The DOI matches its Crossref record; 59 of the 60 references it cites were found in a registry or an index.
Whey and casein labeled with l-[1-13C]leucine and muscle protein synthesis: effect of resistance exercise and protein ingestion
Abstract
Muscle protein turnover following resistance exercise and amino acid availability are relatively well described. By contrast, the beneficial effects of different sources of intact proteins in relation to exercise need further investigation. Our objective was to compare muscle anabolic responses to a single bolus intake of whey or casein after performance of heavy resistance exercise. Young male individuals were randomly assigned to participate in two protein trials ( n = 9) or one control trial ( n = 8). Infusion of l-[1-13 C]leucine was carried out, and either whey, casein (0.3 g/kg lean body mass), or a noncaloric control drink was ingested immediately after exercise. l-[1-13 C]leucine-labeled whey and casein were used while muscle protein synthesis (MPS) was assessed. Blood and muscle tissue samples were collected to measure systemic hormone and amino acid concentrations, tracer enrichments, and myofibrillar protein synthesis. Western blots were used to investigate the Akt signaling pathway. Plasma insulin and branched-chain amino acid concentrations increased to a greater extent after ingestion of whey compared with casein. Myofibrillar protein synthesis was equally increased 1–6 h postexercise after whey and casein intake, both of which were higher compared with control ( P < 0.05). Phosphorylation of Akt and p70 S6K was increased after exercise and protein intake ( P < 0.05), but no differences were observed between the types of protein except for total 4E-BP1, which was higher after whey intake than after casein intake ( P < 0.05). In conclusion, whey and casein intake immediately after resistance exercise results in an overall equal MPS response despite temporal differences in insulin and amino acid concentrations and 4E-BP1.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“When taken in immediately after resistance exercise, whey and casein resulted in equally increased protein synthesis despite temporal differences in postprandial insulin and amino acid concentrations.197”
From Evidence-Based Recommendations for Optimal Dietary Protein Intake in Older People: A Position Paper From the PROT-AGE Study Group (2013) · cites this paper as [197]
Citations
Cites
Bodine, S. C., Stitt, T. N., Gonzalez, M., Kline, W. O., Stover, G. L., Bauerlein, R., Zlotchenko, E., Scrimgeour, A., Lawrence, J. C., Glass, D. J., et al. (2001) · Nature Cell Biology · doi:10.1038/ncb1101-1014 · Cited by 2,752
The underappreciated role of muscle in health and disease
Wolfe, R. R. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/84.3.475 · Cited by 1,641
Heinrikson, R. L., & Meredith, S. C. (1984) · Analytical Biochemistry · doi:10.1016/0003-2697(84)90307-5 · Cited by 1,631
Slow and fast dietary proteins differently modulate postprandial protein accretion
Boirie, Y., Dangin, M., Gachon, P., Vasson, M.-P., Maubois, J.-L., & Beaufrère, B. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.26.14930 · Cited by 1,453
Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle
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 1×
“Furthermore, it has been shown that 20 g of protein seems to be sufficient for maximal stimulation of MPS (15, 44).”
BackgroundMixed 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
Tang, J. E., Moore, D. R., Kujbida, G. W., Tarnopolsky, M. A., & Phillips, S. M. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00076.2009 · Cited by 998
Moore, D. R., Robinson, M. J., Fry, J. L., Tang, J. E., Glover, E. I., Wilkinson, S. B., Prior, T., Tarnopolsky, M. A., & Phillips, S. M. (2009) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.26401 · Cited by 973
Katsanos, C. S., Kobayashi, H., Sheffield-Moore, M., Aarsland, A., & Wolfe, R. R. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00488.2005 · Cited by 923
An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein
Biolo, G., Tipton, K. D., Klein, S., & Wolfe, R. R. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.273.1.e122 · Cited by 825
Aagaard, P., Andersen, J. L., Dyhre‐Poulsen, P., Leffers, A., Wagner, A., Magnusson, S. P., Halkjær‐Kristensen, J., & Simonsen, E. B. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.t01-1-00613.x · Cited by 733 · cited 1×
“Resistance exercise, either alone (5, 13, 47) or in combination with AAs or whole proteins (6, 11, 44), is able to increase muscle protein synthesis (MPS), and as a consequence of repeated training sessions muscle mass and strength will increase (1, 29, 30).”
BackgroundBaar, K., & Esser, K. (1999) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1999.276.1.c120 · Cited by 726
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 · cited 1×
“Resistance exercise, either alone (5, 13, 47) or in combination with AAs or whole proteins (6, 11, 44), is able to increase muscle protein synthesis (MPS), and as a consequence of repeated training sessions muscle mass and strength will increase (1, 29, 30).”
BackgroundKimball, S. R., & Jefferson, L. S. (2006) · Journal of Nutrition · doi:10.1093/jn/136.1.227s · Cited by 637
The digestion rate of protein is an independent regulating factor of postprandial protein retention
Dangin, M., Boirie, Y., Garcia-Rodenas, C., Gachon, P., Fauquant, J., Callier, P., Ballèvre, O., & Beaufrère, B. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.280.2.e340 · Cited by 572
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
Suction applied to a muscle biopsy maximizes sample size
Evans, W. J., Phinney, S. D., & Young, V. R. (1982) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198201000-00018 · Cited by 525
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
Hartman, J. W., Tang, J. E., Wilkinson, S. B., Tarnopolsky, M. A., Lawrence, R. L., Fullerton, A. V., & Phillips, S. M. (2007) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.2.373 · Cited by 498
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
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
Drummond, M. J., Fry, C. S., Glynn, E. L., Dreyer, H. C., Dhanani, S., Timmerman, K. L., Volpi, E., & Rasmussen, B. B. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.163816 · Cited by 439
Changes in human muscle protein synthesis after resistance exercise
Chesley, A., MacDougall, J. D., Tarnopolsky, M. A., Atkinson, S. A., & Smith, K. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.73.4.1383 · Cited by 436
Essential amino acids and muscle protein recovery from resistance exercise
Børsheim, E., Tipton, K. D., Wolf, S. E., & Wolfe, R. R. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00466.2001 · Cited by 422
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
Rieu, I., Balage, M., Sornet, C., Giraudet, C., Pujos, E., Grizard, J., Mosoni, L., & Dardevet, D. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.110742 · Cited by 410
Matthews, D. E., Schwarz, H. P., Yang, R. D., Motil, K. J., Young, V. R., & Bier, D. M. (1982) · Metabolism · doi:10.1016/0026-0495(82)90160-3 · Cited by 402
Koopman, R., Crombach, N., Gijsen, A. P., Walrand, S., Fauquant, J., Kies, A. K., Lemosquet, S., Saris, W. H. M., Boirie, Y., & van Loon, L. J. C. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.27474 · Cited by 383
The Ether Soluble Porphyrins Found in the Urine of Normal Man and Rabbit
Eriksen, L., Eriksen, N., & Haavaldsen, S. (1962) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.1080/00365516209075148 · Cited by 358
Ingestion of Casein and Whey Proteins Result in Muscle Anabolism after Resistance Exercise
Tipton, K. D., Elliott, T. A., Cree‐Green, M., Wolf, S. E., Sanford, A. P., & Wolfe, R. R. (2004) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000147582.99810.c5 · Cited by 353
Nutrient signalling in the regulation of human muscle protein synthesis
Fujita, S., Dreyer, H. C., Drummond, M. J., Glynn, E. L., Cadenas, J. G., Yoshizawa, F., Volpi, E., & Rasmussen, B. B. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.134593 · Cited by 339
Distinct anabolic signalling responses to amino acids in C2C12 skeletal muscle cells
Atherton, P. J., Smith, K., Etheridge, T., Rankin, D., & Rennie, M. J. (2010) · Amino Acids · doi:10.1007/s00726-009-0377-x · Cited by 323
Koopman, R., Wagenmakers, A. J. M., MANDERS, R. J. F., Zorenc, A. H. G., Senden, J. M., Gorselink, M., KEIZER, H. A., & van Loon, L. J. C. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00413.2004 · Cited by 319
Amino acid transceptors: gate keepers of nutrient exchange and regulators of nutrient signaling.
Hundal, H., & Taylor, P. M. (2009) · American Journal of Physiology. Endocrinology and Metabolism · doi:10.1152/ajpendo.91002.2008 · Cited by 305
West, D. W. D., Kujbida, G. W., Moore, D. R., Atherton, P., Burd, N. A., Padzik, J. P., De Lisio, M., Tang, J. E., Parise, G., Rennie, M. J., et al. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.177220 · Cited by 289
Calbet, J. A. L., & Holst, J. J. (2004) · European Journal of Nutrition · doi:10.1007/s00394-004-0448-4 · Cited by 288
Karlsson, H. K. R., Nilsson, P.-A., Nilsson, J., Chibalin, A. V., Zierath, J. R., & Blomstrand, E. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00430.2003 · Cited by 282
Drummond, M., Glynn, E., Fry, C., Timmerman, K., Volpi, E., & Rasmussen, B. (2010) · American Journal of Physiology. Endocrinology and Metabolism · doi:10.1152/ajpendo.00690.2009 · Cited by 231
Holm, L., Reitelseder, S., Pedersen, T. G., Doessing, S., Petersen, S. G., Flyvbjerg, A., Andersen, J. L., Aagaard, P., & Kjaer, M. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.90538.2008 · Cited by 218
Self-citationDoessing, S., Heinemeier, K. M., Holm, L., Mackey, A. L., Schjerling, P., Rennie, M. J., Smith, K., Reitelseder, S., Kappelgaard, A., Rasmussen, M. H., et al. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.179325 · Cited by 207
Self-citationLacroix, M., Bos, C., Léonil, J., Airinei, G., Luengo, C., Daré, S., Benamouzig, R., Fouillet, H., Fauquant, J., Tomé, D., et al. (2006) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/84.5.1070 · Cited by 194
Boirie, Y., Gachon, P., Corny, S., Fauquant, J., Maubois, J. L., & Beaufrere, B. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.271.6.e1083 · Cited by 174
Exercise and the Growth Hormone-Insulin-Like Growth Factor Axis
Frystyk, J. (2009) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181b07d2d · Cited by 171
Self-citationMolecular and Cellular Determinants of Skeletal Muscle Atrophy and Hypertrophy
Sartorelli, V., & Fulco, M. (2004) · Science s STKE · doi:10.1126/stke.2442004re11 · Cited by 155
Nygren, J., & Nair, K. S. (2003) · Diabetes · doi:10.2337/diabetes.52.6.1377 · Cited by 147
Holm, L., van Hall, G., Rose, A. J., Miller, B. F., Doessing, S., Richter, E. A., & Kjaer, M. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00609.2009 · Cited by 132
Self-citationChow, L. S., Albright, R. C., Bigelow, M. L., Toffolo, G., Cobelli, C., & Nair, K. S. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00003.2006 · Cited by 127
Potential Ergogenic Effects of Arginine and Creatine Supplementation
Paddon-Jones, D., Børsheim, E., & Wolfe, R. R. (2004) · The Journal of Nutrition · doi:10.1093/jn/134.10.2888s · Cited by 119
Observations of Branched-Chain Amino Acid Administration in Humans
Matthews, D. E. (2005) · Journal of Nutrition · doi:10.1093/jn/135.6.1580s · Cited by 107
Koopman, R., Verdijk, L. B., Beelen, M., Gorselink, M., Kruseman, A. N., Wagenmakers, A. J. M., Kuipers, H., & van Loon, L. J. C. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114507812013 · Cited by 104
Functional heterogeneity of leucine pools in human skeletal muscle.
Ljungqvist, O. H., Persson, M., Ford, G. C., & Nair, K. S. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.273.3.e564 · Cited by 95
van Loon, L. J. C., Boirie, Y., Gijsen, A. P., Fauquant, J., de Roos, A. L., Kies, A. K., Lemosquet, S., Saris, W. H. M., & Koopman, R. (2009) · Journal of Dairy Science · doi:10.3168/jds.2009-2317 · Cited by 89
Glover, E. I., Oates, B. R., Tang, J. E., Moore, D. R., Tarnopolsky, M. A., & Phillips, S. M. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00097.2008 · Cited by 87
Resistance Exercise Increases Postprandial Muscle Protein Synthesis in Humans
Witard, O. C., Tieland, M., Beelen, M., Tipton, K. D., van Loon, L. J. C., & Koopman, R. (2008) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181844e79 · Cited by 84
Production of Large Amounts of [13C]Leucine-Enriched Milk Proteins by Lactating Cows
Boirie, Y., Fauquant, J., Rulquin, H., Maubois, J., & Beaufrère, B. (1995) · Journal of Nutrition · doi:10.1093/jn/125.1.92 · Cited by 68
Holm, L., Esmarck, B., Mizuno, M., Hansen, H., Suetta, C., Hölmich, P., Krogsgaard, M. R., & Kjær, M. (2006) · Journal of Orthopaedic Research® · doi:10.1002/jor.20147 · Cited by 50
Self-citationAmino acid sensing and mTOR regulation: inside or out?
Goberdhan, D. C. I., Ogmundsdottir, M. H., Kazi, S., Reynolds, B., Visvalingam, S. M., WILSON, C. G., & Boyd, C. A. R. (2009) · Biochemical Society Transactions · doi:10.1042/bst0370248 · Cited by 47
Zhang, X., Chinkes, D. L., & Wolfe, R. R. (2008) · Clinical Nutrition · doi:10.1016/j.clnu.2008.01.006 · Cited by 34
TOFFOLO, G. M., Albright, R. C., Joyner, M. J., Dietz, N. M., Cobelli, C., & Nair, K. S. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00106.2003 · Cited by 18
Research works printed but not linked: 3
- Bergström J, 1962, Scand J Clin Lab Invest, 14, 1, 10.3109/00365516209075148 · DOI
- Evans WJ, 1982, Med Sci Sports Exerc, 14, 101
- World Health Organization, 2007, Protein and Amino Acid Requirements in Human Nutrition: Report of a Joint WHO/FAO/UNU Expert Consultation
Cited by
Sorted by citations
Bauer, J., Biolo, G., Cederholm, T., Cesari, M., Cruz-Jentoft, A. J., Morley, J. E., Phillips, S., Sieber, C., Stehle, P., Teta, D., et al. (2013) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2013.05.021 · Cited by 2,553
Deutz, N. E. P., Bauer, J. M., Barazzoni, R., Biolo, G., Boirie, Y., Bosy-Westphal, A., Cederholm, T., Cruz-Jentoft, A., Krznariç, Z., Nair, K. S., et al. (2014) · Clinical Nutrition · doi:10.1016/j.clnu.2014.04.007 · Cited by 1,738
Protein "requirements" beyond the RDA: implications for optimizing health
Phillips, S. M., Chevalier, S., & Leidy, H. J. (2016) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2015-0550 · Cited by 396
Loh, R., Stamatakis, E., Folkerts, D., Allgrove, J. E., & Moir, H. J. (2020) · Sports Medicine · doi:10.1007/s40279-019-01183-w · Cited by 326
Yang, Y., Churchward-Venne, T. A., Burd, N. A., Breen, L., Tarnopolsky, M. A., & Phillips, S. M. (2012) · Nutrition & Metabolism · doi:10.1186/1743-7075-9-57 · Cited by 286
Metadata
- Authors
- Reitelseder, S., Agergaard, J., Doessing, S., Helmark, I. C., Lund, P., Kristensen, N. B., Frystyk, J., Flyvbjerg, A., Schjerling, P., van Hall, G., Kjaer, M., & Holm, L.
- Affiliations
- University of Copenhagen (DK)
- Aarhus University (DK)
- Aarhus University Hospital (DK)
- Institute of Sports Medicine Copenhagen, Department of Orthopedic Surgery M, Bispebjerg Hospital and Center for Healthy Aging, Faculty of Health Sciences, University of Copenhagen, Copenhagen;
- Corresponding author
- Reitelseder, Søren
- ORCID
- Venue
- American Journal of Physiology-Endocrinology and Metabolism
- Publisher
- American Physiological Society
- Published
- 2011-01
- Volume
- 300
- Issue
- 1
- Pages
- E231-E242
- ISSN
- 0193-1849 (ISSN-L)
- 1522-1555
- OpenAlex
- W2113426840
- Cited by
- 190
- References
- 60
- Citations by year
- 2025: 5 · 2024: 3 · 2023: 7 · 2022: 10 · 2021: 9 · 2020: 14 · 2019: 19 · 2018: 16 · 2017: 13 · 2016: 24 · 2015: 17 · 2014: 13 · 2013: 17 · 2012: 15
- FWCI
- 5.60
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Endocrinology and Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
- Funders
- Heising-Simons Foundation
- Hidradenitis Suppurativa Foundation
- Mejeribrugets ForskningsFond
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology (medical) › Cardiovascular and exercise physiology
- Keywords
- whey protein, casein, muscle protein synthesis, resistance training, myofibrillar protein synthesis, Akt signaling, p70S6K, 4E-BP1, insulin, branched-chain amino acids, leucine tracer, protein turnover
- MeSH terms
- Whey Proteins, Adult, Amino Acids, Carbon Isotopes, Caseins, Dietary Proteins, Food, Formulated, Humans, Insulin, Leucine, Male, Milk Proteins, Muscle Proteins, Myofibrils, Phosphoproteins, Phosphorylation, Signal Transduction, Single-Blind Method, Cell Cycle Proteins, Ribosomal Protein S6 Kinases, 70-kDa, Adaptor Proteins, Signal Transducing, Proto-Oncogene Proteins c-akt, Resistance Training
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review