J, Yonezawa K (2002) Raptor, a binding partner of target of rapamycin (TOR), mediates mTOR action. Cell 110(2):177–189. https://doi.org/10.1016/S0092-8674(02)00833-4
Beugnet A, Tee AR, Taylor PM, Proud CG (2003) Regulation of targets of mTOR (mammalian target of rapamycin) signalling by intracellular amino acid availability. Biochem J 372(1):555–566
Acknowledgments
This work was granted by Firat University Scientific Research Projects Unit (VF.16.20) and the Turkish Academy of Sciences (K.S.). The authors thank Nutrition21 (Purchase, NY, USA) for providing amylopectin + chromium and to Mr. Besir Er for his kind efforts during this study.
Authors’ Contributions
K.S. and J.R.K. participated in the study design and drafting the manuscript. C.O., M.T., and N.S. participated in the data collection and assays, data analysis, and drafting the manuscript. C.O. and D.D.P.B. participated in the data analysis and statistical analysis for the variables and drafting the manuscript. K.S. and J.R.K. participated in drafting the manuscript. All authors read and approved the final manuscript.
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The authors declare that there are no conflicts of interest. J.R.K. is employed by Nutrition21, Purchase, NY, USA.
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All animal experimental procedures followed protocols approved by the Experimental Animal Ethics Committee of Firat University (Elazig, Turkey).
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Kayri, V., Orhan, C., Tuzcu, M. et al. Combination of Soy Protein, Amylopectin, and Chromium Stimulates Muscle Protein Synthesis by Regulation of Ubiquitin–Proteasome Proteolysis Pathway after Exercise. Biol Trace Elem Res 190, 140–149 (2019). https://doi.org/10.1007/s12011-018-1539-z
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DOI: https://doi.org/10.1007/s12011-018-1539-z