Short-term muscle disuse lowers myofibrillar protein synthesis rates and induces anabolic resistance to protein ingestion

American Journal of Physiology - Endocrinology and Metabolism

Volumn 310, Issue 2, 2016, Pages E137-E147

  Wall, Benjamin T ^a,b   Dirks, Marlou L ^b   Snijders, Tim ^b   van Dijk, Jan Willem ^a,b   Fritsch, Mario ^c   Verdijk, Lex B ^a,b   van Loon, Luc J C ^a,b  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Amino acids; Immobilization; Muscle atrophy

Indexed keywords

PROTEIN INTAKE;

HUMAN; IMMOBILIZATION; MALE; METABOLISM; MUSCLE ATROPHY; MUSCLE STRENGTH; PHYSIOLOGY; POSTPRANDIAL STATE; PROTEIN INTAKE; PROTEIN SYNTHESIS; QUADRICEPS FEMORIS MUSCLE; YOUNG ADULT;

DIETARY PROTEINS; HUMANS; IMMOBILIZATION; MALE; MUSCLE STRENGTH; MUSCULAR ATROPHY; POSTPRANDIAL PERIOD; PROTEIN BIOSYNTHESIS; QUADRICEPS MUSCLE; YOUNG ADULT;

EID: 84955107680     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00227.2015     Document Type: Article

References (75)

1. Abumrad NN, Rabin D, Diamond MP, Lacy WW. Use of a heated superficial hand vein as an alternative site for the measurement of amino acid concentrations and for the study of glucose and alanine kinetics in man. Metabolism 30: 936-940, 1981.
2. Baehr L, Furlow J, Bodine S. Muscle sparing in muscle RING finger 1 null mice: response to synthetic glucocorticoids. J Physiol 589: 4759-4776, 2011.
3. Bergström J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35: 609-616, 1975.
4. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valen-zuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001.
5. Boirie Y, Dangin M, Gachon P, Vasson M, Maubois J, Beaufrère B. Slow and fast dietary proteins differently modulate postprandial protein accretion. Proc Natl Acad Sci USA 94: 14930-14935, 1997.
6. Booth F, Zwetsloot K. Basic concepts about genes, inactivity and aging. Scand J Med Sci Sports 20: 1-4, 2010.
7. Burd NA, Cermak NM, Kouw IW, Gorissen SH, Gijsen AP, van Loon LJ. The use of doubly labeled milk protein to measure postprandial muscle protein synthesis rates in vivo in humans. J Appl Physiol 117: 1363-1370, 2014.
8. Burd NA, West DW, Rerecich T, Prior T, Baker SK, Phillips SM. Validation of a single biopsy approach and bolus protein feeding to determine myofibrillar protein synthesis in stable isotope tracer studies in humans. Nutr Metab (Lond) 8: 15, 2011.
9. Burd NA, Hamer HM, Pennings B, Pellikaan WF, Senden JM, Gijsen AP, van Loon LJ. Substantial Differences between Organ and Muscle Specific Tracer Incorporation Rates in a Lactating Dairy Cow. PLoS One 8: e68109, 2013.
10. Burd NA, Pennings B, Groen BB, Gijsen AP, Senden JM, van Loon LJ. The single biopsy approach is reliable for the measurement of muscle protein synthesis rates in vivo in older men. J Appl Physiol 113: 896-902, 2012
11. Calder AG, Anderson SE, Grant I, McNurlan MA, Garlick PJ. The determination of low d5-phenylalanine enrichment (0.002- 0.09 atom percent excess), after conversion to phenylethylamine, in relation to protein turnover studies by gas chromatography/electron ionization mass spectrometry. Rapid Commun Mass Spectrom 6: 421-424, 1992.
12. Chen Y, Gregory C, Scarborough M, Shi R, Walter G, Vandenborne K. Transcriptional pathways associated with skeletal muscle disuse atrophy in humans. Physiol Genomics 31: 510-520, 2007.
13. Churchward-Venne T, Burd N, Mitchell C, West D, Philp A, Marcotte G, Baker S, Baar K, Phillips S. Supplementation of a suboptimal protein dose with leucine or essential amino acids: effects on myofibrillar protein synthesis at rest and following resistance exercise in men. J Physiol 590: 2751-2765, 2012.
14. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor P, Rennie M. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 19: 422-424, 2005.
15. Deitrick J. The effect of immobilization on metabolic and physiological functions of normal men. Bull NY Acad Med 24: 364-375, 1948.
16. Dickinson J, Rasmussen B. Amino acid transporters in the regulation of human skeletal muscle protein metabolism. Curr Opin Clin Nutr Metab Care 16: 638-644, 2013.
17. Dirks M, Wall B, Nilwik R, Weerts D, Verdijk L, van Loon L. Skeletal muscle disuse atrophy is not attenuated by dietary protein supplementation in healthy, older men. J Nutr 144: 1196-1203, 2014.
18. 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) 210: 628-641, 2013.
19. Drummond MJ, Dickinson JM, Fry CS, Walker DK, Gundermann DM, Reidy PT, Timmerman KL, Markofski MM, Paddon-Jones D, Rasmussen BB, Volpi E. Bed rest impairs skeletal muscle amino acid transporter expression, mTORC1 signaling, and protein synthesis in response to essential amino acids in older adults. Am J Physiol Endocrinol Metab 302: E1113-E1122, 2012.
20. Drummond M, Fry C, Glynn E, Dreyer H, Dhanani S, Timmerman K, Volpi E, Rasmussen B. Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis. J Physiol 587: 1535-1546, 2009.
21. Drummond M, Fry C, Glynn E, Timmerman K, Dickinson J, Walker D, Gundermann D, Volpi E, Rasmussen B. Skeletal muscle amino acid transporter expression is increased in young and older adults following resistance exercise. J Appl Physiol 111: 135-142, 2011.
22. Drummond MJ, Glynn EL, Fry CS, Timmerman KL, Volpi E, Rasmussen BB. An increase in essential amino acid availability upregulates amino acid transporter expression in human skeletal muscle. Am J Physiol Endocrinol Metab 298: E1011-E1018, 2010.
23. Drummond MJ, Timmerman KL, Markofski MM, Walker DK, Dickinson JM, Jamaluddin M, Brasier AR, Rasmussen BB, Volpi E. Short-term bed rest increases TLR4 and IL-6 expression in skeletal muscle of older adults. Am J Physiol Regul Integr Comp Physiol 305: R216-R223, 2013.
24. English KL, Paddon-Jones D. Protecting muscle mass and function in older adults during bed rest. Curr Opin Clin Nutr Metab Care 13: 34-39, 2010.
25. Farnfield M, Breen L, Carey K, Garnham A, Cameron-Smith D. Activation of mTOR signalling in young and old human skeletal muscle in response to combined resistance exercise and whey protein ingestion. Appl Physiol Nutr Metab 37: 21-30, 2012.
26. Febbraio M, Hiscock N, Sacchetti M, Fischer C, Pedersen B. Interleukin-6 is a novel factor mediating glucose homeostasis during skeletal muscle contraction. Diabetes 53: 1643-1648, 2004.
27. 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 Endocrinol Metab 270: E627-E633, 1996.
28. Fisher S, Kuo Y, Graham J, Ottenbacher K, Ostir G. Early ambulation and length of stay in older adults hospitalized for acute illness. Arch Intern Med 170: 1942-1943, 2010.
29. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509, 1957.
30. Frayn K, Maycock P. Skeletal muscle triacylglycerol in the rat: methods for sampling and measurement, and studies of biological variability. J Lipid Res 21: 139-144, 1980.
31. Fry C, Drummond M, Glynn E, Dickinson J, Gundermann D, Timmerman K, Walker D, Dhanani S, Volpi E, Rasmussen B. Aging impairs contraction-induced human skeletal muscle mTORC1 signaling and protein synthesis. Skelet Muscle 1: 11, 2011.
32. Gibson J, Halliday D, Morrison W, Stoward P, Hornsby G, Watt P, Murdoch G, Rennie M. Decrease in human quadriceps muscle protein turnover consequent upon leg immobilization. Clin Sci (Lond) 72: 503-509, 1987.
33. Glover E, Phillips S, Oates B, Tang J, Tarnopolsky M, Selby A, Smith K, Rennie M. Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol 586: 6049-6061, 2008.
34. Glover E, Yasuda N, Tarnopolsky M, Abadi A, Phillips S. Little change in markers of protein breakdown and oxidative stress in humans in immobilization-induced skeletal muscle atrophy. Appl Physiol Nutr Metab 35: 125-133, 2010
35. Goldspink D. The effects of denervation on protein turnover of rat skeletal muscle. Biochem J 156: 71-80, 1976.
36. Goldspink D. The influence of immobilization and stretch on protein turnover of rat skeletal muscle. J Physiol 264: 267-282, 1977.
37. Gomes M, Lecker S, Jagoe R, Navon A, Goldberg A. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 98: 14440-14445, 2001.
38. Goodpaster BH, Kelley DE, Thaete FL, He J, Ross R. Skeletal muscle attenuation determined by computed tomography is associated with skel etal muscle lipid content. J Appl Physiol 89: 104-110, 2000.
39. Greenhaff PL, Karagounis LG, Peirce N, Simpson EJ, Hazell M, Layfield R, Wackerhage H, Smith K, Atherton P, Selby A, Rennie MJ. 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: E595-E604, 2008.
40. 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 302: E52-E60, 2012.
41. Haruna Y, Suzuki Y, Kawakubo K, Yanagibori R, Gunji A. Decre- mental reset in basal metabolism during 20-days bed rest. Acta Physiol Scand Suppl 616: 43-49, 1994.
42. Jones S, Hill R, Krasney P, O’Conner B, Peirce N, Greenhaff P. Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass. FASEB J 18: 1025-1027, 2004.
43. Kimball SR, Farrell PA, Jefferson LS. Invited Review: Role of insulin in translational control of protein synthesis in skeletal muscle by amino acids or exercise. J Appl Physiol 93: 1168-1180, 2002.
44. Koopman R, Crombach N, Gijsen AP, Walrand S, Fauquant J, Kies AK, Lemosquet S, Saris WH, Boirie Y, van Loon LJ. Ingestion of a protein hydrolysate is accompanied by an accelerated in vivo digestion and absorption rate when compared with its intact protein. Am J Clin Nutr 90: 106-115, 2009.
45. Koopman R, Verdijk L, Manders RJ, Gijsen AP, Gorselink M, Pijpers E, Wagenmakers AJ, van Loon LJ. Co-ingestion of protein and leucine stimulates muscle protein synthesis rates to the same extent in young and elderly lean men. Am J Clin Nutr 84: 623-632, 2006.
46. Koopman R, Zorenc AH, Gransier RJ, Cameron-Smith D, van Loon LJ. Increase in S6K1 phosphorylation in human skeletal muscle following resistance exercise occurs mainly in type II muscle fibers. Am J Physiol Endocrinol Metab 290: E1245-E1252, 2006.
47. Li H, Malhotra S, Kumar A. Nuclear factor-kappa B signaling in skeletal muscle atrophy. J Mol Med (Berl) 86: 1113-1126, 2008.
48. Loughna P, Goldspink G, Goldspink DF. Effect of inactivity and passive stretch on protein turnover in phasic and postural rat muscles. J Appl Physiol 61: 173-179, 1986.
49. Marimuthu K, Murton A, Greenhaff P. Mechanisms regulating muscle mass during disuse atrophy and rehabilitation in humans. J Appl Physiol 110: 555-560, 2011.
50. Markofski M, Dickinson J, Drummond M, Fry C, Fujita S, Gunder-mann D, Glynn E, Jennings K, Paddon-Jones D, Reidy P, Sheffield-Moore M, Timmerman K, Rasmussen B, Volpi E. Effect of age on basal muscle protein synthesis and mTORC1 signaling in a large cohort of young and older men and women. Exp Gerontol 65: 1-7, 2015.
51. Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson SB, Prior T, Tarnopolsky MA, Phillips SM. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am J Clin Nutr 89: 161-168, 2009.
52. Pennings B, Boirie Y, Senden JM, Gijsen AP, Kuipers H, van Loon LJ. Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. Am J Clin Nutr 93: 997-1005, 2011.
53. 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 302: E992-E999, 2012.
54. Pennings B, Pellikaan WF, Senden JM, van Vuuren AM, Sikkema J, van Loon LJ. The production of intrinsically labeled milk and meat protein is feasible and provides functional tools for human nutrition research. J Dairy Sci 94: 4366-4373, 2011.
55. Rasmussen B, Fujita S, Wolfe R, Mittendorfer B, Roy M, Rowe V, Volpi E. Insulin resistance of muscle protein metabolism in aging. FASEB J 20: 768-769, 2006.
56. Rennie M, Edwards R, Halliday D, Matthews D, Wolman S, Millward D. Muscle protein synthesis measured by stable isotope techniques in man: the effects of feeding and fasting. Clin Sci (Lond) 63: 519-523, 1982.
57. Schwenk WF, Berg PJ, Beaufrere B, Miles JM, Haymond MW. Use of t-butyldimethylsilylation in the gas chromatographic/mass spectrometric analysis of physiologic compounds found in plasma using electron-impact ionization. Anal Biochem 141: 101-109, 1984.
58. Stefanyk L, Dyck D. The interaction between adipokines, diet and exercise on muscle insulin sensitivity. Curr Opin Clin Nutr Metab Care 13: 255-259, 2010.
59. Stephens FB, Chee C, Wall BT, Murton AJ, Shannon CE, van Loon LJ, Tsintzas K. Lipid-induced insulin resistance is associated with an impaired skeletal muscle protein synthetic response to amino acid inges- tion in healthy young men. Diabetes 64: 1615-1620, 2015.
60. Strandberg S, Wretling ML, Wredmark T, Shalabi A. Reliability of computed tomography measurements in assessment of thigh muscle cross- sectional area and attenuation. BMC Med Imaging 10: 18, 2010.
61. Stuart C, Shangraw R, Prince M, Peters E, Wolfe R. Bed-rest-induced insulin resistance occurs primarily in muscle. Metabolism 37: 802-806, 1988.
62. Timmerman K, Lee J, Dreyer H, Dhanani S, Glynn E, Fry C, Drummond M, Sheffield-Moore M, Rasmussen B, Volpi E. Insulin stimulates human skeletal muscle protein synthesis via an indirect mech- anism involving endothelial-dependent vasodilation and mammalian tar- get of rapamycin complex 1 signaling. J Clin Endocrinol Metab 95: 3848-3857, 2010.
63. Urso ML, Scrimgeour AG, Chen YW, Thompson PD, Clarkson PM. Analysis of human skeletal muscle after 48 h immobilization reveals alterations in mRNA and protein for extracellular matrix components. J Appl Physiol 101: 1136-1148, 2006.
64. van Loon LJ, Boirie Y, Gijsen AP, Fauquant J, de Roos AL, Kies AK, Lemosquet S, Saris WH, Koopman R. The production of intrinsically labeled milk protein provides a functional tool for human nutrition research. J Dairy Sci 92: 4812-4822, 2009.
65. 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) 210: 600-611, 2014.
66. Wall BT, Dirks ML, Snijders T, Stephens FB, Senden JM, Verschei-jden ML, van Loon LJ. Short-term muscle disuse atrophy is not associated with increased intramuscular lipid deposition or a decline in the maximal activity of key mitochondrial enzymes in young and older males. Exp Gerontol 61: 76-83, 2015.
67. Wall BT, Dirks ML, van Loon LJ. Skeletal muscle atrophy during short-term disuse: implications for age-related sarcopenia. Ageing Res Rev 12: 898-906, 2013.
68. Wall BT, Dirks ML, Verdijk LB, Snijders T, Hansen D, Vranckx P, Burd NA, Dendale P, van Loon LJ. Neuromuscular electrical stimulation increases muscle protein synthesis in elderly type 2 diabetic men. Am J Physiol Endocrinol Metab 303: E614-E623, 2012.
69. Wall BT, Hamer HM, de Lange A, Kiskini A, Groen BB, Senden JM, Gijsen AP, Verdijk LB, van Loon LJ. Leucine co-ingestion improves post-prandial muscle protein accretion in elderly men. Clin Nutr 32: 412-419, 2013.
70. Wall BT, Morton JP, van Loon LJ. Strategies to maintain skeletal muscle mass in the injured athlete: nutritional considerations and exercise mimetics. Eur J Sport Sci 15: 53-62, 2014.
71. 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 98: 4872-4878, 2013.
72. Wall BT, van Loon LJ. Nutritional strategies to attenuate muscle disuse atrophy. Nutr Rev 71: 195-208, 2012.
73. West D, Burd N, Coffey V, Baker S, Burke L, Hawley J, Moore D, Stellingwerff T, Phillips S. Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise. Am J Clin Nutr 94: 795-803, 2011.
74. Witard OC, Jackman SR, Breen L, Smith K, Selby A, Tipton KD. 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: 86-95, 2014.
75. Yang Y, Breen L, Burd NA, Hector AJ, Churchward-Venne TA, Josse AR, Tarnopolsky MA, Phillips SM. Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men. Br J Nutr 7: 1-9, 2012.