The effects of glucagon and the target of rapamycin (TOR) on skeletal muscle protein synthesis and age-dependent sarcopenia in humans

Clinical Nutrition ESPEN - Tập 44 - Trang 15-25 - 2021
María M. Adeva‐Andany1, Carlos Fernández‐Fernández1, Yosua López-Pereiro1, Isabel Castro-Calvo1, Natalia Carneiro-Freire1
1Internal Medicine Department, Hospital General Juan Cardona, c/ Pardo Bazán s/n, 15406, Ferrol, Spain

Tóm tắt

Từ khóa


Tài liệu tham khảo

Putra, 2021, Protein source and muscle health in older adults: a literature review, Nutrients, 13, 10.3390/nu13030743

Lim, 2021, Animal protein versus plant protein in supporting lean mass and muscle strength: a systematic review and meta-analysis of randomized controlled trials, Nutrients, 13, 10.3390/nu13020661

Deane, 2020, Animal, plant, collagen and blended dietary proteins: effects on musculoskeletal outcomes, Nutrients, 12, 10.3390/nu12092670

Berrazaga, 2019, The role of the anabolic properties of plant- versus animal-based protein sources in supporting muscle mass maintenance: a critical review, Nutrients, 11, 10.3390/nu11081825

Messina, 2018, No difference between the effects of supplementing with soy protein versus animal protein on gains in muscle mass and strength in response to resistance exercise, Int J Sport Nutr Exerc Metabol, 28, 674, 10.1123/ijsnem.2018-0071

Haring, 2017, Dietary protein sources and risk for incident chronic kidney disease: results from the atherosclerosis risk in communities (ARIC) study, J Ren Nutr, 27, 233

Bernier-Jean, 2020, Dietary plant and animal protein intake and decline in estimated glomerular filtration rate among elderly women: a 10-year longitudinal cohort study, Nephrol Dial Transplant, 1

Mirmiran, 2020, A prospective study of dietary meat intake and risk of incident chronic kidney disease, J Ren Nutr, 30, 111

Alvirdizadeh, 2020, A prospective study on total protein, plant protein and animal protein in relation to the risk of incident chronic kidney disease, BMC Nephrol, 21, 489, 10.1186/s12882-020-02079-y

Yuzbashian, 2015, Associations of dietary macronutrients with glomerular filtration rate and kidney dysfunction: tehran lipid and glucose study, J Nephrol, 28, 173

Rohde, 2001, The TOR kinases link nutrient sensing to cell growth, J Biol Chem, 276, 9583, 10.1074/jbc.R000034200

Fingar, 2004, Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression, Oncogene, 23, 3151, 10.1038/sj.onc.1207542

Wullschleger, 2005, Molecular organization of target of rapamycin complex 2, J Biol Chem, 280, 30697, 10.1074/jbc.M505553200

Rosner, 2008, Cytoplasmic and nuclear distribution of the protein complexes mTORC1 and mTORC2: rapamycin triggers dephosphorylation and delocalization of the mTORC2 components rictor and sin1, Hum Mol Genet, 17, 2934, 10.1093/hmg/ddn192

Song, 2017, Resistance exercise initiates mechanistic target of rapamycin (mTOR) translocation and protein complex co-localisation in human skeletal muscle, Sci Rep, 7, 5028, 10.1038/s41598-017-05483-x

Hodson, 2017, Differential localization and anabolic responsiveness of mTOR complexes in human skeletal muscle in response to feeding and exercise, Am J Physiol Cell Physiol, 313, C604, 10.1152/ajpcell.00176.2017

Kotani, 1994, Involvement of phosphoinositide 3-kinase in insulin- or IGF-1-induced membrane ruffling, EMBO J, 13, 2313, 10.1002/j.1460-2075.1994.tb06515.x

Kimball, 1994, Regulation of protein synthesis by insulin, Annu Rev Physiol, 56, 321, 10.1146/annurev.ph.56.030194.001541

Cenni, 2003, Targeting of the Akt/PKB kinase to the actin skeleton, Cell Mol Life Sci, 60, 2710, 10.1007/s00018-003-3349-4

Jacinto, 2004, Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive, Nat Cell Biol, 6, 1122, 10.1038/ncb1183

Li, 2004, Biochemical and functional characterizations of small GTPase Rheb and TSC2 GAP activity, Mol Cell Biol, 24, 7965, 10.1128/MCB.24.18.7965-7975.2004

Sarbassov, 2005, Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex, Science, 307, 1098, 10.1126/science.1106148

Martin, 2005, The expanding TOR signaling network, Curr Opin Cell Biol, 17, 158, 10.1016/j.ceb.2005.02.008

Yang, 2006, TSC1/TSC2 and Rheb have different effects on TORC1 and TORC2 activity, Proc Natl Acad Sci U S A, 103, 6811, 10.1073/pnas.0602282103

Avruch, 2006, Insulin and amino-acid regulation of mTOR signaling and kinase activity through the Rheb GTPase, Oncogene, 25, 6361, 10.1038/sj.onc.1209882

Wullschleger, 2006, TOR signaling in growth and metabolism, Cell, 124, 471, 10.1016/j.cell.2006.01.016

Martin, 2007, Rapamycin promotes vascular smooth muscle cell differentiation through insulin receptor substrate-1/phosphatidylinositol 3-kinase/Akt2 feedback signaling, J Biol Chem, 282, 36112, 10.1074/jbc.M703914200

Liu, 2008, Rapamycin inhibits F-actin reorganization and phosphorylation of focal adhesion proteins, Oncogene, 27, 4998, 10.1038/onc.2008.137

Huang, 2008, The TSC1-TSC2 complex is required for proper activation of mTOR complex 2, Mol Cell Biol, 28, 4104, 10.1128/MCB.00289-08

Sancak, 2008, The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1, Science, 320, 1496, 10.1126/science.1157535

Takahara, 2013, Evolutionarily conserved regulation of TOR signalling, J Biochem, 154, 1, 10.1093/jb/mvt047

Farhan, 2015, Endothelial cell mTOR complex-2 regulates sprouting angiogenesis, PloS One, 10, 10.1371/journal.pone.0135245

Walker, 2016, Mechanistic target of rapamycin complex 1 (mTORC1) and mTORC2 as key signaling intermediates in mesenchymal cell activation, J Biol Chem, 291, 6262, 10.1074/jbc.M115.672170

Nitulescu, 2018, The Akt pathway in oncology therapy and beyond (Review), Int J Oncol, 53, 2319

Liu, 2002, Amino acids stimulate translation initiation and protein synthesis through an Akt-independent pathway in human skeletal muscle, J Clin Endocrinol Metab, 87, 5553, 10.1210/jc.2002-020424

Byfield, 2005, hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase, J Biol Chem, 280, 33076, 10.1074/jbc.M507201200

Nobukuni, 2005, Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase, Proc Natl Acad Sci U S A, 102, 14238, 10.1073/pnas.0506925102

Nobukuni, 2007, hvps34, an ancient player, enters a growing game: mTOR Complex1/S6K1 signaling, Curr Opin Cell Biol, 19, 135, 10.1016/j.ceb.2007.02.019

Gulati, 2007, Nutrient sensing in the mTOR/S6K1 signalling pathway, Biochem Soc Trans, 35, 236, 10.1042/BST0350236

Shah, 2000, 4E-BP1 and S6K1: translational integration sites for nutritional and hormonal information in muscle, Am J Physiol Endocrinol Metab, 279, E715, 10.1152/ajpendo.2000.279.4.E715

Hannan, 2003, Activation of S6K1 (p70 ribosomal protein S6 kinase 1) requires an initial calcium-dependent priming event involving formation of a high-molecular-mass signalling complex, Biochem J, 370, 469, 10.1042/bj20021709

Vollenbröker, 2009, mTOR regulates expression of slit diaphragm proteins and cytoskeleton structure in podocytes, Am J Physiol Ren Physiol, 296, F418, 10.1152/ajprenal.90319.2008

Wolfson, 2016, Sestrin2 is a leucine sensor for the mTORC1 pathway, Science, 351, 43, 10.1126/science.aab2674

Yoon, 2016, Leucyl-tRNA synthetase activates Vps34 in amino acid-sensing mTORC1 signaling, Cell Rep, 16, 1510, 10.1016/j.celrep.2016.07.008

Sancak, 2010, Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids, Cell, 141, 290, 10.1016/j.cell.2010.02.024

Korolchuk, 2011, Lysosomal positioning coordinates cellular nutrient responses, Nat Cell Biol, 13, 453, 10.1038/ncb2204

Gulati, 2008, Amino acids activate mTOR complex 1 via Ca2+/CaM signaling to hVps34, Cell Metabol, 7, 456, 10.1016/j.cmet.2008.03.002

Castellino, 1987, Effect of insulin and plasma amino acid concentrations on leucine metabolism in man. Role of substrate availability on estimates of whole body protein synthesis, J Clin Invest, 80, 1784, 10.1172/JCI113272

Fryburg, 1995, Insulin and insulin-like growth factor-I enhance human skeletal muscle protein anabolism during hyperaminoacidemia by different mechanisms, J Clin Invest, 96, 1722, 10.1172/JCI118217

Volpi, 1996, Contribution of amino acids and insulin to protein anabolism during meal absorption, Diabetes, 45, 1245, 10.2337/diab.45.9.1245

Wahren, 1976, Effect of protein ingestion on splanchnic and leg metabolism in normal man and in patients with diabetes mellitus, J Clin Invest, 57, 987, 10.1172/JCI108375

Abumrad, 1982, The effect of leucine infusion on substrate flux across the human forearm, J Surg Res, 32, 453, 10.1016/0022-4804(82)90126-3

Pozefsky, 1976, Effects of brief starvation on muscle amino acid metabolism in nonobese man, J Clin Invest, 57, 444, 10.1172/JCI108295

Gelfand, 1986, Removal of infused amino acids by splanchnic and leg tissues in humans, Am J Physiol, 250, E407

Pozefsky, 1976, Metabolism of forearm tissues in man. Studies with glucagon, Diabetes, 25, 128, 10.2337/diab.25.2.128

Bennet, 1990, The effect of amino acid infusion on leg protein turnover assessed by L-[15N]phenylalanine and L-[1-13C]leucine exchange, Eur J Clin Invest, 20, 41, 10.1111/j.1365-2362.1990.tb01789.x

Louard, 1990, Effect of infused branched-chain amino acids on muscle and whole-body amino acid metabolism in man, Clin Sci, 79, 457, 10.1042/cs0790457

Smith, 1992, Flooding with L-[1-13C]leucine stimulates human muscle protein incorporation of continuously infused L-[1-13C]valine, Am J Physiol, 262, E372

Louard, 1995, Overnight branched-chain amino acid infusion causes sustained suppression of muscle proteolysis, Metabolism, 44, 424, 10.1016/0026-0495(95)90047-0

Charlton, 1996, Evidence for a catabolic role of glucagon during an amino acid load, J Clin Invest, 98, 90, 10.1172/JCI118782

Liu, 2001, Branched chain amino acids activate messenger ribonucleic acid translation regulatory proteins in human skeletal muscle, and glucocorticoids blunt this action, J Clin Endocrinol Metab, 86, 2136

Dickinson, 2011, Mammalian target of rapamycin complex 1 activation is required for the stimulation of human skeletal muscle protein synthesis by essential amino acids, J Nutr, 141, 856

Volpi, 1999, Oral amino acids stimulate muscle protein anabolism in the elderly despite higher first-pass splanchnic extraction, Am J Physiol, 277, E513

Paddon-Jones, 2004, Amino acid ingestion improves muscle protein synthesis in the young and elderly, Am J Physiol Endocrinol Metab, 286, E321, 10.1152/ajpendo.00368.2003

Dreyer, 2008, Leucine-enriched essential amino acid and carbohydrate ingestion following resistance exercise enhances mTOR signaling and protein synthesis in human muscle, Am J Physiol Endocrinol Metab, 294, E392, 10.1152/ajpendo.00582.2007

Dillon, 2009, Amino acid supplementation increases lean body mass, basal muscle protein synthesis, and insulin-like growth factor-I expression in older women, J Clin Endocrinol Metab, 94, 1630, 10.1210/jc.2008-1564

English, 2016, Leucine partially protects muscle mass and function during bed rest in middle-aged adults, Am J Clin Nutr, 103, 465, 10.3945/ajcn.115.112359

Volpi, 1998, Exogenous amino acids stimulate net muscle protein synthesis in the elderly, J Clin Invest, 101, 2000, 10.1172/JCI939

Drummond, 2009, Nutritional and contractile regulation of human skeletal muscle protein synthesis and mTORC1 signaling, J Appl Physiol, 106, 1374, 10.1152/japplphysiol.91397.2008

Krebs, 2007, The Mammalian target of rapamycin pathway regulates nutrient-sensitive glucose uptake in man, Diabetes, 56, 1600, 10.2337/db06-1016

Walker, 2011, Exercise, amino acids, and aging in the control of human muscle protein synthesis, Med Sci Sports Exerc, 43, 2249, 10.1249/MSS.0b013e318223b037

Vendelbo, 2014, Fasting increases human skeletal muscle net phenylalanine release and this is associated with decreased mTOR signaling, PloS One, 9, 10.1371/journal.pone.0102031

Bak, 2016, Differential regulation of lipid and protein metabolism in obese vs. lean subjects before and after a 72-h fast, Am J Physiol Endocrinol Metab, 311, E224, 10.1152/ajpendo.00464.2015

Peng, 2002, The immunosuppressant rapamycin mimics a starvation-like signal distinct from amino acid and glucose deprivation, Mol Cell Biol, 22, 5575, 10.1128/MCB.22.15.5575-5584.2002

Nair, 1987, Leucine, glucose, and energy metabolism after 3 days of fasting in healthy human subjects, Am J Clin Nutr, 46, 557, 10.1093/ajcn/46.4.557

Fryburg, 1990, Effect of starvation on human muscle protein metabolism and its response to insulin, Am J Physiol, 259, E477

Frexes-Steed, 1990, Role of insulin and branched-chain amino acids in regulating protein metabolism during fasting, Am J Physiol, 258, E907

Fry, 2011, Skeletal muscle protein balance and metabolism in the elderly, Curr Aging Sci, 4, 260, 10.2174/1874609811104030260

Drummond, 2009, Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis, J Physiol, 587, 1535, 10.1113/jphysiol.2008.163816

Welle, 1998, High-protein meals do not enhance myofibrillar synthesis after resistance exercise in 62- to 75-yr-old men and women, Am J Physiol, 274, E677

Fry, 2011, Aging impairs contraction-induced human skeletal muscle mTORC1 signaling and protein synthesis, Skeletal Muscle, 1, 11, 10.1186/2044-5040-1-11

Dreyer, 2006, Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle, J Physiol, 576, 613, 10.1113/jphysiol.2006.113175

Fujita, 2009, Essential amino acid and carbohydrate ingestion before resistance exercise does not enhance postexercise muscle protein synthesis, J Appl Physiol, 106, 1730, 10.1152/japplphysiol.90395.2008

Fiatarone, 1994, Exercise training and nutritional supplementation for physical frailty in very elderly people, N Engl J Med, 330, 1769, 10.1056/NEJM199406233302501

Deutz, 2013, Effect of β-hydroxy-β-methylbutyrate (HMB) on lean body mass during 10 days of bed rest in older adults, Clin Nutr, 32, 704, 10.1016/j.clnu.2013.02.011

Mascher, 2007, Changes in signalling pathways regulating protein synthesis in human muscle in the recovery period after endurance exercise, Acta Physiol, 191, 67, 10.1111/j.1748-1716.2007.01712.x

Léger, 2006, Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy, J Physiol, 576, 923, 10.1113/jphysiol.2006.116715

Nair, 1987, Hyperglucagonemia during insulin deficiency accelerates protein catabolism, Am J Physiol, 253, E208

Pacy, 1990, Influence of glucagon on protein and leucine metabolism: a study in fasting man with induced insulin resistance, Br J Surg, 77, 791, 10.1002/bjs.1800770723

Hartl, 1990, Bradykinin attenuates glucagon-induced leucine oxidation in humans, Am J Physiol, 259, E239

Nair, 1987, Failure of carbohydrate to spare leucine oxidation in obese subjects, Int J Obes, 11, 537

Petrides, 1994, Time-dependent regulation by insulin of leucine metabolism in young healthy adults, Am J Physiol, 267, E361

Charlton, 1998, Role of hyperglucagonemia in catabolism associated with type 1 diabetes: effects on leucine metabolism and the resting metabolic rate, Diabetes, 47, 1748, 10.2337/diabetes.47.11.1748

Klein, 1992, In vivo assessment of the metabolic alterations in glucagonoma syndrome, Metabolism, 41, 1171, 10.1016/0026-0495(92)90005-U

Zimmerman, 1989, Contribution of insulin resistance to catabolic effect of prednisone on leucine metabolism in humans, Diabetes, 38, 1238, 10.2337/diab.38.10.1238

Schwenk, 1987, Effects of leucine, isoleucine, or threonine infusion on leucine metabolism in humans, Am J Physiol, 253, E428

Katsanos, 2006, A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly, Am J Physiol Endocrinol Metab, 291, E381, 10.1152/ajpendo.00488.2005

Chiasson, 1975, Gluconeogenesis from alanine in normal postabsorptive man. Intrahepatic stimulatory effect of glucagon, Diabetes, 24, 574, 10.2337/diab.24.6.574

Boden, 1990, Role of glucagon in disposal of an amino acid load, Am J Physiol, 259, E225

Del Prato, 1983, Effect of insulin replacement on intermediary metabolism in diabetes secondary to pancreatectomy, Diabetologia, 25, 252, 10.1007/BF00279939

Vigili de Kreutzenberg, 1990, Glucose turnover and recycling in diabetes secondary to total pancreatectomy: effect of glucagon infusion, J Clin Endocrinol Metab, 70, 1023, 10.1210/jcem-70-4-1023

Almdal, 1990, Increased amino acid clearance and urea synthesis in a patient with glucagonoma, Gut, 31, 946, 10.1136/gut.31.8.946

Freund, 1978, Amino acid derangements in patients with sepsis: treatment with branched chain amino acid rich infusions, Ann Surg, 188, 423, 10.1097/00000658-197809000-00017

Thiessen, 2018, Role of glucagon in protein catabolism, Curr Opin Crit Care, 24, 228, 10.1097/MCC.0000000000000509

Roth, 1987, Free amino acid levels in muscle and liver of a patient with glucagonoma syndrome, Metabolism, 36, 7, 10.1016/0026-0495(87)90055-2

Broyer, 1980, Plasma and muscle free amino acids in children at the early stages of renal failure, Am J Clin Nutr, 33, 1396, 10.1093/ajcn/33.7.1396

Canepa, 1992, Nutritional status and muscle amino acids in children with end-stage renal failure, Kidney Int, 41, 1016, 10.1038/ki.1992.154

Morgan, 2021, Protein source and quality for skeletal muscle anabolism in young and older adults: a systematic review and meta-analysis, J Nutr, 151, 1901

Miki, 2017, Protein intake, especially vegetable protein intake, is associated with higher skeletal muscle mass in elderly patients with type 2 diabetes, J Diabetes Res, 7985728

Gielen, 2021, Nutritional interventions to improve muscle mass, muscle strength, and physical performance in older people: an umbrella review of systematic reviews and meta-analyses, Nutr Rev, 79, 121, 10.1093/nutrit/nuaa011

Morton, 2018, A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults, Br J Sports Med, 52, 376, 10.1136/bjsports-2017-097608

Hevia-Larraín, 2021, High-protein plant-based diet versus a protein-matched omnivorous diet to support resistance training adaptations: a comparison between habitual vegans and omnivores, Sports Med, 51, 1317, 10.1007/s40279-021-01434-9

Connor, 1978, The plasma lipids, lipoproteins, and diet of the Tarahumara indians of Mexico, Am J Clin Nutr, 31, 1131, 10.1093/ajcn/31.7.1131

Walrand, 2008, Functional impact of high protein intake on healthy elderly people, Am J Physiol Endocrinol Metab, 295, E921, 10.1152/ajpendo.90536.2008

Campbell, 1995, Effects of resistance training and dietary protein intake on protein metabolism in older adults, Am J Physiol, 268, E1143

Paddon-Jones, 2008, Role of dietary protein in the sarcopenia of aging, Am J Clin Nutr, 87, 10.1093/ajcn/87.5.1562S

Nieman, 1988, Vegetarian dietary practices and endurance performance, Am J Clin Nutr, 48, 754, 10.1093/ajcn/48.3.754

Goodpaster, 2000, Composition of skeletal muscle evaluated with computed tomography, Ann N Y Acad Sci, 904, 18, 10.1111/j.1749-6632.2000.tb06416.x

Sanada, 2010, A cross-sectional study of sarcopenia in Japanese men and women: reference values and association with cardiovascular risk factors, Eur J Appl Physiol, 110, 57, 10.1007/s00421-010-1473-z

Srikanthan, 2011, Relative muscle mass is inversely associated with insulin resistance and prediabetes. Findings from the third National Health and Nutrition Examination Survey, J Clin Endocrinol Metab, 96, 2898, 10.1210/jc.2011-0435

Chin, 2013, Sarcopenia is independently associated with cardiovascular disease in older Korean adults: the Korea National Health and Nutrition Examination Survey (KNHANES) from 2009, PloS One, 8, 10.1371/journal.pone.0060119

Du, 2018, Associations between sarcopenia and metabolic risk factors: a systematic review and meta-analysis, J Obes Metab Syndr, 27, 175, 10.7570/jomes.2018.27.3.175

Abramowitz, 2018, Muscle mass, BMI, and mortality among adults in the United States: a population-based cohort study, PloS One, 13, 10.1371/journal.pone.0194697

Solerte, 2008, Nutritional supplements with oral amino acid mixtures increases whole-body lean mass and insulin sensitivity in elderly subjects with sarcopenia, Am J Cardiol, 101, 69E, 10.1016/j.amjcard.2008.03.004

Guillet, 2004, Impaired anabolic response of muscle protein synthesis is associated with S6K1 dysregulation in elderly humans, Faseb J, 18, 1586, 10.1096/fj.03-1341fje

Solerte, 2008, Improvement of blood glucose control and insulin sensitivity during a long-term (60 weeks) randomized study with amino acid dietary supplements in elderly subjects with type 2 diabetes mellitus, Am J Cardiol, 101

Volpi, 2000, The response of muscle protein anabolism to combined hyperaminoacidemia and glucose-induced hyperinsulinemia is impaired in the elderly, J Clin Endocrinol Metab, 85, 4481

Cuthbertson, 2005, Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle, Faseb J, 19, 422, 10.1096/fj.04-2640fje

Rasmussen, 2006, Insulin resistance of muscle protein metabolism in aging, Faseb J, 20, 768, 10.1096/fj.05-4607fje

Cleasby, 2016, Insulin resistance and sarcopenia: mechanistic links between common co-morbidities, J Endocrinol, 229, R67, 10.1530/JOE-15-0533

Yoshimura, 2019, Effects of a leucine-enriched amino acid supplement on muscle mass, muscle strength, and physical function in post-stroke patients with sarcopenia: a randomized controlled trial, Nutrition, 58, 1, 10.1016/j.nut.2018.05.028

Drummond, 2008, Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging, J Appl Physiol, 104, 1452, 10.1152/japplphysiol.00021.2008