Skip to main content Accessibility help
×
Home
Hostname: page-component-747cfc64b6-rtmr9 Total loading time: 0.308 Render date: 2021-06-15T05:12:39.759Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true }

Dietary protein, exercise, ageing and physical inactivity: interactive influences on skeletal muscle proteostasis

Published online by Cambridge University Press:  07 October 2020

Colleen S. Deane
Affiliation:
Department of Sport and Health Sciences, College of Life and Environmental Sciences, University of Exeter, Exeter EX1 2LU, UK Living Systems Institute, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
Isabel A. Ely
Affiliation:
MRC Versus Arthritis Centre for Musculoskeletal Ageing Research & NIHR Nottingham Biomedical Research Centre, University of Nottingham, Royal Derby Hospital Centre, Derby DE22 3DT, UK
Daniel J. Wilkinson
Affiliation:
MRC Versus Arthritis Centre for Musculoskeletal Ageing Research & NIHR Nottingham Biomedical Research Centre, University of Nottingham, Royal Derby Hospital Centre, Derby DE22 3DT, UK
Kenneth Smith
Affiliation:
MRC Versus Arthritis Centre for Musculoskeletal Ageing Research & NIHR Nottingham Biomedical Research Centre, University of Nottingham, Royal Derby Hospital Centre, Derby DE22 3DT, UK
Bethan E. Phillips
Affiliation:
MRC Versus Arthritis Centre for Musculoskeletal Ageing Research & NIHR Nottingham Biomedical Research Centre, University of Nottingham, Royal Derby Hospital Centre, Derby DE22 3DT, UK
Philip J. Atherton
Affiliation:
MRC Versus Arthritis Centre for Musculoskeletal Ageing Research & NIHR Nottingham Biomedical Research Centre, University of Nottingham, Royal Derby Hospital Centre, Derby DE22 3DT, UK
Corresponding

Abstract

Dietary protein is a pre-requisite for the maintenance of skeletal muscle mass; stimulating increases in muscle protein synthesis (MPS), via essential amino acids (EAA), and attenuating muscle protein breakdown, via insulin. Muscles are receptive to the anabolic effects of dietary protein, and in particular the EAA leucine, for only a short period (i.e. about 2–3 h) in the rested state. Thereafter, MPS exhibits tachyphylaxis despite continued EAA availability and sustained mechanistic target of rapamycin complex 1 signalling. Other notable characteristics of this ‘muscle full’ phenomenon include: (i) it cannot be overcome by proximal intake of additional nutrient signals/substrates regulating MPS; meaning a refractory period exists before a next stimulation is possible, (ii) it is refractory to pharmacological/nutraceutical enhancement of muscle blood flow and thus is not induced by muscle hypo-perfusion, (iii) it manifests independently of whether protein intake occurs in a bolus or intermittent feeding pattern, and (iv) it does not appear to be dependent on protein dose per se. Instead, the main factor associated with altering muscle full is physical activity. For instance, when coupled to protein intake, resistance exercise delays the muscle full set-point to permit additional use of available EAA for MPS to promote muscle remodelling/growth. In contrast, ageing is associated with blunted MPS responses to protein/exercise (anabolic resistance), while physical inactivity (e.g. immobilisation) induces a premature muscle full, promoting muscle atrophy. It is crucial that in catabolic scenarios, anabolic strategies are sought to mitigate muscle decline. This review highlights regulatory protein turnover interactions by dietary protein, exercise, ageing and physical inactivity.

Type
Research Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below.

References

Rosenberg, IH (1997) Sarcopenia: origins and clinical relevance. J Nutr 127, 990S991S.10.1093/jn/127.5.990SCrossRefGoogle ScholarPubMed
Aversa, Z, Costelli, P & Muscaritoli, M (2017) Cancer-induced muscle wasting: latest findings in prevention and treatment. Ther Adv Med Oncol 9, 369382.10.1177/1758834017698643CrossRefGoogle ScholarPubMed
Sala, D & Zorzano, A (2015) Differential control of muscle mass in type 1 and type 2 diabetes mellitus. Cell Mol Life Sci 72, 38033817.10.1007/s00018-015-1954-7CrossRefGoogle ScholarPubMed
Challal, S, Minichiello, E, Boissier, MC et al. (2016) Cachexia and adiposity in rheumatoid arthritis. Relevance for disease management and clinical outcomes. Joint Bone Spine 83, 127133.10.1016/j.jbspin.2015.04.010CrossRefGoogle ScholarPubMed
Breen, L, Stokes, KA, Churchward-Venne, TA et al. (2013) Two weeks of reduced activity decreases leg lean mass and induces ‘anabolic resistance’ of myofibrillar protein synthesis in healthy elderly. J Clin Endocrinol Metab 98, 26042612.10.1210/jc.2013-1502CrossRefGoogle Scholar
Kilroe, SP, Fulford, J, Holwerda, AM et al. (2020) Short-term muscle disuse induces a rapid and sustained decline in daily myofibrillar protein synthesis rates. Am J Physiol Endocrinol Metab 318, E117E130.10.1152/ajpendo.00360.2019CrossRefGoogle ScholarPubMed
Wolfe, RR (2006) The underappreciated role of muscle in health and disease. Am J Clin Nutr 84, 475482.10.1093/ajcn/84.3.475CrossRefGoogle ScholarPubMed
Guo, Z, Burguera, B & Jensen, MD (2000) Kinetics of intramuscular triglyceride fatty acids in exercising humans. J Appl Physiol (1985) 89, 20572064.10.1152/jappl.2000.89.5.2057CrossRefGoogle ScholarPubMed
Ivy, JL, Katz, AL, Cutler, CL et al. (1988) Muscle glycogen synthesis after exercise: effect of time of carbohydrate ingestion. J Appl Physiol (1985) 64, 14801485.10.1152/jappl.1988.64.4.1480CrossRefGoogle ScholarPubMed
Brook, MS, Wilkinson, DJ & Atherton, PJ (2020) An update on nutrient modulation in the management of disease-induced muscle wasting: evidence from human studies. Curr Opin Clin Nutr Metab Care 23, 174180.10.1097/MCO.0000000000000652CrossRefGoogle ScholarPubMed
Atherton, PJ, Greenhaff, PL, Phillips, SM et al. (2016) Control of skeletal muscle atrophy in response to disuse: clinical/preclinical contentions and fallacies of evidence. Am J Physiol Endocrinol Metab 311, E594604.10.1152/ajpendo.00257.2016CrossRefGoogle ScholarPubMed
Prado, CM, Purcell, SA, Alish, C et al. (2018) Implications of low muscle mass across the continuum of care: a narrative review. Ann Med 50, 675693.10.1080/07853890.2018.1511918CrossRefGoogle ScholarPubMed
Luukinen, H, Koski, K, Laippala, P et al. (1997) Factors predicting fractures during falling impacts among home-dwelling older adults. J Am Geriatr Soc 45, 13021309.10.1111/j.1532-5415.1997.tb02928.xCrossRefGoogle ScholarPubMed
Cruz-Jentoft, AJ, Baeyens, JP, Bauer, JM et al. (2010) Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 39, 412423.10.1093/ageing/afq034CrossRefGoogle ScholarPubMed
Laukkanen, P, Heikkinen, E & Kauppinen, M (1995) Muscle strength and mobility as predictors of survival in 75–84-year-old people. Age Ageing 24, 468473.10.1093/ageing/24.6.468CrossRefGoogle ScholarPubMed
Atherton, PJ & Smith, K (2012) Muscle protein synthesis in response to nutrition and exercise. J Physiol 590, 10491057.10.1113/jphysiol.2011.225003CrossRefGoogle ScholarPubMed
Gorissen, SHM & Witard, OC (2018) Characterising the muscle anabolic potential of dairy, meat and plant-based protein sources in older adults. Proc Nutr Soc 77, 2031.10.1017/S002966511700194XCrossRefGoogle ScholarPubMed
Deane, CS, Bass, JJ, Crossland, H et al. (2020) Animal, plant, collagen and blended dietary proteins: effects on musculoskeletal outcomes. Nutrients 12 [Epublication 1 September 2020].10.3390/nu12092670CrossRefGoogle ScholarPubMed
Gorissen, SH, Remond, D & van Loon, LJ (2015) The muscle protein synthetic response to food ingestion. Meat Sci 109, 96100.10.1016/j.meatsci.2015.05.009CrossRefGoogle ScholarPubMed
Stokes, T, Hector, AJ, Morton, RW et al. (2018) Recent perspectives regarding the role of dietary protein for the promotion of muscle hypertrophy with resistance exercise training. Nutrients 10 [Epublication 7 February 2018].Google ScholarPubMed
Trommelen, J, Betz, MW & van Loon, LJC (2019) The muscle protein synthetic response to meal ingestion following resistance-type exercise. Sports Med 49, 185197.10.1007/s40279-019-01053-5CrossRefGoogle ScholarPubMed
Breen, L & Phillips, SM (2011) Skeletal muscle protein metabolism in the elderly: interventions to counteract the ‘anabolic resistance’ of ageing. Nutr Metab (Lond) 8, 68.10.1186/1743-7075-8-68CrossRefGoogle ScholarPubMed
Brook, MS & Wilkinson, DJ (2020) Contemporary stable isotope tracer approaches: insights into skeletal muscle metabolism in health and disease. Exp Physiol 105, 10811089.10.1113/EP087492CrossRefGoogle ScholarPubMed
Brook, MS, Wilkinson, DJ, Atherton, PJ et al. (2017) Recent developments in deuterium oxide tracer approaches to measure rates of substrate turnover: implications for protein, lipid, and nucleic acid research. Curr Opin Clin Nutr Metab Care 20, 375381.10.1097/MCO.0000000000000392CrossRefGoogle ScholarPubMed
Rennie, MJ (1999) An introduction to the use of tracers in nutrition and metabolism. Proc Nutr Soc 58, 935944.10.1017/S002966519900124XCrossRefGoogle ScholarPubMed
Wilkinson, DJ, Brook, MS, Smith, K et al. (2017) Stable isotope tracers and exercise physiology: past, present and future. J Physiol 595, 28732882.10.1113/JP272277CrossRefGoogle ScholarPubMed
Wilkinson, DJ, Cegielski, J, Phillips, BE et al. (2015) Internal comparison between deuterium oxide (D2O) and L-[ring-13C6] phenylalanine for acute measurement of muscle protein synthesis in humans. Physiol Rep 3 [Epublication 6 July 2015].10.14814/phy2.12433CrossRefGoogle ScholarPubMed
Wilkinson, DJ, Franchi, MV, Brook, MS et al. (2014) A validation of the application of D(2)O stable isotope tracer techniques for monitoring day-to-day changes in muscle protein subfraction synthesis in humans. Am J Physiol Endocrinol Metab 306, E571579.10.1152/ajpendo.00650.2013CrossRefGoogle ScholarPubMed
Rennie, MJ, Edwards, RH, Halliday, D et al. (1982) Muscle protein synthesis measured by stable isotope techniques in man: the effects of feeding and fasting. Clin Sci (Lond) 63, 519523.10.1042/cs0630519CrossRefGoogle ScholarPubMed
Bennet, WM, Connacher, AA, Scrimgeour, CM et al. (1989) Increase in anterior tibialis muscle protein synthesis in healthy man during mixed amino acid infusion: studies of incorporation of [1-13C]leucine. Clin Sci (Lond) 76, 447454.10.1042/cs0760447CrossRefGoogle Scholar
Smith, K, Barua, JM, Watt, PW et al. (1992) Flooding with L-[1-13C]leucine stimulates human muscle protein incorporation of continuously infused L-[1-13C]valine. Am J Physiol 262, E372376.Google Scholar
Smith, K, Reynolds, N, Downie, S et al. (1998) Effects of flooding amino acids on incorporation of labeled amino acids into human muscle protein. Am J Physiol 275, E7378.Google ScholarPubMed
Cuthbertson, D, Smith, K, Babraj, J et al. (2005) Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 19, 422424.10.1096/fj.04-2640fjeCrossRefGoogle ScholarPubMed
Moore, DR, Churchward-Venne, TA, Witard, O et al. (2015) Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men. J Gerontol A Biol Sci Med Sci 70, 5762.10.1093/gerona/glu103CrossRefGoogle ScholarPubMed
Moore, DR, Robinson, MJ, Fry, JL et al. (2009) Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am J Clin Nutr 89, 161168.10.3945/ajcn.2008.26401CrossRefGoogle ScholarPubMed
Symons, TB, Sheffield-Moore, M, Wolfe, RR et al. (2009) A moderate serving of high-quality protein maximally stimulates skeletal muscle protein synthesis in young and elderly subjects. J Am Diet Assoc 109, 15821586.10.1016/j.jada.2009.06.369CrossRefGoogle Scholar
Witard, OC, Jackman, SR, Breen, L et al. (2014) Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise. Am J Clin Nutr 99, 8695.10.3945/ajcn.112.055517CrossRefGoogle ScholarPubMed
Macnaughton, LS, Wardle, SL, Witard, OC et al. (2016) The response of muscle protein synthesis following whole-body resistance exercise is greater following 40 g than 20 g of ingested whey protein. Physiol Rep 4 [Epublication 4 August 2016].10.14814/phy2.12893CrossRefGoogle ScholarPubMed
Wilkinson, DJ, Hossain, T, Hill, DS et al. (2013) Effects of leucine and its metabolite beta-hydroxy-beta-methylbutyrate on human skeletal muscle protein metabolism. J Physiol 591, 29112923.CrossRefGoogle ScholarPubMed
Bukhari, SS, Phillips, BE, Wilkinson, DJ et al. (2015) Intake of low-dose leucine-rich essential amino acids stimulates muscle anabolism equivalently to bolus whey protein in older women at rest and after exercise. Am J Physiol Endocrinol Metab 308, E10561065.10.1152/ajpendo.00481.2014CrossRefGoogle ScholarPubMed
Benelam, B (2009) Satiety and the anorexia of ageing. Br J Community Nurs 14, 332335.10.12968/bjcn.2009.14.8.43512CrossRefGoogle ScholarPubMed
Burd, NA, Yang, Y, Moore, DR et al. (2012) Greater stimulation of myofibrillar protein synthesis with ingestion of whey protein isolate v. micellar casein at rest and after resistance exercise in elderly men. Br J Nutr 108, 958962.CrossRefGoogle ScholarPubMed
Pennings, B, Boirie, Y, Senden, JM et al. (2011) Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. Am J Clin Nutr 93, 9971005.CrossRefGoogle ScholarPubMed
Mitchell, WK, Phillips, BE, Williams, JP et al. (2015) The impact of delivery profile of essential amino acids upon skeletal muscle protein synthesis in older men: clinical efficacy of pulse vs. bolus supply. Am J Physiol Endocrinol Metab 309, E450457.CrossRefGoogle ScholarPubMed
Wagenmakers, AJ (1998) Protein and amino acid metabolism in human muscle. Adv Exp Med Biol 441, 307319.CrossRefGoogle ScholarPubMed
Mitchell, WK, Wilkinson, DJ, Phillips, BE et al. (2016) Human skeletal muscle protein metabolism responses to amino acid nutrition. Adv Nutr 7, 828S838S.CrossRefGoogle ScholarPubMed
Escobar, J, Frank, JW, Suryawan, A et al. (2010) Leucine and alpha-ketoisocaproic acid, but not norleucine, stimulate skeletal muscle protein synthesis in neonatal pigs. J Nutr 140, 14181424.CrossRefGoogle Scholar
Van Koevering, M & Nissen, S (1992) Oxidation of leucine and alpha-ketoisocaproate to beta-hydroxy-beta-methylbutyrate in vivo. Am J Physiol 262, E2731.Google ScholarPubMed
Wilkinson, DJ, Hossain, T, Limb, MC et al. (2018) Impact of the calcium form of beta-hydroxy-beta-methylbutyrate upon human skeletal muscle protein metabolism. Clin Nutr 37, 20682075.CrossRefGoogle ScholarPubMed
Deane, CS, Wilkinson, DJ, Phillips, BE et al. (2017) ‘Nutraceuticals’ in relation to human skeletal muscle and exercise. Am J Physiol Endocrinol Metab 312, E282E299.CrossRefGoogle Scholar
Atherton, PJ, Etheridge, T, Watt, PW et al. (2010) Muscle full effect after oral protein: time-dependent concordance and discordance between human muscle protein synthesis and mTORC1 signaling. Am J Clin Nutr 92, 10801088.CrossRefGoogle ScholarPubMed
Wilson, GJ, Layman, DK, Moulton, CJ et al. (2011) Leucine or carbohydrate supplementation reduces AMPK and eEF2 phosphorylation and extends postprandial muscle protein synthesis in rats. Am J Physiol Endocrinol Metab 301, E12361242.CrossRefGoogle ScholarPubMed
Wilson, GJ, Moulton, CJ, Garlick, PJ et al. (2012) Post-meal responses of elongation factor 2 (eEF2) and adenosine monophosphate-activated protein kinase (AMPK) to leucine and carbohydrate supplements for regulating protein synthesis duration and energy homeostasis in rat skeletal muscle. Nutrients 4, 17231739.CrossRefGoogle ScholarPubMed
Mitchell, WK, Phillips, BE, Hill, I et al. (2017) Human skeletal muscle is refractory to the anabolic effects of leucine during the postprandial muscle-full period in older men. Clin Sci (Lond) 131, 26432653.CrossRefGoogle ScholarPubMed
Phillips, BE, Atherton, PJ, Varadhan, K et al. (2014) Pharmacological enhancement of leg and muscle microvascular blood flow does not augment anabolic responses in skeletal muscle of young men under fed conditions. Am J Physiol Endocrinol Metab 306, E168176.CrossRefGoogle Scholar
Phillips, BE, Atherton, PJ, Varadhan, K et al. (2016) Acute cocoa flavanol supplementation improves muscle macro- and microvascular but not anabolic responses to amino acids in older men. Appl Physiol Nutr Metab 41, 548556.CrossRefGoogle Scholar
Kimball, SR (2014) Integration of signals generated by nutrients, hormones, and exercise in skeletal muscle. Am J Clin Nutr 99, 237S242S.CrossRefGoogle ScholarPubMed
Wolfson, RL, Chantranupong, L, Saxton, RA et al. (2016) Sestrin2 is a leucine sensor for the mTORC1 pathway. Science 351, 4348.CrossRefGoogle ScholarPubMed
Proud, CG (2009) mTORC1 signalling and mRNA translation. Biochem Soc Trans 37, 227231.CrossRefGoogle ScholarPubMed
Proud, CG (2011) mTOR signalling in health and disease. Biochem Soc Trans 39, 431436.CrossRefGoogle ScholarPubMed
Wilkes, EA, Selby, AL, Atherton, PJ et al. (2009) Blunting of insulin inhibition of proteolysis in legs of older subjects may contribute to age-related sarcopenia. Am J Clin Nutr 90, 13431350.CrossRefGoogle ScholarPubMed
Greenhaff, PL, Karagounis, LG, Peirce, N et al. (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, E595604.CrossRefGoogle ScholarPubMed
Abdulla, H, Smith, K, Atherton, PJ et al. (2016) Role of insulin in the regulation of human skeletal muscle protein synthesis and breakdown: a systematic review and meta-analysis. Diabetologia 59, 4455.CrossRefGoogle ScholarPubMed
Biolo, G, Maggi, SP, Williams, BD et al. (1995) Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol 268, E514520.Google ScholarPubMed
Pennings, B, Koopman, R, Beelen, M et al. (2011) Exercising before protein intake allows for greater use of dietary protein-derived amino acids for de novo muscle protein synthesis in both young and elderly men. Am J Clin Nutr 93, 322331.CrossRefGoogle Scholar
Staples, AW, Burd, NA, West, DW et al. (2011) Carbohydrate does not augment exercise-induced protein accretion versus protein alone. Med Sci Sports Exerc 43, 11541161.CrossRefGoogle Scholar
Burd, NA, West, DW, Moore, DR et al. (2011) Enhanced amino acid sensitivity of myofibrillar protein synthesis persists for up to 24 h after resistance exercise in young men. J Nutr 141, 568573.CrossRefGoogle ScholarPubMed
Wilkinson, DJ, Piasecki, M & Atherton, PJ (2018) The age-related loss of skeletal muscle mass and function: measurement and physiology of muscle fibre atrophy and muscle fibre loss in humans. Ageing Res Rev 47, 123132.CrossRefGoogle ScholarPubMed
Welle, S, Thornton, C, Jozefowicz, R et al. (1993) Myofibrillar protein synthesis in young and old men. Am J Physiol 264, E693698.Google Scholar
Welle, S, Thornton, C & Statt, M (1995) Myofibrillar protein synthesis in young and old human subjects after three months of resistance training. Am J Physiol 268, E422427.Google Scholar
Phillips, BE, Hill, DS & Atherton, PJ (2012) Regulation of muscle protein synthesis in humans. Curr Opin Clin Nutr Metab Care 15, 5863.CrossRefGoogle ScholarPubMed
Wall, BT, Gorissen, SH, Pennings, B et al. (2015) Aging is accompanied by a blunted muscle protein synthetic response to protein ingestion. PLoS ONE 10, e0140903.CrossRefGoogle ScholarPubMed
Marshall, RN, Smeuninx, B, Morgan, PT et al. (2020) Nutritional strategies to offset disuse-induced skeletal muscle atrophy and anabolic resistance in older adults: from whole-foods to isolated ingredients. Nutrients 12 [Epublication 25 May 2020].CrossRefGoogle ScholarPubMed
Brook, MS, Wilkinson, DJ, Mitchell, WK et al. (2016) Synchronous deficits in cumulative muscle protein synthesis and ribosomal biogenesis underlie age-related anabolic resistance to exercise in humans. J Physiol 594, 73997417.CrossRefGoogle ScholarPubMed
Mitchell, WK, Williams, J, Atherton, P et al. (2012) Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol 3, 260.CrossRefGoogle ScholarPubMed
Chevalier, S, Goulet, ED, Burgos, SA et al. (2011) Protein anabolic responses to a fed steady state in healthy aging. J Gerontol A Biol Sci Med Sci 66, 681688.CrossRefGoogle Scholar
Bauer, J, Biolo, G, Cederholm, T et al. (2013) Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group. J Am Med Dir Assoc 14, 542559.CrossRefGoogle ScholarPubMed
Atherton, PJ, Kumar, V, Selby, AL et al. (2017) Enriching a protein drink with leucine augments muscle protein synthesis after resistance exercise in young and older men. Clin Nutr 36, 888895.CrossRefGoogle Scholar
Jackman, SR, Witard, OC, Philp, A et al. (2017) Branched-chain amino acid ingestion stimulates muscle myofibrillar protein synthesis following resistance exercise in humans. Front Physiol 8, 390.CrossRefGoogle ScholarPubMed
Fuchs, CJ, Hermans, WJH, Holwerda, AM et al. (2019) Branched-chain amino acid and branched-chain ketoacid ingestion increases muscle protein synthesis rates in vivo in older adults: a double-blind, randomized trial. Am J Clin Nutr 110, 862872.CrossRefGoogle ScholarPubMed
van Vliet, S, Smith, GI, Porter, L et al. (2018) The muscle anabolic effect of protein ingestion during a hyperinsulinaemic euglycaemic clamp in middle-aged women is not caused by leucine alone. J Physiol 596, 46814692.CrossRefGoogle Scholar
Bell, KE, Brook, MS, Snijders, T et al. (2019) Integrated myofibrillar protein synthesis in recovery from unaccustomed and accustomed resistance exercise with and without multi-ingredient supplementation in overweight older men. Front Nutr 6, 40.CrossRefGoogle ScholarPubMed
Kumar, V, Selby, A, Rankin, D et al. (2009) Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 587, 211217.CrossRefGoogle Scholar
Fry, CS, Glynn, EL, Drummond, MJ et al. (2010) Blood flow restriction exercise stimulates mTORC1 signaling and muscle protein synthesis in older men. J Appl Physiol (1985) 108, 11991209.CrossRefGoogle ScholarPubMed
Durham, WJ, Casperson, SL, Dillon, EL et al. (2010) Age-related anabolic resistance after endurance-type exercise in healthy humans. FASEB J 24, 41174127.CrossRefGoogle ScholarPubMed
Drummond, MJ, Glynn, EL, Fry, CS et al. (2010) An increase in essential amino acid availability upregulates amino acid transporter expression in human skeletal muscle. Am J Physiol Endocrinol Metab 298, E10111018.CrossRefGoogle ScholarPubMed
Burd, NA, West, DW, Staples, AW et al. (2010) Low-load high volume resistance exercise stimulates muscle protein synthesis more than high-load low volume resistance exercise in young men. PLoS ONE 5, e12033.CrossRefGoogle ScholarPubMed
de Boer, MD, Selby, A, Atherton, P et al. (2007) The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585, 241251.CrossRefGoogle ScholarPubMed
Glover, EI, Phillips, SM, Oates, BR et al. (2008) Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol 586, 60496061.CrossRefGoogle ScholarPubMed
McGlory, C, Gorissen, SHM, Kamal, M et al. (2019) Omega-3 fatty acid supplementation attenuates skeletal muscle disuse atrophy during two weeks of unilateral leg immobilization in healthy young women. FASEB J 33, 45864597.CrossRefGoogle ScholarPubMed
Shad, BJ, Thompson, JL, Holwerda, AM et al. (2019) One week of step reduction lowers myofibrillar protein synthesis rates in young men. Med Sci Sports Exerc 51, 21252134.CrossRefGoogle ScholarPubMed
Wall, BT, Dirks, ML, Snijders, T et al. (2016) Short-term muscle disuse lowers myofibrillar protein synthesis rates and induces anabolic resistance to protein ingestion. Am J Physiol Endocrinol Metab 310, E137147.CrossRefGoogle ScholarPubMed
Wall, BT, Snijders, T, Senden, JM et al. (2013) Disuse impairs the muscle protein synthetic response to protein ingestion in healthy men. J Clin Endocrinol Metab 98, 48724881.CrossRefGoogle ScholarPubMed
Dirks, ML, Wall, BT, van de Valk, B et al. (2016) One week of bed rest leads to substantial muscle atrophy and induces whole-body insulin resistance in the absence of skeletal muscle lipid accumulation. Diabetes 65, 28622875.CrossRefGoogle ScholarPubMed
Wall, BT, Dirks, ML, van Loon, LJ (2013) Skeletal muscle atrophy during short-term disuse: implications for age-related sarcopenia. Ageing Res Rev 12, 898906.CrossRefGoogle ScholarPubMed
McGlory, C, von Allmen, MT, Stokes, T et al. (2018) Failed recovery of glycemic control and myofibrillar protein synthesis with 2 wk of physical inactivity in overweight, prediabetic older adults. J Gerontol A Biol Sci Med Sci 73, 10701077.CrossRefGoogle ScholarPubMed
Suetta, C, Hvid, LG, Justesen, L et al. (2009) Effects of aging on human skeletal muscle after immobilization and retraining. J Appl Physiol (1985) 107, 11721180.CrossRefGoogle ScholarPubMed
Pennings, B, Groen, BB, van Dijk, JW et al. (2013) Minced beef is more rapidly digested and absorbed than beef steak, resulting in greater postprandial protein retention in older men. Am J Clin Nutr 98, 121128.CrossRefGoogle ScholarPubMed
Pennings, B, Groen, B, de Lange, A et al. (2012) Amino acid absorption and subsequent muscle protein accretion following graded intakes of whey protein in elderly men. Am J Physiol Endocrinol Metab 302, E992999.CrossRefGoogle ScholarPubMed
Mitchell, CJ, D'Souza, RF, Mitchell, SM et al. (2018) Impact of dairy protein during limb immobilization and recovery on muscle size and protein synthesis; a randomized controlled trial. J Appl Physiol (1985) 124, 717728.CrossRefGoogle ScholarPubMed
Kilroe, SP, Fulford, J, Jackman, S et al. (2020) Dietary protein intake does not modulate daily myofibrillar protein synthesis rates or loss of muscle mass and function during short-term immobilization in young men: a randomized controlled trial. Am J Clin Nutr [Epublication ahead of print version].Google Scholar
Paddon-Jones, D, Sheffield-Moore, M, Urban, RJ et al. (2005) The catabolic effects of prolonged inactivity and acute hypercortisolemia are offset by dietary supplementation. J Clin Endocrinol Metab 90, 14531459.CrossRefGoogle ScholarPubMed
Paddon-Jones, D, Sheffield-Moore, M, Urban, RJ et al. (2004) Essential amino acid and carbohydrate supplementation ameliorates muscle protein loss in humans during 28 days bedrest. J Clin Endocrinol Metab 89, 43514358.CrossRefGoogle ScholarPubMed
English, KL, Mettler, JA, Ellison, JB et al. (2016) Leucine partially protects muscle mass and function during bed rest in middle-aged adults. Am J Clin Nutr 103, 465473.CrossRefGoogle ScholarPubMed
Backx, EMP, Horstman, AMH, Marzuca-Nassr, GN et al. (2018) Leucine supplementation does not attenuate skeletal muscle loss during leg immobilization in healthy, young men. Nutrients 10 [Epublication 17 May 2018].CrossRefGoogle Scholar
Davies, RW, Bass, JJ, Carson, BP et al. (2019) Differential stimulation of post-exercise myofibrillar protein synthesis in humans following isonitrogenous, isocaloric pre-exercise feeding. Nutrients 11 [Epublication 19 July 2019].CrossRefGoogle ScholarPubMed
Holloway, TM, McGlory, C, McKellar, S et al. (2019) A novel amino acid composition ameliorates short-term muscle disuse atrophy in healthy young men. Front Nutr 6, 105.CrossRefGoogle ScholarPubMed
Nishizaki, K, Ikegami, H, Tanaka, Y et al. (2015) Effects of supplementation with a combination of beta-hydroxy-beta-methyl butyrate, L-arginine, and L-glutamine on postoperative recovery of quadriceps muscle strength after total knee arthroplasty. Asia Pac J Clin Nutr 24, 412420.Google ScholarPubMed
Mitchell, WK, Phillips, BE, Wilkinson, DJ et al. (2017) Supplementing essential amino acids with the nitric oxide precursor, l-arginine, enhances skeletal muscle perfusion without impacting anabolism in older men. Clin Nutr 36, 15731579.CrossRefGoogle ScholarPubMed
Chantranupong, L, Scaria, SM, Saxton, RA et al. (2016) The CASTOR proteins are arginine sensors for the mTORC1 pathway. Cell 165, 153164.CrossRefGoogle ScholarPubMed
Bamman, MM, Clarke, MS, Feeback, DL et al. (1998) Impact of resistance exercise during bed rest on skeletal muscle sarcopenia and myosin isoform distribution. J Appl Physiol (1985) 84, 157163.CrossRefGoogle ScholarPubMed
Oates, BR, Glover, EI, West, DW et al. (2010) Low-volume resistance exercise attenuates the decline in strength and muscle mass associated with immobilization. Muscle Nerve 42, 539546.CrossRefGoogle ScholarPubMed
Dirks, ML, Groen, BB, Franssen, R et al. (2017) Neuromuscular electrical stimulation prior to presleep protein feeding stimulates the use of protein-derived amino acids for overnight muscle protein synthesis. J Appl Physiol (1985) 122, 2027.CrossRefGoogle ScholarPubMed
Dirks, ML, Wall, BT, Snijders, T et al. (2014) Neuromuscular electrical stimulation prevents muscle disuse atrophy during leg immobilization in humans. Acta Physiol (Oxf) 210, 628641.CrossRefGoogle ScholarPubMed
Arentson-Lantz, EJ, Fiebig, KN, Anderson-Catania, KJ et al. (2020) Countering disuse atrophy in older adults with low-volume leucine supplementation. J Appl Physiol (1985) 128, 967977.CrossRefGoogle ScholarPubMed
He, W, Sengupta, M, Velkoff, VA et al. (2005) 65+ in the United States: 2005. Current Population Reports.Google Scholar
Dirks, ML, Wall, BT, Nilwik, R et al. (2014) Skeletal muscle disuse atrophy is not attenuated by dietary protein supplementation in healthy older men. J Nutr 144, 11961203.CrossRefGoogle Scholar
Kortebein, P, Ferrando, A, Lombeida, J et al. (2007) Effect of 10 days of bed rest on skeletal muscle in healthy older adults. JAMA 297, 17721774.CrossRefGoogle ScholarPubMed
Ferrando, AA, Lane, HW, Stuart, CA et al. (1996) Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol 270, E627633.Google ScholarPubMed
Ferrando, AA, Paddon-Jones, D, Hays, NP et al. (2010) EAA Supplementation to increase nitrogen intake improves muscle function during bed rest in the elderly. Clin Nutr 29, 1823.CrossRefGoogle ScholarPubMed
Flakoll, P, Sharp, R, Baier, S et al. (2004) Effect of beta-hydroxy-beta-methylbutyrate, arginine, and lysine supplementation on strength, functionality, body composition, and protein metabolism in elderly women. Nutrition 20, 445451.CrossRefGoogle ScholarPubMed
Deutz, NE, Pereira, SL, Hays, NP et al. (2013) Effect of beta-hydroxy-beta-methylbutyrate (HMB) on lean body mass during 10 days of bed rest in older adults. Clin Nutr 32, 704712.CrossRefGoogle ScholarPubMed
Mahoney, JE (1999) Gender differences in hallway ambulation by older adults hospitalized for medical illness. WMJ 98, 4043.Google ScholarPubMed
Reidy, PT, McKenzie, AI, Brunker, P et al. (2017) Neuromuscular electrical stimulation combined with protein ingestion preserves thigh muscle mass but not muscle function in healthy older adults during 5 days of bed rest. Rejuvenation Res 20, 449461.CrossRefGoogle Scholar
Phillips, SM, Paddon-Jones, D, Layman, DK (2020) Optimizing adult protein intake during catabolic health conditions. Adv Nutr 11, S1058S1069.CrossRefGoogle ScholarPubMed
2
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Dietary protein, exercise, ageing and physical inactivity: interactive influences on skeletal muscle proteostasis
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Dietary protein, exercise, ageing and physical inactivity: interactive influences on skeletal muscle proteostasis
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Dietary protein, exercise, ageing and physical inactivity: interactive influences on skeletal muscle proteostasis
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *