Cited by 152Muscle metabolism and nutritionMuscle Physiology and DisordersCardiovascular and exercise physiology

The DOI matches its Crossref record; 103 of the 103 references it cites were found in a registry or an index.

Assessing the role of muscle protein breakdown in response to nutrition and exercise in humans.

Open access

Tipton, Kevin D., Hamilton, D. Lee, Gallagher, Iain J.·2018·Sports Medicine

DOI 10.1007/s40279-017-0845-5PMC PMC5790854

Open this paper in CoChat — free account Open PDF

Abstract

Muscle protein breakdown (MPB) is an important metabolic component of muscle remodeling, adaptation to training, and increasing muscle mass. Degradation of muscle proteins occurs via the integration of three main systems-autophagy and the calpain and ubiquitin-proteasome systems. These systems do not operate independently, and the regulation is complex. Complete degradation of a protein requires some combination of the systems. Determination of MPB in humans is technically challenging, leading to a relative dearth of information. Available information on the dynamic response of MPB primarily comes from stable isotopic methods with expression and activity measures providing complementary information. It seems clear that resistance exercise increases MPB, but not as much as the increase in muscle protein synthesis. Both hyperaminoacidemia and hyperinsulinemia inhibit the post-exercise response of MPB. Available data do not allow a comprehensive examination of the mechanisms behind these responses. Practical nutrition recommendations for interventions to suppress MPB following exercise are often made. However, it is likely that some degree of increased MPB following exercise is an important component for optimal remodeling. At this time, it is not possible to determine the impact of nutrition on any individual muscle protein. Thus, until we can develop and employ better methods to elucidate the role of MPB following exercise and the response to nutrition, recommendations to optimize post exercise nutrition should focus on the response of muscle protein synthesis. The aim of this review is to provide a comprehensive examination of the state of knowledge, including methodological considerations, of the response of MPB to exercise and nutrition in humans.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1007/s40279-017-0845-5

Cites

103 of 103 references verified0 citation errors · 0 not checkable

Statistics

Fig. 1 Methods of assessing skeletal muscle protein breakdown (MPB). Skeletal muscle proteins are broken down by a combination of the three main protein breakdown systems. These breakdown systems do not work in isolation but rather work together to remodel skeletal muscle. (1) The calpain proteases disassemble myofibrils into smaller component parts, (2) the ubiquitin-proteasome system degrades these component into individual amino acids, and can label proteins (membrane receptors, channels and transporters) for destruction by the third system, (3) the autophagy-lysosome system, which predominantly breaks down membrane based proteins. Dynamic MPB measures use labelled amino-acid tracers (such as phenylalanine stable-isotopes) and provide a dynamic view of whole MPB. 3-Methylhistidine is a unique metabolite of myofibrillar protein breakdown and its appearance in blood and urine can be assumed to have come from the processes of myofibrillar protein breakdown. Skeletal muscle is the body’s largest depot of myofibrillar protein so changes in plasma/urinary/interstitial 3-methylhistidine are believed reflective of skeletal MPB. Other static markers of protein breakdown include the assessment of the messenger RNA (mRNA)/protein expression/activity/localization of components of the breakdown machinery. Markers are available to estimate changes in the activity of each of the three breakdown systems. L-Phe l-phenylalanine, AV arterio-venous, MuRF muscle ring finger protein, FKHR forkhead transcription factorCC BY · PubMed Central

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Gene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., & Speleman, F. (2002) · Genome Biology · doi:10.1186/gb-2002-3-7-research0034 · Cited by 20,038
The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., et al. (2009) · Clinical Chemistry · doi:10.1373/clinchem.2008.112797 · Cited by 16,303 · cited 1×
“reporting of qRT-PCR studies were published [65].”
Sequencing technologies – the next generation
Metzker, M. L. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2626 · Cited by 7,066
Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper – Excel-based tool using pair-wise correlations
Pfaffl, M. W., Tichopad, A., Prgomet, C., & Neuvians, T. P. (2004) · Biotechnology Letters · doi:10.1023/b:bile.0000019559.84305.47 · Cited by 5,065
Identification of ubiquitin ligases required for skeletal muscle atrophy.
Bodine, S. C., Latres, E., Baumhueter, S., Lai, V. K.-M., Nunez, L., Clarke, B. A., Poueymirou, W. T., Panaro, F. J., Na, E., Dharmarajan, K., et al. (2001) · Science · doi:10.1126/science.1065874 · Cited by 3,521
Real-time RT-PCR normalisation; strategies and considerations
Huggett, J. F., Dheda, K. U. J., Bustin, S. A., & Zumla, A. I. (2005) · Genes and Immunity · doi:10.1038/sj.gene.6364190 · Cited by 1,858
Reactome: a database of reactions, pathways and biological processes
Croft, D., O'Kelly, G., Wu, G., Haw, R., Gillespie, M., Matthews, L., Caudy, M., Garapati, P., Gopinath, G., Jassal, B., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkq1018 · Cited by 1,751
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
Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression
Lecker, S. H., Jagoe, R. T., Gilbert, A., Gomes, M., Baracos, V., Bailey, J., Price, S. R., Mitch, W. E., & Goldberg, A. L. (2004) · The FASEB Journal · doi:10.1096/fj.03-0610com · Cited by 1,539
GSEA-P : a desktop application for Gene Set Enrichment Analysis
Subramanian, A., Kuehn, H., Gould, J., Tamayo, P., & Mesirov, J. P. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm369 · Cited by 1,399
Twenty-Five Years of Quantitative PCR for Gene Expression Analysis
VanGuilder, H. D., Vrana, K. E., & Freeman, W. M. (2008) · BioTechniques · doi:10.2144/000112776 · Cited by 1,246
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
The Molecular Basis of Skeletal Muscle Atrophy
Jackman, R. W., & Kandarian, S. C. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00579.2003 · Cited by 1,008 · cited 2×
“Whereas mechanistic data are lacking from human studies, data from animal models suggest that the UPP and calpain systems play a much larger role than autophagy [17].”
Background
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
Self-citation
Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions
Du, J., Wang, X., Miereles, C., Bailey, J. L., Debigaré, R., Zheng, B., Price, S. R., & Mitch, W. E. (2004) · Journal of Clinical Investigation · doi:10.1172/jci18330 · Cited by 730
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 · cited 10×
“Given that exercise increases the metabolism of the muscle with little impact on other tissues, it is a reasonable assumption that measurements made using these AV models following exercise represent changes in muscle metabolism [3, 7].”
BackgroundMethodResultInfluentialSelf-citation
Timing of amino acid-carbohydrate ingestion alters anabolic response of muscle to resistance exercise
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
Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise
Witard, O. C., Jackman, S. R., Breen, L., Smith, K., Selby, A., & Tipton, K. D. (2014) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.055517 · Cited by 517
Self-citation
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
Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis
Areta, J. L., Burke, L. M., Ross, M. L., Camera, D. M., West, D. W. D., Broad, E. M., Jeacocke, N. A., Moore, D. R., Stellingwerff, T., Phillips, S. M., et al. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2012.244897 · Cited by 495
Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle
Louis, E., Raue, U., Yang, Y., Jemiolo, B., & Trappe, S. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00679.2007 · Cited by 478
Importance of the ATP-Ubiquitin-Proteasome Pathway in the Degradation of Soluble and Myofibrillar Proteins in Rabbit Muscle Extracts
Solomon, V., & Goldberg, A. L. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.43.26690 · Cited by 433
A database for post-genome analysis
Kanehisa, M. I. (1997) · Trends in Genetics · doi:10.1016/s0168-9525(97)01223-7 · Cited by 420
Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and μ-types
Sorimachi, H., Imajoh‐Ohmi, S., Emori, Y., Kawasaki, H., Ohno, S., Minami, Y., & Suzuki, K. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)47225-6 · Cited by 381
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
With Reference to Reference Genes: A Systematic Review of Endogenous Controls in Gene Expression Studies
Chapman, J. R., & Waldenström, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0141853 · Cited by 329
Pathways to the analysis of microarray data
Curtis, R. K., Orešič, M., & Vidal‐Puig, A. (2005) · Trends in biotechnology · doi:10.1016/j.tibtech.2005.05.011 · Cited by 309
RefGenes: identification of reliable and condition specific reference genes for RT-qPCR data normalization
Hrúz, T., Wyss, M., Docquier, M., Pfaffl, M. W., Masanetz, S., Borghi, L., Verbrugghe, P., Kalaydjieva, L. V., Stefan Bleuler, A., Laule, O., et al. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-156 · Cited by 292
The involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and atrophy
Murton, A. J., Constantin, D., & Greenhaff, P. L. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.10.011 · Cited by 286
Protein and amino acids for athletes
Tipton, K. D., & Wolfe, R. R. (2004) · Journal of Sports Sciences · doi:10.1080/0264041031000140554 · Cited by 274
Self-citation
Structural Insights into E1-Catalyzed Ubiquitin Activation and Transfer to Conjugating Enzymes
Lee, I., & Schindelin, H. (2008) · Cell · doi:10.1016/j.cell.2008.05.046 · Cited by 265
Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise.
Biolo, G., Williams, B. D., Fleming, R. Y., & Wolfe, R. R. (1999) · Diabetes · doi:10.2337/diabetes.48.5.949 · Cited by 256
Effect of exercise and recovery on muscle protein synthesis in human subjects
Carraro, F., Stuart, C. A., Hartl, W. H., Rosenblatt, J., & Wolfe, R. R. (1990) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1990.259.4.e470 · Cited by 247
Nutritional interventions to augment resistance training-induced skeletal muscle hypertrophy
Morton, R. W., McGlory, C., & Phillips, S. M. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00245 · Cited by 234
Role of insulin in the regulation of human skeletal muscle protein synthesis and breakdown: a systematic review and meta-analysis
Abdulla, H., Smith, K., Atherton, P. J., & Idris, I. (2016) · Diabetologia · doi:10.1007/s00125-015-3751-0 · Cited by 229
Molecular adaptations of neuromuscular disease‐associated proteins in response to eccentric exercise in human skeletal muscle
Féasson, L., Stockholm, D., Freyssenet, D. G., Richard, I., Duguez, S., Beckmann, J. S., & Denis, C. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.018689 · Cited by 224
Non-canonical ubiquitin-based signals for proteasomal degradation
Kravtsova‐Ivantsiv, Y., & Ciechanover, A. J. (2012) · Journal of Cell Science · doi:10.1242/jcs.093567 · Cited by 221
Rapid measurement of whole body and forearm protein turnover using a [2H5]phenylalanine model
Thompson, G. N., Pacy, P. J., Merritt, H., Ford, G. C., Read, M. A., Cheng, K., & Halliday, D. (1989) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1989.256.5.e631 · Cited by 202
Postexercise protein metabolism in older and younger men following moderate-intensity aerobic exercise
Sheffield-Moore, M., Yeckel, C. W., Volpi, E., Wolf, S. E., Morio, B., Chinkes, D. L., Paddon-Jones, D., & Wolfe, R. R. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00334.2003 · Cited by 197
Control of skeletal muscle atrophy in response to disuse: clinical/preclinical contentions and fallacies of evidence
Atherton, P. J., Greenhaff, P. L., Phillips, S. M., Bodine, S. C., Adams, C. M., & Lang, C. H. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00257.2016 · Cited by 180
Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise
Glynn, E. L., Fry, C. S., Drummond, M. J., Dreyer, H. C., Dhanani, S., Volpi, E., & Rasmussen, B. B. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00077.2010 · Cited by 177
LGMD2A: genotype–phenotype correlations based on a large mutational survey on the calpain 3 gene
Sáenz, A., Leturcq, F., Cobo, A. M., Poza, J. J., Ferrer, X., Otaegui, D., Camaño, P., Urtasun, M., Vilchez, J. J., Gutiérrez‐Rivas, E., et al. (2005) · Brain · doi:10.1093/brain/awh408 · Cited by 176
Resistance-training-induced adaptations in skeletal muscle protein turnover in the fed state
Phillips, S. M., Parise, G., Roy, B. D., Tipton, K. D., Wolfe, R. R., & Tarnopolsky, M. A. (2002) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y02-134 · Cited by 168
Self-citation
Repeated resistance exercise training induces different changes in mRNA expression of MAFbx and MuRF-1 in human skeletal muscle
Mascher, H., Tannerstedt, J., Brink-Elfegoun, T., Ekblom, B. T., Gustafsson, T. P., & Blomstrand, E. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00504.2007 · Cited by 165
Measurement of Autophagy in Cells and Tissues
Tanida, I., & Waguri, S. (2010) · Methods in molecular biology · doi:10.1007/978-1-60761-756-3_13 · Cited by 162
Carbohydrate Does Not Augment Exercise-Induced Protein Accretion versus Protein Alone
STAPLES, A. W., BURD, N. A., WEST, D. W. D., CURRIE, K. D., ATHERTON, P. J., MOORE, D. R., RENNIE, M. J., MACDONALD, M. J., BAKER, S. K., & PHILLIPS, S. M. (2011) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31820751cb · Cited by 162
Harry M. Vars Research Award: A New Model to Determine in Vivo the Relationship Between Amino Acid Transmembrane Transport and Protein Kinetics in Muscle
Biolo, G., Chinkes, D. L., Zhang, X., & Wolfe, R. R. (1992) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607192016004305 · Cited by 159
Modulation of autophagy and ubiquitin-proteasome pathways during ultra-endurance running
Jamart, C., Francaux, M., Millet, G. Y., Deldicque, L., Frère, D., & Féasson, L. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00952.2011 · Cited by 157
Coingestion of carbohydrate with protein does not further augment postexercise muscle protein synthesis
Koopman, R., Beelen, M., Stellingwerff, T., Pennings, B., Saris, W. H. M., Kies, A. K., Kuipers, H., & van Loon, L. J. C. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00135.2007 · Cited by 150
Is there a maximal anabolic response to protein intake with a meal?
Deutz, N. E., & Wolfe, R. R. (2013) · Clinical Nutrition · doi:10.1016/j.clnu.2012.11.018 · Cited by 144
Interaction of contractile activity and training history on mRNA abundance in skeletal muscle from trained athletes
Coffey, V. G., SHIELD, A. J., Canny, B. J., Carey, K. A., Cameron‐Smith, D., & Hawley, J. A. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00299.2005 · Cited by 144
Skeletal muscle and resistance exercise training; the role of protein synthesis in recovery and remodeling
McGlory, C., Devries, M. C., & Phillips, S. M. (2017) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00613.2016 · Cited by 135
Human NADH:ubiquinone oxidoreductase deficiency: radical changes in mitochondrial morphology?
Koopman, W. J. H., Verkaart, S., Visch, H.-J., Vries, S. E. V. E., Nijtmans, L. G. J., Smeitink, J. A. M., & Willems, P. H. G. M. (2007) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00194.2006 · Cited by 134
Protein Considerations for Optimising Skeletal Muscle Mass in Healthy Young and Older Adults
Witard, O., Wardle, S., Macnaughton, L., Hodgson, A., & Tipton, K. (2016) · Nutrients · doi:10.3390/nu8040181 · Cited by 132
Self-citation
Exercise‐induced changes in protein metabolism
Tipton, K. D., & Wolfe, R. R. (1998) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1998.00306.x · Cited by 125
Self-citation
Proteolytic mRNA expression in response to acute resistance exercise in human single skeletal muscle fibers
Yang, Y., Jemioło, B., & Trappe, S. W. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00438.2006 · Cited by 125
Calcium-dependent proteolytic system and muscle dysfunctions: A possible role of calpains in sarcopenia
Dargelos, É., Poussard, S., Brulé, C., Daury, L., & Cottin, P. (2007) · Biochimie · doi:10.1016/j.biochi.2007.07.018 · Cited by 116
Ca2+ activation of diffusible and bound pools of μ‐calpain in rat skeletal muscle
Murphy, R. M., Verburg, E., & Lamb, G. D. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.114090 · Cited by 114
Influence of age and resistance exercise on human skeletal muscle proteolysis: a microdialysis approach
Trappe, T. A., Williams, R. H., Carrithers, J. A., Raue, U., Esmarck, B., Kjær, M., & Hickner, R. C. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.051755 · Cited by 100
Endoplasmic Reticulum Stress Markers and Ubiquitin-Proteasome Pathway Activity in Response to a 200-km Run
Kim, H. J., Jamart, C., Deldicque, L., An, G.-L., Lee, Y. H., Kim, C. K., Raymackers, J., & Francaux, M. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181e4c5d1 · Cited by 94
Intake of branched-chain amino acids influences the levels of MAFbx mRNA and MuRF-1 total protein in resting and exercising human muscle
Moberg, M., Apró, W., & Blomstrand, E. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00353.2011 · Cited by 93
Pronounced energy restriction with elevated protein intake results in no change in proteolysis and reductions in skeletal muscle protein synthesis that are mitigated by resistance exercise
Hector, A. J., McGlory, C., Damas, F., Mazara, N., Baker, S. K., & Phillips, S. M. (2018) · The FASEB Journal · doi:10.1096/fj.201700158rr · Cited by 91
An isotopic method for measurement of muscle protein fractional breakdown rate in vivo
Zhang, X. J., Chinkes, D. L., Sakurai, Y., & Wolfe, R. R. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.270.5.e759 · Cited by 90
Measurement of muscle protein fractional synthesis and breakdown rates from a pulse tracer injection
Zhang, X., Chinkes, D. L., & Wolfe, R. R. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00053.2002 · Cited by 88
Assessment of skeletal muscle proteolysis and the regulatory response to nutrition and exercise
Pasiakos, S. M., & Carbone, J. W. (2014) · IUBMB Life · doi:10.1002/iub.1291 · Cited by 79
NO upregulation of a cyclic nucleotide-gated channel contributes to calcium elevation in endothelial cells
Zhang, J., Xia, S., Block, E. R., & Patel, J. M. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00048.2002 · Cited by 78
In vivo analysis of fluid transport in cystic fibrosis airway epithelia of bronchial xenografts
Zhang, J. Y., Yankaskas, J. R., Wilson, J. M., & Engelhardt, J. F. (1996) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1996.270.5.c1326 · Cited by 77
Human soleus muscle protein synthesis following resistance exercise
Trappe, T. A., Raue, U., & Tesch, P. A. (2004) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2004.01348.x · Cited by 76
Calpain-3 is autolyzed and hence activated in human skeletal muscle 24 h following a single bout of eccentric exercise
Murphy, R. M., Goodman, C. A., McKenna, M. J., Bennie, J. A., Leikis, M. J., & Lamb, G. D. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01422.2006 · Cited by 73
Dynamic proteome profiling of individual proteins in human skeletal muscle after a high-fat diet and resistance exercise
Camera, D. M., Burniston, J. G., Pogson, M. A., Smiles, W. J., & Hawley, J. A. (2017) · The FASEB Journal · doi:10.1096/fj.201700531r · Cited by 72
Regulation of ubiquitin proteasome pathway molecular markers in response to endurance and resistance exercise and training
Stefanetti, R. J., Lamon, S., Wallace, M. A., Vendelbo, M. H., Russell, A. P., & Vissing, K. (2014) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-014-1587-y · Cited by 71
Protein synthesis and breakdown in skin and muscle: a leg model of amino acid kinetics
Biolo, G., Gastaldelli, A., Zhang, X. J., & Wolfe, R. R. (1994) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1994.267.3.e467 · Cited by 71
Evidence Based Selection of Commonly Used RT-qPCR Reference Genes for the Analysis of Mouse Skeletal Muscle
Thomas, K. C., Zheng, X., Suarez, F. G., Raftery, J. M., Quinlan, K. G. R., Yang, N., North, K. N., & Houweling, P. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088653 · Cited by 69
The meteoric rise of regulated intracellular proteolysis
Mayer, R. J. (2000) · Nature Reviews Molecular Cell Biology · doi:10.1038/35040090 · Cited by 66
Identifying aggressive prostate cancer foci using a DNA methylation classifier
Mundbjerg, K., Chopra, S. S., Mehrdad Alemozaffar, A., Duymich, C. E., Lakshminarasimhan, R., Nichols, P. W., Aron, M., Siegmund, K. D., Ukimura, O., Aron, M., et al. (2017) · Genome biology · doi:10.1186/s13059-016-1129-3 · Cited by 64
Expression patterns of atrogenic and ubiquitin proteasome component genes with exercise: effect of different loading patterns and repeated exercise bouts
Nedergaard, A., Vissing, K., Overgaard, K., Kjær, M., & Schjerling, P. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01445.2006 · Cited by 57
Endogenous Calpain-3 Activation Is Primarily Governed by Small Increases in Resting Cytoplasmic [Ca2+] and Is Not Dependent on Stretch
Murphy, R. M., & Lamb, G. D. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m808655200 · Cited by 55
Effects of short-term energy deficit on muscle protein breakdown and intramuscular proteolysis in normal-weight young adults
Carbone, J. W., Pasiakos, S. M., Vislocky, L. M., Anderson, J. M., & Rodriguez, N. R. (2014) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2013-0433 · Cited by 49
Internal comparison between deuterium oxide (D2O) and L-[ring-13C6] phenylalanine for acute measurement of muscle protein synthesis in humans
Wilkinson, D. J., Cegielski, J., Phillips, B. E., Boereboom, C., Lund, J. N., Atherton, P. J., & Smith, K. (2015) · Physiological Reports · doi:10.14814/phy2.12433 · Cited by 49
Determination of steady-state protein breakdown rate in vivo by the disappearance of protein-bound tracer-labeled amino acids: a method applicable in humans
Holm, L., O’Rourke, B., Ebenstein, D. B., Toth, M. J., Bechshoeft, R. L., Holstein‐Rathlou, N., Kjær, M., & Matthews, D. E. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00579.2012 · Cited by 44
Practical considerations in the use of stable isotope labelled compounds as tracers in clinical studies
Thompson, G. N., Pacy, P. J., Ford, G. C., & Halliday, D. (1989) · Journal of Mass Spectrometry · doi:10.1002/bms.1200180507 · Cited by 38
Effects of pre-exercise feeding on serum hormone concentrations and biomarkers of myostatin and ubiquitin proteasome pathway activity
Dalbo, V. J., Roberts, M. D., Hassell, S., & Kerksick, C. M. (2013) · European Journal of Nutrition · doi:10.1007/s00394-012-0349-x · Cited by 35
Influence of divergent exercise contraction mode and whey protein supplementation on atrogin-1, MuRF1, and FOXO1/3A in human skeletal muscle
Stefanetti, R. J., Lamon, S., Rahbek, S. K., Farup, J., Zacharewicz, E., Wallace, M. A., Vendelbo, M. H., Russell, A. P., & Vissing, K. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00136.2013 · Cited by 35
Methods for measuring tissue protein breakdown rate in vivo
Chinkes, D. L. (2005) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/01.mco.0000170754.25372.37 · Cited by 34
Pleiotropic Effects of ATP·Mg2+ Binding in the Catalytic Cycle of Ubiquitin-activating Enzyme
Tokgöz, Z., Bohnsack, R. N., & Haas, A. L. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m513562200 · Cited by 34
Molecular Responses to Moderate Endurance Exercise in Skeletal Muscle
Pasiakos, S. M., McClung, H. L., McClung, J. P., Urso, M. L., Pikosky, M. A., Cloutier, G. J., Fielding, R. A., & Young, A. (2010) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.20.4.282 · Cited by 33
Positive muscle protein net balance and differential regulation of atrogene expression after resistance exercise and milk protein supplementation
Reitelseder, S., Agergaard, J., Doessing, S., Helmark, I. C., Schjerling, P., van Hall, G., Kjær, M., & Holm, L. (2013) · European Journal of Nutrition · doi:10.1007/s00394-013-0530-x · Cited by 32
The impact of postexercise essential amino acid ingestion on the ubiquitin proteasome and autophagosomal-lysosomal systems in skeletal muscle of older men
Dickinson, J. M., Reidy, P. T., Gundermann, D. M., Borack, M. S., Walker, D. K., D’Lugos, A. C., Volpi, E., & Rasmussen, B. B. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00632.2016 · Cited by 30
Contractile protein breakdown in human leg skeletal muscle as estimated by [2H3]-3-methylhistidine: A new method
Vesali, R. F., Klaude, M., Thunblad, L., Rooyackers, O., & Wernerman, J. (2004) · Metabolism · doi:10.1016/j.metabol.2004.02.017 · Cited by 28
ICAM-1-mediated leukocyte adhesion is critical for the activation of endothelial LSP1
Hossain, M., Qadri, S. M., Su, Y., & Liu, L. (2013) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00297.2012 · Cited by 28
Method for the determination of the arteriovenous muscle protein balance during non-steady-state blood and muscle amino acid concentrations
Katsanos, C. S., Chinkes, D. L., Sheffield‐Moore, M., Aarsland, A. A., Kobayashi, H., & Wolfe, R. R. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00141.2005 · Cited by 26
Reliability of results and interpretation of measures of 3-methylhistidine in muscle interstitium as marker of muscle proteolysis
Rennie, M. J., Phillips, S. M., & Smith, K. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.90782.2008 · Cited by 23
Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise
Glynn, E. L., Fry, C. S., Drummond, M. J., Dreyer, H. C., Dhanani, S., Volpi, E., & Rasmussen, B. B. (2010) · The FASEB Journal · doi:10.1096/fasebj.24.1_supplement.740.5 · Cited by 22
A proteomics strategy for determining the synthesis and degradation rates of individual proteins in fish
Doherty, M. K., Brownridge, P., Owen, M. A. G., Davies, S. J., Young, I. S., & Whitfield, P. D. (2012) · Journal of Proteomics · doi:10.1016/j.jprot.2012.03.025 · Cited by 22
Myofibrillar proteolysis in response to voluntary or electrically stimulated muscle contractions in humans
Hansen, M., Trappe, T. A., Crameri, R. M., Qvortrup, K., Kjær, M., & Langberg, H. (2009) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2007.00766.x · Cited by 21
Measuring protein breakdown rate in individual proteins in vivo
Holm, L., & Kjær, M. (2010) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32833c3c64 · Cited by 20
The effect of strenuous aerobic exercise on skeletal muscle myofibrillar proteolysis in humans
Haus, J. M., Miller, B. F., Carroll, C. C., Weinheimer-Haus, E. M., & Trappe, T. A. (2006) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2006.00566.x · Cited by 18
A novel stable isotope tracer method to measure muscle protein fractional breakdown rate during a physiological non-steady-state condition
Tuvdendorj, D., Chinkes, D. L., Herndon, D. N., Zhang, X., & Wolfe, R. R. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00552.2012 · Cited by 17
Assessing the regulation of skeletal muscle plasticity in response to protein ingestion and resistance exercise
McGlory, C., & Phillips, S. M. (2014) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000083 · Cited by 15
Aging and Sequential Resistance Exercise Bout Effects on Housekeeping Gene Messenger RNA Expression in Human Skeletal Muscle
Sunderland, K., Roberts, M. D., Dalbo, V. J., & Kerksick, C. M. (2012) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e3182779830 · Cited by 7
Muscling in on microarrays
Virtanen, C., & Takahashi, M. T. (2008) · Applied Physiology Nutrition and Metabolism · doi:10.1139/h07-150 · Cited by 7
Application of deuterium oxide (D2O) to metabolic research: just D2O it? Depends just how you D2O it!
Wilkinson, D. J., Atherton, P. J., Phillips, B. E., Greenhaff, P. L., & Smith, K. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00581.2014 · Cited by 6

Sorted by citations

Skeletal muscle atrophy: From mechanisms to treatments
Yin, L., Li, N., Jia, W., Wang, N., Liang, M., Yang, X., & Du, G. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105807 · Cited by 423
Stimuli and sensors that initiate skeletal muscle hypertrophy following resistance exercise
Wackerhage, H., Schoenfeld, B. J., Hamilton, D. L., Lehti, M., & Hulmi, J. J. (2019) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00685.2018 · Cited by 357
Self-citation
Metabolite Concentration Changes in Humans After a Bout of Exercise: a Systematic Review of Exercise Metabolomics Studies
Schranner, D., Kastenmüller, G., Schönfelder, M., Römisch‐Margl, W., & Wackerhage, H. (2020) · Sports Medicine - Open · doi:10.1186/s40798-020-0238-4 · Cited by 263
Mechanisms of mechanical overload-induced skeletal muscle hypertrophy: current understanding and future directions
Roberts, M. D., McCarthy, J. J., Hornberger, T. A., Phillips, S. M., Mackey, A. L., Nader, G. A., Boppart, M. D., Kavazis, A. N., Reidy, P. T., Ogasawara, R., et al. (2023) · Physiological Reviews · doi:10.1152/physrev.00039.2022 · Cited by 214
Antioxidant and Adaptative Response Mediated by Nrf2 during Physical Exercise
Vargas-Mendoza, N., Morales‐González, Á., Madrigal‐Santillán, E., Madrigal‐Bujaidar, E., Álvarez‐González, I., García-Melo, L. F., Anguiano‐Robledo, L., Fregoso-Aguilar, T. A., & Morales‐González, J. A. (2019) · Antioxidants · doi:10.3390/antiox8060196 · Cited by 170

See all 152

Authors: Tipton, K. D., Hamilton, D. L., & Gallagher, I. J.
Affiliations: University of Stirling (GB)
Corresponding author: Tipton, Kevin D.
ORCID: Tipton, Kevin D.
Hamilton, D. Lee
Gallagher, Iain J.
Venue: Sports Medicine
Publisher: Springer Science and Business Media LLC
Published: 2018-01-24
Volume: 48
Issue: S1
Pages: 53-64
ISSN: 0112-1642 (ISSN-L)
1179-2035
DOI: 10.1007/s40279-017-0845-5
PMC: PMC5790854
OpenAlex: W2785778503
Cited by: 152
References: 103
Citations by year: 2026: 12 · 2025: 16 · 2024: 20 · 2023: 20 · 2022: 28 · 2021: 26 · 2020: 16 · 2019: 8 · 2018: 6
FWCI: 1.57
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
Locations: Sports Medicine (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Durham Research Online (Durham University) (acceptedVersion, cc-by)
Durham Research Online (Durham University) (submittedVersion, cc-by)
Deakin Research Online (Deakin University) (submittedVersion)
Stirling Online Research Repository (University of Stirling) (submittedVersion, cc-by)
Figshare (submittedVersion, cc-by)
Funders: PepsiCo
Gran Sasso Science Institute
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: muscle protein degradation, muscle protein synthesis, resistance training, post-exercise nutrition, autophagy, calpain, ubiquitin-proteasome system, hyperaminoacidemia, hyperinsulinemia, muscle remodeling, muscle mass
MeSH terms: Humans, Muscle Proteins, Nutritional Status, Exercise, Muscle, Skeletal

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

Assessing the role of muscle protein breakdown in response to nutrition and exercise in humans.

Abstract

Overview

Integrity signals

Figures

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks