Cited by 112Muscle metabolism and nutritionNutrition and Health in AgingMuscle Physiology and Disorders

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The anabolic response to resistance exercise and a protein-rich meal is not diminished by age

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Symonsi, T.B., Sheffield-Moore, M., Mamerow, M.M., Wolfe, R.R., Paddon-Jones, Douglas·2011·The Journal of nutrition, health and aging

DOI 10.1007/s12603-010-0319-zPMC PMC3280506

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Abstract

OBJECTIVES: The synergistic effect of resistance exercise and protein ingestion on muscle protein anabolism in young adults has been well described. However, it is unclear if this relationship is maintained in older adults who are at greater risk of sarcopenic muscle loss. To this end, we sought to determine if the synergistic response to a bout of resistance exercise and a protein-rich lean beef meal was altered by age. SETTING: The University of Texas Medical Branch, Clinical Research Center, Galveston, Texas. PARTICIPANTS: Healthy young (n=7, 29±3 y) and older (n=7, 67±2 y) adults. DESIGN: Mixed muscle fractional synthesis rate (FSR) was calculated during a 3 h post-absorptive/rest period and again during a 5 h period following ingestion of a protein-rich meal (340 g lean beef) and bout of resistance exercise (6 sets of 8 repetitions of isotonic knee extension exercise at 80% one repetition maximum). MEASUREMENTS: Venous blood samples and vastus lateralis muscle biopsy samples were obtained during a primed (2.0 µmol/kg) constant infusion (0.08 µmol∙kg(-1)min(-1)) of L- [ring-13C6] phenylalanine. RESULTS: Mixed muscle FSR increased by approximately 108% in both young [pre: 0.073±0.008; post: 0.156±0.021(SE) %/h, p<0.001] and older adults (pre: 0.075±0.004; post: 0.152±0.017 %/h, p=0.003) following the meal and resistance exercise bout. CONCLUSION: Aging does not diminish the increase in muscle protein synthesis following a high-quality protein rich meal and bout of resistance exercise.

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Cuthbertson, D., Smith, K., Babraj, J., Leese, G., Waddell, T., Atherton, P., Wackerhage, H., Taylor, P. M., & Rennie, M. J. (2005) · The FASEB Journal · doi:10.1096/fj.04-2640fje · Cited by 1,211 · cited 4×
“For example, ingestion of more than approximately 30 g of protein in a single meal does not result in continued improvement in muscle protein synthesis (13, 16).”
BackgroundInfluential
Percutaneous Needle Biopsy of Skeletal Muscle in Physiological and Clinical Research
Bergström, J. P. (1975) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.3109/00365517509095787 · Cited by 1,173
Mixed muscle protein synthesis and breakdown after resistance exercise in humans
Phillips, S. M., Tipton, K. D., Aarsland, A., Wolf, S. E., & Wolfe, R. R. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.273.1.e99 · Cited by 1,132
Self-citation
Dietary protein recommendations and the prevention of sarcopenia
Paddon-Jones, D., & Rasmussen, B. B. (2009) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32831cef8b · Cited by 823
Self-citation
Age‐related differences in the dose–response relationship of muscle protein synthesis to resistance exercise in young and old men
Kumar, V., Selby, A., Rankin, D., Patel, R., Atherton, P., Hildebrandt, W., Williams, J., Smith, K., Seynnes, O., Hiscock, N., et al. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.164483 · Cited by 740 · cited 1×
“Certainly, a blunted response to these fundamental anabolic stimuli could contribute to the characteristic slow, progressive loss of muscle mass experienced by many older individuals (13, 34).”
Background
Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans
Biolo, G., Maggi, S. P., Williams, B. D., Tipton, K. D., & Wolfe, R. R. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.268.3.e514 · Cited by 713
Self-citation
Postexercise net protein synthesis in human muscle from orally administered amino acids
Tipton, K. D., Ferrando, A. A., Phillips, S. M., Doyle, D., & Wolfe, R. R. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.276.4.e628 · Cited by 616
Self-citation
Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle
Dreyer, H. C., Fujita, S., Cadenas, J. G., Chinkes, D. L., Volpi, E., & Rasmussen, B. B. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.113175 · Cited by 570 · cited 1×
“However, approximately 60 minutes post-exercise, the capacity for muscle protein synthesis is restored and ultimately increased via the activation of protein kinase B, mTOR, S6K1 and eEF2 (29).”
Background
Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage
Wilkinson, S. B., Tarnopolsky, M. A., MacDonald, M. J., MacDonald, J. R., Armstrong, D., & Phillips, S. M. (2007) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/85.4.1031 · Cited by 530
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Tipton, K. D., Rasmussen, B. B., Miller, S. L., Wolf, S. E., Owens-Stovall, S. K., Petrini, B. E., & Wolfe, R. R. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.281.2.e197 · Cited by 526
Self-citation
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Rasmussen, B. B., Tipton, K. D., Miller, S. L., Wolf, S. E., & Wolfe, R. R. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.88.2.386 · Cited by 523
Self-citation
Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids
Katsanos, C. S., Kobayashi, H., Sheffield‐Moore, M., Aarsland, A. A., & Wolfe, R. R. (2005) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/82.5.1065 · Cited by 515
Self-citation
Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults
Kosek, D. J., Kim, J.-S., Petrella, J. K., Cross, J. M., & Bamman, M. M. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01474.2005 · Cited by 503
Isotope Tracers in Metabolic Research: Principles and Practice of Kinetic Analysis
Wolfe, R. R., & Chinkes, D. L. (2004) · Medical Entomology and Zoology · Cited by 497
Self-citation
Amino acid ingestion improves muscle protein synthesis in the young and elderly
Paddon-Jones, D., Sheffield-Moore, M., Zhang, X.-J., Volpi, E., Wolf, S. E., Aarsland, A., Ferrando, A. A., & Wolfe, R. R. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00368.2003 · Cited by 467 · cited 2×
“The synergistic anabolic response to resistance exercise and hyperaminoacidemia has been well documented in young adults (9, 12, 17, 18).”
BackgroundSelf-citation
Leucine-enriched essential amino acid and carbohydrate ingestion following resistance exercise enhances mTOR signaling and protein synthesis in human muscle
Dreyer, H. C., Drummond, M. J., Pennings, B., Fujita, S., Glynn, E. L., Chinkes, D. L., Dhanani, S., Volpi, E., & Rasmussen, B. B. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00582.2007 · Cited by 447
Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging
Drummond, M. J., Dreyer, H. C., Pennings, B., Fry, C. S., Dhanani, S., Dillon, E. L., Sheffield‐Moore, M., Volpi, E., & Rasmussen, B. B. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00021.2008 · Cited by 410
Self-citation
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Symons, T. B., Sheffield‐Moore, M., Wolfe, R. R., & Paddon‐Jones, D. (2009) · Journal of the American Dietetic Association · doi:10.1016/j.jada.2009.06.369 · Cited by 368
Self-citation
Resistance training reduces the acute exercise-induced increase in muscle protein turnover
Phillips, S. M., Tipton, K. D., Ferrando, A. A., & Wolfe, R. R. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.276.1.e118 · Cited by 336
Self-citation
Functional and Metabolic Consequences of Sarcopenia
Vandervoort, A. A., & Symons, T. B. (2001) · Canadian Journal of Applied Physiology · doi:10.1139/h01-007 · Cited by 326
Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men
Verdijk, L. B., Jonkers, R. A., Gleeson, B. G., Beelen, M., Meijer, K., Savelberg, H. H., Wodzig, W. K., Dendale, P., & van Loon, L. J. (2009) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.26626 · Cited by 253
Aging does not impair the anabolic response to a protein-rich meal
Symons, T. B., Schutzler, S. E., Cocke, T. L., Chinkes, D. L., Wolfe, R. R., & Paddon-Jones, D. (2007) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.2.451 · Cited by 240
Self-citation
Milk ingestion stimulates net muscle protein synthesis following resistance exercise
ELLIOT, T. A., CREE, M. G., SANFORD, A. P., WOLFE, R. R., & TIPTON, K. D. (2006) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000210190.64458.25 · Cited by 237
Self-citation
Differential stimulation of muscle protein synthesis in elderly humans following isocaloric ingestion of amino acids or whey protein
Paddon-Jones, D., Sheffield-Moore, M., Katsanos, C. S., Zhang, X.-J., & Wolfe, R. R. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2005.10.006 · Cited by 223 · cited 1×
“Free-form amino acids and whey protein appear in the circulation within 15–30 minutes of ingestion (8, 9).”
BackgroundSelf-citation
Functional and Metabolic Consequences of Sarcopenia
Evans, W. J. (1997) · Journal of Nutrition · doi:10.1093/jn/127.5.998s · Cited by 218
Resistance training alters the response of fed state mixed muscle protein synthesis in young men
Tang, J. E., Perco, J. G., Moore, D. R., Wilkinson, S. B., & Phillips, S. M. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00636.2007 · Cited by 181
Effects of high-intensity resistance training on untrained older men. II. Muscle fiber characteristics and nucleo-cytoplasmic relationships
Hikida, R. S., Staron, R. S., Hagerman, F. C., Walsh, S., Kaiser, E., Shell, S., & Hervey, S. (2000) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/55.7.b347 · Cited by 167
The determination of low d 5 ‐phenylalanine enrichment (0.002–0.09 atom percent excess), after conversion to phenylethylamine, in relation to protein turnover studies by gass chromatography/electron ionization mass spectrometry
Calder, A. G., Anderson, S. E., Grant, I., McNurlan, M. A., & Garlick, P. J. (1992) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.1290060704 · Cited by 164
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Tang, J. E., Manolakos, J. J., Kujbida, G. W., Lysecki, P. J., Moore, D. R., & Phillips, S. M. (2007) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h07-076 · Cited by 130
Sarcopenia--exercise as a treatment strategy.
Taaffe, D. R. (2006) · PubMed · Cited by 129
Essential amino acid and carbohydrate ingestion before resistance exercise does not enhance postexercise muscle protein synthesis
Fujita, S., Dreyer, H. C., Drummond, M. J., Glynn, E. L., Volpi, E., & Rasmussen, B. B. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.90395.2008 · Cited by 129
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Phillips, S. M. (2009) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h09-042 · Cited by 122
Measurement of very low stable isotope enrichments by gas chromatography/mass spectrometry: Application to measurement of muscle protein synthesis
Patterson, B. W., Zhang, X.-J., Chen, Y., Klein, S., & Wolfe, R. R. (1997) · Metabolism · doi:10.1016/s0026-0495(97)90084-6 · Cited by 118
Self-citation
Higher muscle protein synthesis in women than men across the lifespan, and failure of androgen administration to amend age‐related decrements
Henderson, G. C., Dhatariya, K., Ford, G. C., Klaus, K. A., Basu, R., Rizza, R. A., Jensen, M. D., Khosla, S., O’Brien, P. C., & Nair, K. S. (2008) · The FASEB Journal · doi:10.1096/fj.08-117200 · Cited by 114
Latency, Duration and Dose Response Relationships of Amino Acid Effects on Human Muscle Protein Synthesis
Rennie, M. J., Bohé, J., & Wolfe, R. R. (2002) · The Journal of Nutrition · doi:10.1093/jn/131.10.3225s · Cited by 74
Self-citation
Synergistic Use of Higher-Protein Diets or Nutritional Supplements with Resistance Training to Counter Sarcopenia
Campbell, W. W. (2007) · Nutrition Reviews · doi:10.1111/j.1753-4887.2007.tb00320.x · Cited by 70

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Authors: Symonsi, T. B., Sheffield-Moore, M., Mamerow, M. M., Wolfe, R. R., & Paddon-Jones, D.
Affiliations: The University of Texas Medical Branch at Galveston (US)
ORCID: Wolfe, R.R.
Venue: The Journal of nutrition, health and aging
Publisher: Elsevier BV
Published: 2011-05
Volume: 15
Issue: 5
Pages: 376-381
ISSN: 1279-7707 (ISSN-L)
DOI: 10.1007/s12603-010-0319-z
PMC: PMC3280506
OpenAlex: W2085792315
Cited by: 112
References: 36
Citations by year: 2026: 4 · 2025: 3 · 2024: 4 · 2023: 3 · 2022: 2 · 2021: 6 · 2020: 10 · 2019: 9 · 2018: 9 · 2017: 9 · 2016: 9 · 2015: 12 · 2014: 8 · 2013: 7 · 2012: 12
FWCI: 3.22
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor, 4619 d)
Locations: The journal of nutrition health & aging (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (UL1TR000071)
National Institute on Aging (P30 AG17231, P60AG017231, P30AG024832)
National Center for Research Resources (M01 RR-00073, UL1RR029876, M01RR000073)
National Center for Advancing Translational Sciences
Topics: Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
Health Sciences › Medicine › Physiology (medical) › Nutrition and Health in Aging
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Keywords: muscle protein synthesis, resistance training, protein intake, aging, older adults, sarcopenia, knee extension exercise, phenylalanine tracer, vastus lateralis
MeSH terms: Adult, Aged, Aging, Biopsy, Dietary Proteins, Female, Humans, Male, Meat, Muscle Proteins, Phenylalanine, Exercise, Quadriceps Muscle, Resistance Training

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The anabolic response to resistance exercise and a protein-rich meal is not diminished by age

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