Skeletal muscle disuse atrophy is not attenuated by dietary protein supplementation in healthy older men

Journal of Nutrition

Volumn 144, Issue 8, 2014, Pages 1196-1203

  Dirks, Marlou L ^a   Wall, Benjamin T ^a   Nilwik, Rachel ^a   Weerts, Daniëlle H J M ^b   Verdijk, Lex B ^a   van Loon, Luc J C ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ATROGIN 1; CARBOHYDRATE; F BOX PROTEIN; MESSENGER RNA; MUSCLE RING FINGER 1 PROTEIN; MYOGENIN; MYOSTATIN; PROTEIN;

AGED; ARTICLE; ATROPHY; CAST APPLICATION; COMPARATIVE STUDY; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DIET SUPPLEMENTATION; GENE OVEREXPRESSION; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; IMMOBILIZATION; LEG MUSCLE; MALE; MUSCLE ATROPHY; MUSCLE BIOPSY; MUSCLE CELL; MUSCLE MASS; MUSCLE STRENGTH; NORMAL HUMAN; PROTEIN INTAKE; QUADRICEPS FEMORIS MUSCLE; SKELETAL MUSCLE; SKELETAL MUSCLE DISUSE ATROPHY;

AGED; DIET; DIETARY PROTEINS; DIETARY SUPPLEMENTS; ENERGY INTAKE; HUMANS; IMMOBILIZATION; MALE; MUSCLE PROTEINS; MUSCLE STRENGTH; MUSCULAR DISORDERS, ATROPHIC; MYOGENIN; MYOSTATIN; QUADRICEPS MUSCLE; QUESTIONNAIRES; RNA, MESSENGER; SARCOPENIA; UBIQUITIN-PROTEIN LIGASES;

EID: 84904279765     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.114.194217     Document Type: Article

References (57)

1. Deitrick JE. The effect of immobilization on metabolic and physiological functions of normal men. Bull N Y Acad Med 1948;24:364-75.
2. Ingemann-Hansen T, Halkjaer-Kristensen J. Computerized tomographic determination of human thigh components. The effects of immobilization in plaster and subsequent physical training. Scand J Rehabil Med 1980;12:27-31.
3. White MJ, Davies CT, Brooksby P. The effects of short-term voluntary immobilization on the contractile properties of the human triceps surae. Q J Exp Physiol 1984;69:685-91.
4. LeBlanc AD, Schneider VS, Evans HJ, Pientok C, Rowe R, Spector E. Regional changes in muscle mass following 17 weeks of bed rest. J Appl Physiol 1992;73:2172-8.
5. Stuart CA, Shangraw RE, Prince MJ, Peters EJ,Wolfe RR. Bed-rest-induced insulin resistance occurs primarily in muscle. Metabolism 1988; 37:802-6.
6. Haruna Y, Suzuki Y, Kawakubo K, Yanagibori R, Gunji A. Decremental reset in basal metabolism during 20-days bed rest. Acta Physiol Scand Suppl 1994;616:43-9.
7. Tzankoff SP, Norris AH. Effect of muscle mass decrease on age-related BMR changes. J Appl Physiol 1977;43:1001-6.
8. Dirks ML, Wall BT, Snijders T, Ottenbros CL, Verdijk LB, van Loon LJ. Neuromuscular electrical stimulation prevents muscle disuse atrophy during leg immobilization in humans. Acta Physiol (Oxf) 2014;210:628-41.
9. Wall BT, Dirks ML, Snijders T, Senden JM, Dolmans J, van Loon LJ. Substantial skeletal muscle loss occurs during only 5 days of disuse. Acta Physiol (Oxf) 2014;210:600-11.
10. Suetta C, Frandsen U, Jensen L, Jensen MM, Jespersen JG, Hvid LG, Bayer M, Petersson SJ, Schroder HD, Andersen JL, et al. Aging affects the transcriptional regulation of human skeletal muscle disuse atrophy. PLoS ONE 2012;7:e51238.
11. Fisher SR, Kuo YF, Graham JE, Ottenbacher KJ, Ostir GV. Early ambulation and length of stay in older adults hospitalized for acute illness. Arch Intern Med 2010;170:1942-3.
12. English KL, Paddon-Jones D. Protecting muscle mass and function in older adults during bed rest. Curr Opin Clin Nutr Metab Care 2010;13:34-9.
13. Wall BT, Dirks ML, van Loon LJ. Skeletal muscle atrophy during shortterm disuse: implications for age-related sarcopenia. Ageing Res Rev 2013;12:898-906.
14. Ferrando AA, Lane HW, Stuart CA, Davis-Street J, Wolfe RR. Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol 1996;270:E627-33.
15. Ferrando AA, Tipton KD, Bamman MM,Wolfe RR. Resistance exercise maintains skeletal muscle protein synthesis during bed rest. J Appl Physiol 1997;82:807-10.
16. Kortebein P, Ferrando A, Lombeida J, Wolfe R, Evans WJ. Effect of 10 days of bed rest on skeletal muscle in healthy older adults. JAMA 2007;297:1772-4.
17. Glover EI, Phillips SM, Oates BR, Tang JE, Tarnopolsky MA, Selby A, Smith K, Rennie MJ. Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol 2008;586:6049-61.
18. Gibson JN, Halliday D, Morrison WL, Stoward PJ, Hornsby GA, Watt PW, Murdoch G, Rennie MJ. Decrease in human quadriceps muscle protein turnover consequent upon leg immobilization. Clin Sci (Lond) 1987;72:503-9.
19. de Boer MD, Selby A, Atherton P, Smith K, Seynnes OR, Maganaris CN, Maffulli N, Movin T, Narici MV, Rennie MJ. The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 2007;585:241-51.
20. Wall BT, Snijders T, Senden JM, Ottenbros CL, Gijsen AP, Verdijk LB, van Loon LJ. Disuse impairs the muscle protein synthetic response to protein ingestion in healthy men. J Clin Endocrinol Metab 2013;98:4872-81.
21. Biolo G, Ciocchi B, Lebenstedt M, Barazzoni R, Zanetti M, Platen P, Heer M, Guarnieri G. Short-term bed rest impairs amino acid-induced protein anabolism in humans. J Physiol 2004;558:381-8.
22. Biolo G, Ciocchi B, Lebenstedt M, Heer M, Guarnieri G. Sensitivity of whole body protein synthesis to amino acid administration during short-term bed rest. J Gravit Physiol 2002;9:P197-8.
23. Abadi A, Glover EI, Isfort RJ, Raha S, Safdar A, Yasuda N, Kaczor JJ, Melov S, Hubbard A, Qu X, et al. Limb immobilization induces a coordinate down-regulation of mitochondrial and other metabolic pathways in men and women. PLoS ONE 2009;4:e6518.
24. Glover EI, Yasuda N, Tarnopolsky MA, Abadi A, Phillips SM. Little change in markers of protein breakdown and oxidative stress in humans in immobilization-induced skeletal muscle atrophy. Appl Physiol Nutr Metab 2010;35:125-33.
25. Gustafsson T, Osterlund T, Flanagan JN, von Walden F, Trappe TA, Linnehan RM, Tesch PA. Effects of 3 days unloading on molecular regulators of muscle size in humans. J Appl Physiol 2010;109:721-7.
26. Phillips SM, Glover EI, Rennie MJ. Alterations of protein turnover underlying disuse atrophy in human skeletal muscle. J Appl Physiol 2009;107:645-54.
27. Wall BT, van Loon LJ. Nutritional strategies to attenuate muscle disuse atrophy. Nutr Rev 2013;71:195-208.
28. Rennie MJ, Edwards RH, Halliday D, Matthews DE, Wolman SL, Millward DJ. Muscle protein synthesis measured by stable isotope techniques in man: the effects of feeding and fasting. Clin Sci (Lond) 1982;63:519-23.
29. Paddon-Jones D, Sheffield-Moore M, Urban RJ, Sanford AP, Aarsland A, Wolfe RR, Ferrando AA. Essential amino acid and carbohydrate supplementation ameliorates muscle protein loss in humans during 28 days bedrest. J Clin Endocrinol Metab 2004;89:4351-8.
30. Stein TP, Donaldson MR, Leskiw MJ, Schluter MD, Baggett DW, Boden G. Branched-chain amino acid supplementation during bed rest: effect on recovery. J Appl Physiol 2003;94:1345-52.
31. Stuart CA, Shangraw RE, Peters EJ, Wolfe RR. Effect of dietary protein on bed-rest-related changes in whole-body-protein synthesis. Am J Clin Nutr 1990;52:509-14.
32. Ferrando AA, Paddon-Jones D, Hays NP, Kortebein P, Ronsen O, Williams RH, McComb A, Symons TB, Wolfe RR, Evans W. EAA supplementation to increase nitrogen intake improves muscle function during bed rest in the elderly. Clin Nutr 2010;29:18-23.
33. Verdijk LB, Koopman R, Schaart G, Meijer K, Savelberg HH, van Loon LJ. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab 2007;292:E151-7.
34. Waterval WA, Scheijen JL, Ortmans-Ploemen MM, Habets-van der Poel CD, Bierau J. Quantitative UPLC-MS/MS analysis of underivatised amino acids in body fluids is a reliable tool for the diagnosis and followup of patients with inborn errors of metabolism. Clin Chim Acta 2009;407:36-42.
35. Bonstato. Dieetinzicht. 2012 [cited 2013 July 18]. Available from: www.dieetinzicht.nl.
36. Hallal PC, Andersen LB, Bull FC, Guthold R, Haskell W, Ekelund U, Lancet Physical Activity Series Working Group. Global physical activity levels: surveillance progress, pitfalls, and prospects. Lancet 2012;380:247-57.
37. Suetta C, Frandsen U, Mackey AL, Jensen L, Hvid LG, Bayer ML, Petersson SJ, Schroder HD, Andersen JL, Aagaard P, et al. Ageing is associated with diminished muscle re-growth and myogenic precursor cell expansion early after immobility-induced atrophy in human skeletal muscle. J Physiol 2013;591:3789-804.
38. Stein TP, Blanc S. Does protein supplementation prevent muscle disuse atrophy and loss of strength? Crit Rev Food Sci Nutr 2011;51:828-34.
39. Trappe TA, Burd NA, Louis ES, Lee GA, Trappe SW. Influence of concurrent exercise or nutrition countermeasures on thigh and calf muscle size and function during 60 days of bed rest in women. Acta Physiol (Oxf) 2007;191:147-59.
40. Pennings B, Boirie Y, Senden JMG, Gijsen AP, Kuipers H, van Loon LJC. Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. Am J Clin Nutr 2011;93:997-1005.
41. Tieland M, Borgonjen-Van den Berg KJ, van Loon LJ, de Groot LC. Dietary protein intake in community-dwelling, frail, and institutionalized elderly people: scope for improvement. Eur J Nutr 2012;51:173-9.
42. Pennings B, Groen B, de Lange A, Gijsen AP, Zorenc AH, Senden JM, van Loon LJ. Amino acid absorption and subsequent muscle protein accretion following graded intakes of whey protein in elderly men. Am J Physiol Endocrinol Metab 2012;302:E992-9.
43. Groen BB, Res PT, Pennings B, Hertle E, Senden JM, Saris WH, van Loon LJ. Intragastric protein administration stimulates overnight muscle protein synthesis in elderly men. Am J Physiol Endocrinol Metab 2012;302:E52-60.
44. Boirie Y, Dangin M, Gachon P, Vasson MP, Maubois JL, Beaufrere B. Slow and fast dietary proteins differently modulate postprandial protein accretion. Proc Natl Acad Sci USA 1997;94:14930-5.
45. Garlick PJ, McNurlan MA, Ballmer PE. Influence of dietary protein intake on whole-body protein turnover in humans. Diabetes Care 1991;14:1189-98.
46. Res PT, Groen B, Pennings B, Beelen M, Wallis GA, Gijsen AP, Senden JM, VAN Loon LJ. Protein ingestion before sleep improves postexercise overnight recovery. Med Sci Sports Exerc 2012;44:1560-9.
47. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997;387:83-90.
48. McFarlane C, Plummer E, Thomas M, Hennebry A, Ashby M, Ling N, Smith H, Sharma M, Kambadur R. Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-kappaBindependent, FoxO1-dependent mechanism. J Cell Physiol 2006;209: 501-14.
49. Amthor H, Huang R,McKinnell I, Christ B, Kambadur R, Sharma M, Patel K. The regulation and action of myostatin as a negative regulator of muscle development during avian embryogenesis. Dev Biol 2002;251:241-57.
50. Snijders T, Wall BT, Dirks ML, Senden JM, Hartgens F, Dolmans J, Losen M, Verdijk LB, van Loon LJ. Muscle disuse atrophy is not accompanied by changes in skeletal muscle satellite cell content. Clin Sci (Lond) 2014;126:557-66.
51. Dickinson JM, Rasmussen BB. Essential amino acid sensing, signaling, and transport in the regulation of human muscle protein metabolism. Curr Opin Clin Nutr Metab Care 2011;14:83-8.
52. Dickinson JM, Rasmussen BB. Amino acid transporters in the regulation of human skeletal muscle protein metabolism. Curr Opin Clin Nutr Metab Care 2013;16:638-44.
53. Oates BR, Glover EI, West DW, Fry JL, Tarnopolsky MA, Phillips SM. Low-volume resistance exercise attenuates the decline in strength and muscle mass associated with immobilization. Muscle Nerve 2010; 42:539-46.
54. Hespel P, Op't Eijnde B, Van Leemputte M, Urso B, Greenhaff PL, Labarque V, Dymarkowski S, Van Hecke P, Richter EA. Oral creatine supplementation facilitates the rehabilitation of disuse atrophy and alters the expression of muscle myogenic factors in humans. J Physiol 2001;536:625-33.
55. Magne H, Savary-Auzeloux I, Migne C, Peyron MA, Combaret L, Remond D, Dardevet D. Unilateral hindlimb casting induced a delayed generalized muscle atrophy during rehabilitation that is prevented by a whey or a high protein diet but not a free leucine-enriched diet. PLoS ONE 2013;8:e70130.
56. Savary-Auzeloux I, Magne H, Migne C, Oberli M, Breuille D, Faure M, Vidal K, Perrot M, Remond D, Combaret L, et al. A dietary supplementation with leucine and antioxidants is capable to accelerate muscle mass recovery after immobilization in adult rats. PLoS ONE 2013;8:e81495.
57. Alway SE, Pereira SL, Edens NK, Hao Y, Bennett BT. β-Hydroxyβ-methylbutyrate (HMB) enhances the proliferation of satellite cells in fast muscles of aged rats during recovery from disuse atrophy. Exp Gerontol 2013;48:973-84.