Skeletal muscle responses to negative energy balance: Effects of dietary protein
Open accessAbstract
Sustained periods of negative energy balance decrease body mass due to losses of both fat and skeletal muscle mass. Decreases in skeletal muscle mass are associated with a myriad of negative consequences, including suppressed basal metabolic rate, decreased protein turnover, decreased physical performance, and increased risk of injury. Decreases in skeletal muscle mass in response to negative energy balance are due to imbalanced rates of muscle protein synthesis and degradation. However, the underlying physiological mechanisms contributing to the loss of skeletal muscle during energy deprivation are not well described. Recent studies have demonstrated that consuming dietary protein at levels above the current recommended dietary allowance (0.8 g · kg(-1) · d(-1)) may attenuate the loss of skeletal muscle mass by affecting the intracellular regulation of muscle anabolism and proteolysis. However, the specific mechanism by which increased dietary protein spares skeletal muscle through enhanced molecular control of muscle protein metabolism has not been elucidated. This article reviews the available literature related to the effects of negative energy balance on skeletal muscle mass, highlighting investigations that assessed the influence of varying levels of dietary protein on skeletal muscle protein metabolism. Further, the molecular mechanisms that may contribute to the regulation of skeletal muscle mass in response to negative energy balance and alterations in dietary protein level are described.
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In response to sustained NEB, there is a downregulation of whole-body protein turnover including SM protein synthesis in the early stages, probably to conserve energy and protein reserves.
“in response to sustained NEB, there is a downregulation of whole-body protein turnover including SM protein synthesis in the early stages, probably to conserve energy and protein reserves [85].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
The passages on whole-body protein turnover report decreases during sustained energy deficit, and the muscle-synthesis passage suggests a decrease in the early stages of negative energy balance. The claim states these responses more definitively than the review does and omits its qualification that the whole-body finding may depend on dietary protein intake being at the recommended level. No page numbers are provided in our copy. (LLM, conf=0.82)
Experimental — accuracy not yet measuredLoss of SM mass has a negative impact on metabolic processes (including downregulation of protein turnover and basal metabolic rate (BMR) and worsening IR), physical performance, SM function, and susceptibility to physical injury.
“Such a loss of SM mass has a negative impact on metabolic processes (including a downregulation of protein turnover and BMR and a worsening IR), physical performance, SM function, and susceptibility to physical injury [85].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
The Introduction links skeletal muscle loss to reduced protein turnover and basal metabolic rate, poorer muscular function and physical performance, and greater susceptibility to injury. The paper does not say that muscle loss worsens insulin resistance; its discussion of insulin concerns a possible mechanism of muscle proteolysis during negative energy balance. (LLM, conf=0.88)
Experimental — accuracy not yet measuredAcute periods of NEB result in an increase in whole-body proteolysis, amino acid (AA) oxidation, and nitrogen excretion.
“Acute periods of NEB result in an increase in whole-body proteolysis, AA oxidation, and nitrogen excretion [85].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
The passage discussing whole-body protein turnover (section label rendered '$d 21 ).)'; page not provided) states that acute negative energy balance associated with fasting increases all three measures. The citing sentence omits the fasting qualification, extending the statement to acute negative energy balance generally. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIn that study, there was a lower reduction in FFM (17.3%) for women consuming a HPD compared to those on a low-protein diet (FFM loss of 37.5%).
“there was a lower reduction in FFM (17.3%) for those women consuming a HPD compared to those on a low-protein diet (FFM loss of 37.5%) [85,106].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
The discussion of negative energy balance and dietary protein intake (passage 1; page not supplied) reports the 17.3% and 37.5% figures for women on high- and low-protein diets. But these are the percentages of total weight loss attributable to FFM loss, not percentage reductions in FFM itself as the citing sentence suggests. (LLM, conf=0.88)
Experimental — accuracy not yet measuredOne key lifestyle approach to mitigate against the diminishment of SM mass and function is a nutritional strategy to ensure the provision of a high-protein diet (HPD): a diet with protein intake in excess of the usual recommended dietary allowance (0.8 g/kg/day).
“One key lifestyle approach to mitigate against the diminishment of SM mass and function is a nutritional strategy to ensure the provision of a HPD: a diet that consists of a protein intake in excess of the usual recommended dietary allowance (0.8 g kg−1 day−1) [85].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
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Enhanced SM proteolysis is regulated through caspase-mediated and ubiquitin proteasome systems.
“the enhanced SM proteolysis that occurs within the SM is regulated through ‘caspase-mediated’ and ‘ubiquitin proteasome’ systems [85].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
Enhanced SM proteolysis occurs in response to hypoinsulinaemia, a physiological feature of NEB.
“this provides a mechanism whereby enhanced SM proteolysis occurs in response to hypoinsulinaemia (a physiological feature of NEB) [85,90].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
Following sustained periods of NEB, typically around 25% of total body weight loss stems from Fat-Free Mass (FFM), of which SM forms a major component, with typically just 75% of body weight loss being from AT.
“following sustained periods of NEB, typically around 25% of total body weight loss stems from Fat-Free Mass (FFM), of which the SM forms a major component, with typically just 75% of body weight loss being from the AT [85,86].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
A 10-day moderate NEB resulted in a 19% reduction in fasting SM protein synthesis.
“a 10-day moderate NEB resulted in a 19% reduction in fasting SM protein synthesis [85,90].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
AMPK acts as a fuel sensor within SM (with downstream inhibitory effects on mTORC1 activity), and inhibits anabolic signalling pathways in response to limited energy availability and a reduction in cellular ATP.
“‘AMP-activated protein kinase’ (AMPK) also acts as a fuel sensor within the SM (with downstream inhibitory effects on mTORC1 activity [91]), and inhibits anabolic signalling pathways in response to limited energy availability and a reduction in cellular levels of ATP [85].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
Branched-chain amino acids (BCAAs) maintain SM protein synthesis and attenuate nitrogen excretion and muscle proteolysis.
“branched-chain AAs (BCAAs) maintain SM protein synthesis and attenuate nitrogen excretion and muscle proteolysis [85,110].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
Leucine is a potent stimulator of SM protein synthesis, and in human studies the consumption of a leucine-containing food product during physical exercise decreased whole-body proteolysis and increased SM protein synthesis through stimulation of the mTORC1 pathway.
“leucine is a potent stimulator of SM protein synthesis, and in human studies the consumption of a leucine-containing food product during physical exercise decreased whole-body proteolysis and increased SM protein synthesis through stimulation of the mTORC1 pathway [85,112].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
In postmenopausal women with obesity, the extent of SM loss in response to NEB was proportional to dietary protein intake.
“a study on postmenopausal women with obesity in which the extent of SM loss in response to NEB was proportional to dietary protein intake [85,106].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
In the context of NEB, negative nitrogen balance (including increased nitrogen excretion) generally occurs, and increasing dietary protein intake can offset this process.
“In the context of NEB, negative nitrogen balance (including increased nitrogen excretion) generally occurs, and increasing dietary protein intake can offset this process [85].”
From Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management (2025) · cites this paper as [85]
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Cites
Hershko, A., & Ciechanover, A. (1998) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.67.1.425 · Cited by 8,840 · see citing works
The Ubiquitin-Proteasome Proteolytic Pathway: Destruction for the Sake of Construction
Glickman, M. H., & Ciechanover, A. J. (2002) · Physiological Reviews · doi:10.1152/physrev.00027.2001 · Cited by 4,216 · see citing works
Goll, D. E., Thompson, V. F., Li, H., WEI, W., & Cong, J. (2003) · Physiological Reviews · doi:10.1152/physrev.00029.2002 · Cited by 2,826 · see citing works
Stitt, T. N., Drujan, D., Clarke, B. A., Panaro, F., Timofeyva, Y., Kline, W. O., Gonzalez, M., Yancopoulos, G. D., & Glass, D. J. (2004) · Molecular Cell · doi:10.1016/s1097-2765(04)00211-4 · Cited by 1,964 · see citing works
Energy and protein requirements : report of a Joint FAO/WHO/UNU Expert Consultation
Fao, J., Energy, U. E. C. O., & Requirements, P. (1985) · Medical Entomology and Zoology · Cited by 1,857 · see citing works
Reduced Rate of Energy Expenditure as a Risk Factor for Body-Weight Gain
Ravussin, E., Lillioja, S., Knowler, W. C., Christin, L., Freymond, D., Abbott, W. G. H., Boyce, V., Howard, B. V., & Bogardus, C. (1988) · New England Journal of Medicine · doi:10.1056/nejm198802253180802 · Cited by 1,215 · see citing works
Bolster, D. R., Crozier, S. J., Kimball, S. R., & Jefferson, L. S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c200171200 · Cited by 851 · see citing works
Skov, A., Toubro, S., Rønn, B., Holm, L., & Astrup, A. (1999) · International Journal of Obesity · doi:10.1038/sj.ijo.0800867 · Cited by 743 · see citing works
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 · see citing works
Energy and protein requirements the 1985 report of the 1981 Joint FAO/WHO/UNU Expert Consultation
Livesey, G. (1987) · Nutrition Bulletin · doi:10.1111/j.1467-3010.1987.tb00040.x · Cited by 674 · see citing works
Layman, D. K., Boileau, R. A., Erickson, D. J., Painter, J. E., Shiue, H., Sather, C., & Christou, D. D. (2003) · The Journal of Nutrition · doi:10.1093/jn/133.2.411 · Cited by 541 · see citing works
Latres, E., Amini, A. R., Amini, A. A., Griffiths, J. S., Martin, F. J., Wei, Y., Lin, H. C., Yancopouloš, G., & Glass, D. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m407517200 · Cited by 514 · see citing works
Tran, H. G., Brunet, A., Griffith, E. C., & Greenberg, M. E. (2003) · Science Signaling · doi:10.1126/stke.2003.172.re5 · Cited by 456 · see citing works
Sandri, M. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.01.056 · Cited by 451 · see citing works
Farnsworth, E., Luscombe, N. D., Noakes, M., Wittert, G., Argyiou, E., & Clifton, P. M. (2003) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/78.1.31 · Cited by 438 · cited 1× · see citing works
“Others have also demonstrated benefits of consuming higher protein diets during prolonged periods of negative energy balance, with consistent reports documenting the attenuation of the loss of FFM after weight loss (4,6).”
BackgroundSolomon, V., & Goldberg, A. L. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.43.26690 · Cited by 432 · see citing works
Intracellular signaling during skeletal muscle atrophy
Kandarian, S. C., & Jackman, R. W. (2005) · Muscle & Nerve · doi:10.1002/mus.20442 · Cited by 393 · see citing works
Weinheimer, E. M., Sands, L. P., & Campbell, W. W. (2010) · Nutrition Reviews · doi:10.1111/j.1753-4887.2010.00298.x · Cited by 391 · see citing works
Regulation of Muscle Protein Degradation
Lee, S. W., Dai, G., Hu, Z., Wang, X., Du, J., & Mitch, W. E. (2004) · Journal of the American Society of Nephrology · doi:10.1097/01.asn.0000127211.86206.e1 · Cited by 323 · see citing works
P ROTEIN AND A MINO A CID M ETABOLISM D URING AND A FTER E XERCISE AND THE E FFECTS OF N UTRITION
Rennie, M. J., & Tipton, K. D. (2000) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.20.1.457 · Cited by 321 · see citing works
Drummond, M. J., & Rasmussen, B. B. (2008) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/mco.0b013e3282fa17fb · Cited by 274 · see citing works
Nitrogen Balance as Related to Caloric and Protein Intake in Active Young Men
Calloway, D. H., & Spector, H. (1954) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/2.6.405 · Cited by 269 · see citing works
Tiao, G. M., Hobler, S. C., Wang, J. J., Meyer, T. A., Luchette, F. A., Fischer, J. E., & Hasselgren, P.-O. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119143 · Cited by 264 · see citing works
Doyle, A., Zhang, G., Fattah, E. A. A., Eissa, N. T., & Li, Y. (2011) · The FASEB Journal · doi:10.1096/fj.10-164152 · Cited by 256 · see citing works
Proteasomes: Machines for All Reasons
Demartino, G., & Gillette, T. G. (2007) · Cell · doi:10.1016/j.cell.2007.05.007 · Cited by 239 · see citing works
Leucine as a regulator of whole body and skeletal muscle protein metabolism in humans
Nair, K. S., Schwartz, R. G., & Welle, S. L. (1992) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1992.263.5.e928 · Cited by 225 · see citing works
Mansoor, O., Beaufrère, B., Boirie, Y., Rallière, C., Taillandier, D., AUROUSSEAU, E., Schoeffler, P., Arnal, M., & Attaix, D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.7.2714 · Cited by 221 · see citing works
Metabolic Adaptation to Low Intakes of Energy and Protein
Waterlow, J. C. (1986) · Annual Review of Nutrition · doi:10.1146/annurev.nu.06.070186.002431 · Cited by 206 · see citing works
Glynn, E. L., Fry, C. S., Drummond, M. J., Timmerman, K. L., Dhanani, S., Volpi, E., & Rasmussen, B. B. (2010) · The Journal of Nutrition · doi:10.3945/jn.110.127647 · Cited by 194 · see citing works
Increased Muscle Proteasome Activity Correlates With Disease Severity in Gastric Cancer Patients
Bossola, M., Muscaritoli, M., Costelli, P., Grieco, G., Bonelli, G., Pacelli, F., Fanelli, F., Doglietto, G., & Baccino, F. (2003) · Annals of Surgery · doi:10.1097/01.sla.0000055225.96357.71 · Cited by 189 · see citing works
Leucine and Protein Synthesis: mTOR and Beyond
Stipanuk, M. H. (2008) · Nutrition Reviews · doi:10.1111/j.1753-4887.2007.tb00289.x · Cited by 178 · see citing works
Pasiakos, S. M., Vislocky, L. M., Carbone, J. W., Altieri, N., Konopelski, K., Freake, H. C., Anderson, J. M., Ferrando, A. A., Wolfe, R. R., & Rodriguez, N. R. (2010) · The Journal of Nutrition · doi:10.3945/jn.109.118372 · Cited by 176 · see citing works
Jiang, W., Zhu, Z., & Thompson, H. J. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-6721 · Cited by 175 · see citing works
Dietary composition and physiologic adaptations to energy restriction
Agus, M. S. D., SWAIN, J. F., Larson, C. L., Eckert, E. A., & Ludwig, D. S. (2000) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/71.4.901 · Cited by 163 · see citing works
Effect of Infused Branched-Chain Amino Acids on Muscle and Whole-Body Amino Acid Metabolism in Man
Louard, R. J., Barrett, E. J., & Gelfand, R. A. (1990) · Clinical Science · doi:10.1042/cs0790457 · Cited by 157 · see citing works
Young, V. R., & Borgonha, S. (2000) · Journal of Nutrition · doi:10.1093/jn/130.7.1841s · Cited by 156 · see citing works
Ca2+-dependent proteolysis in muscle wasting
Costelli, P., Reffo, P., Penna, F., Autelli, R., Bonelli, G., & Baccino, F. M. (2005) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2005.03.010 · Cited by 151 · see citing works
Nitrogen Balance of Men with Marginal Intakes of Protein and Energy
Calloway, D. H. (1975) · Journal of Nutrition · doi:10.1093/jn/105.7.914 · Cited by 138 · see citing works
Amino acids and mTOR signalling in anabolic function
Proud, C. G. (2007) · Biochemical Society Transactions · doi:10.1042/bst0351187 · Cited by 129 · see citing works
Torrazza, R. J. M., Suryawan, A., Gazzaneo, M. C., Orellana, R. A., Frank, J. W., Nguyen, H. V., Fiorotto, M. L., El‐Kadi, S. W., & Davis, T. A. (2010) · Journal of Nutrition · doi:10.3945/jn.110.128421 · Cited by 124 · see citing works
Pasiakos, S. M., McClung, H. L., McClung, J. P., Margolis, L. M., Andersen, N. E., Cloutier, G. J., Pikosky, M. A., Rood, J. C., Fielding, R. A., & Young, A. J. (2011) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.017061 · Cited by 118 · see citing works
Self-citationLeucine, glucose, and energy metabolism after 3 days of fasting in healthy human subjects
Nair, K. S., Woolf, P. D., Welle, S. L., & Matthews, D. E. (1987) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/46.4.557 · Cited by 118 · see citing works
Protein Quantity and Quality at Levels above the RDA Improves Adult Weight Loss
Layman, D. K. (2004) · Journal of the American College of Nutrition · doi:10.1080/07315724.2004.10719435 · Cited by 114 · see citing works
Alterations in mRNA expression and protein products following spinal cord injury in humans
Urso, M. L., Chen, Y., Scrimgeour, A. G., Lee, P. C., Lee, K. F., & Clarkson, P. M. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2006.118042 · Cited by 111 · see citing works
Overnight branched-chain amino acid infusion causes sustained suppression of muscle proteolysis
Louard, R. J., Barrett, E. J., & Gelfand, R. (1995) · Metabolism · doi:10.1016/0026-0495(95)90047-0 · Cited by 105 · see citing works
Nakashima, K., Ishida, A., Yamazaki, M., & Abé, H. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.08.138 · Cited by 102 · see citing works
Reiter, A. K., Bolster, D. R., Crozier, S. J., Kimball, S. R., & Jefferson, L. S. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00333.2004 · Cited by 75 · see citing works
Campbell, W. W., Haub, M. D., Wolfe, R. R., Ferrando, A. A., Sullivan, D. H., Apolzan, J. W., & Iglay, H. B. (2009) · Obesity · doi:10.1038/oby.2009.2 · Cited by 74 · see citing works
Leucine metabolism during fasting and exercise
Knapik, J. J., Meredith, C. N., Jones, B., Fielding, R. A., Young, V. R., & Evans, W. P. (1991) · Journal of Applied Physiology · doi:10.1152/jappl.1991.70.1.43 · Cited by 74 · see citing works
Oral Branched‐Chain Amino Acids Decrease Whole‐Body Proteolysis
Ferrando, A. A., Williams, B. D., Stuart, C. A., Lane, H. W., & Wolfe, R. R. (1995) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/014860719501900147 · Cited by 68 · see citing works
Wohlgemuth, S. E., Lees, H. A., Marzetti, E., Manini, T. M., Aranda, J. M., Daniels, M. J., Pahor, M., Perri, M. G., Leeuwenburgh, C., & Anton, S. D. (2011) · Rejuvenation Research · doi:10.1089/rej.2010.1132 · Cited by 65 · see citing works
Effect of reduced dietary intake on energy expenditure, protein turnover, and glucose cycling in man
Stein, T. P., Rumpler, W. V., Leskiw, M. J., Schluter, M. D., Staples, R., & Bodwell, C. E. (1991) · Metabolism · doi:10.1016/0026-0495(91)90228-o · Cited by 62 · see citing works
Response of alanine metabolism in humans to manipulation of dietary protein and energy intakes
Yang, R. D., Matthews, D. E., Bier, D. M., Wen, Z. M., & Young, V. R. (1986) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1986.250.1.e39 · Cited by 57 · see citing works
Three weeks of caloric restriction alters protein metabolism in normal-weight, young men
Friedlander, A. L., Braun, B., Pollack, M., MacDonald, J. R., Fulco, C. S., Muza, S. R., Rock, P. B., Henderson, G. C., Horning, M. A., Brooks, G. A., et al. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00001.2005 · Cited by 56 · see citing works
Pasiakos, S. M., & McClung, J. P. (2011) · Nutrition Reviews · doi:10.1111/j.1753-4887.2011.00420.x · Cited by 53 · see citing works
Self-citationIncreased Protein Maintains Nitrogen Balance during Exercise-Induced Energy Deficit
Pikosky, M. A., Smith, T. J., Grediagin, A., Castaneda‐Sceppa, C., Byerley, L. O., Glickman, E. L., & Young, A. (2008) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31815f6643 · Cited by 52 · see citing works
Increased leucine flux in short-term fasted human subjects: evidence for increased proteolysis
Tsalikian, E., Howard, C., Gerich, J. E., & Haymond, M. W. (1984) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1984.247.3.e323 · Cited by 52 · see citing works
Protein metabolic effects of a prolonged fast and hypocaloric refeeding
Hoffer, L. J., & Forse, R. A. (1990) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1990.258.5.e832 · Cited by 52 · see citing works
Effects of dietary protein on the composition of weight loss in post-menopaus al women
Gordons, M. M., Bopp, M. J., Easter, L., Miller, G. D., Lyles, M. F., Houston, D. K., Nicklas, B. J., & Kritchevsky, S. B. (2008) · The Journal of nutrition, health and aging · doi:10.1007/bf02983202 · Cited by 50 · see citing works
Villareal, D. T., Smith, G. I., Shah, K., & Mittendorfer, B. (2012) · Obesity · doi:10.1038/oby.2011.280 · Cited by 49 · see citing works
Daily requirement for and splanchnic uptake of leucine in healthy adult Indians
Kurpad, A. V., Raj, T. D. S., El-Khoury, A. E., Kuriyan, R., Maruthy, K., Borgonha, S., Chandukudlu, D., Regan, M. M., & Young, V. R. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/74.6.747 · Cited by 40 · see citing works
Regulation of ATP-ubiquitin-dependent proteolysis in muscle wasting
Attaix, D., Taillandier, D., Temparis, S., Larbaud, D., AUROUSSEAU, E., Combaret, L., & Voisin, L. (1994) · annales de biologie animale biochimie biophysique · doi:10.1051/rnd:19940605 · Cited by 39 · see citing works
Introduction to Protein Summit 2007: Exploring the Impact of High-Quality Protein on Optimal Health
Rodriguez, N. R., & Garlick, P. J. (2008) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/87.5.1551s · Cited by 36 · see citing works
Sadiq, F., Hazlerigg, D. G., & Lomax, M. A. (2007) · BMC Molecular Biology · doi:10.1186/1471-2199-8-23 · Cited by 32 · see citing works
Jiang, W., Zhu, Z., & Thompson, H. J. (2008) · Molecular Carcinogenesis · doi:10.1002/mc.20425 · Cited by 31 · see citing works
Protein and Energy Interactions Throughout Life1
Young, V. R., YU, Y., & Fukagawa, N. K. (1991) · Acta Paediatrica · doi:10.1111/j.1651-2227.1991.tb18147.x · Cited by 27 · see citing works
Lundholm, K., Ekman, L. G., Karlberg, I. H., et al. (1980) · PubMed · Cited by 27 · see citing works
Regulation of different proteolytic pathways in skeletal muscle in fasting and diabetes mellitus.
Kettelhut, Í. D. C., Pepato, M. T., Migliorini, R. H., Medina, R., & Goldberg, A. L. (1994) · PubMed · Cited by 25 · see citing works
Effect of fasting and thyroidectomy on cysteine proteinase activities in liver and muscle
Belkhou, R., Béchet, D., Cherel, Y., Galluser, M., Ferrara, M. M., & Maho, Y. L. (1994) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(94)90115-5 · Cited by 20 · see citing works
Protein metabolism in obese subjects during a very-low-energy diet
Gougeon, R., Hoffer, L. J., Pencharz, P. B., & Eb, M. (1992) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/56.1.249s · Cited by 17 · see citing works
Pasiakos, S. M., Mettel, J. B., West, K. L., Lofgren, I. E., Fernández, M. L., Koo, S. I., & Rodriguez, N. R. (2008) · Metabolism · doi:10.1016/j.metabol.2007.11.006 · Cited by 14 · see citing works
Self-citationEffects of leucine on whole body leucine, valine, and threonine metabolism in humans
Hoffer, L. J., Taveroff, A., Robitaille, L., Hamadeh, M. J., & Mamer, O. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.272.6.e1037 · Cited by 8 · see citing works
Higher Protein during an Energy Deficit
Phillips, S. M. (2008) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181629a44 · Cited by 7 · see citing works
Parkes, S. C., Angelo, N., elcastro, McCargar, L. J., & McKenzie, D. C. (1998) · Canadian Journal of Applied Physiology · doi:10.1139/h98-016 · Cited by 2 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- [11]11. Gordon MM, Bopp MJ, Easter L, Miller GD, Lyles MF, Houston DK, Nicklas BJ, Kritchevsky SB. Effects of dietary protein on the composi- tion of weight loss in post-menopausal women. J Nutr Health Aging. 2008;12:505-9.
- [27]27. Rennie MJ, Tipton KD. Protein and amino acid metabolism during and after exercise and the effects of nutrition. Annu Rev Nutr. 2000;20:457-83.
- [29]29. Pasiakos SM, McClung JP. Supplemental dietary leucine and the skeletal muscle anabolic response to essential amino acids. Nutr Rev. 2011;69: 550-7.
Cited by
Sorted by citations
Pasiakos, S. M., McLellan, T. M., & Lieberman, H. R. (2015) · Sports Medicine · doi:10.1007/s40279-014-0242-2 · Cited by 202 · see citing works
Self-citationFinger, D., Goltz, F. R., Umpierre, D., Meyer, E., Rosa, L. H. T., & Schneider, C. D. (2015) · Sports Medicine · doi:10.1007/s40279-014-0269-4 · Cited by 185 · see citing works
Muscle-generated BDNF is a sexually dimorphic myokine that controls metabolic flexibility
Yang, X., Brobst, D., Chan, W. S., Tse, M. C. L., Herlea-Pana, O., Ahuja, P., Bi, X., Zaw, A. M., Kwong, Z. S. W., Jia, W.-H., et al. (2019) · Science Signaling · doi:10.1126/scisignal.aau1468 · Cited by 99 · see citing works
Carbone, J. W., McClung, J. P., & Pasiakos, S. M. (2019) · Advances in Nutrition · doi:10.1093/advances/nmy087 · Cited by 93 · see citing works
Self-citationWeight Management for Athletes and Active Individuals: A Brief Review
Manore, M. M. (2015) · Sports Medicine · doi:10.1007/s40279-015-0401-0 · Cited by 92 · see citing works
Coskun, T., Wu, Q., Schloot, N. C., Haupt, A., Milicevic, Z., Khouli, C., & Harris, C. (2025) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(25)00092-0 · Cited by 57 · see citing works
Carbone, J. W., Margolis, L. M., McClung, J. P., Cao, J. J., Murphy, N. E., Sauter, E. R., Combs, G. F., Young, A. J., & Pasiakos, S. M. (2013) · The FASEB Journal · doi:10.1096/fj.13-239228 · Cited by 43 · see citing works
Self-citationMetabolic Adaptations to Weight Loss: A Brief Review
Martínez-Gómez, M. G., & Roberts, B. M. (2022) · Journal of Strength & Conditioning Research · doi:10.1519/jsc.0000000000003991 · Cited by 32 · see citing works
Optimised Skeletal Muscle Mass as a Key Strategy for Obesity Management
Barber, T. M., Kabisch, S., Pfeiffer, A. F. H., & Weickert, M. O. (2025) · Metabolites · doi:10.3390/metabo15020085 · Cited by 19 · see citing works
“Broadly, there are two strategies: (i) lifestyle and (ii) novel pharmacotherapies.”
Biology or Behavior: Which Is the Strongest Contributor to Weight Gain?
Byrne, N. M., & Hills, A. P. (2013) · Current Obesity Reports · doi:10.1007/s13679-012-0040-9 · Cited by 13 · see citing works
- Authors
- Carbone, J. W., McClung, J. P., & Pasiakos, S. M.
- Affiliations
- Eastern Michigan University (US)
- U.S. Army Research Institute of Environmental Medicine (US)
- Corresponding author
- Pasiakos, Stefan M.
- Venue
- Advances in Nutrition
- Publisher
- Elsevier BV
- Published
- 2012-03
- Volume
- 3
- Issue
- 2
- Pages
- 119-126
- ISSN
- 2156-5376 (ISSN-L)
- 2161-8313
- PMC
- PMC3648712
- OpenAlex
- W2118596934
- Cited by
- 138
- References
- 74
- Citations by year
- 2026: 8 · 2025: 11 · 2024: 8 · 2023: 8 · 2022: 7 · 2021: 16 · 2020: 7 · 2019: 13 · 2018: 4 · 2017: 12 · 2016: 14 · 2015: 6 · 2014: 14 · 2013: 10
- FWCI
- 0.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Advances in Nutrition (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
- Keywords
- negative energy balance, skeletal muscle mass, dietary protein, muscle protein synthesis, muscle protein degradation, muscle anabolism, energy deprivation, muscle atrophy, protein turnover
- MeSH terms
- Animals, Basal Metabolism, Body Weight, Energy Intake, Dietary Proteins, Energy Metabolism, Female, Humans, Leucine, Male, Muscle Proteins, Nitrogen, Muscle, Skeletal, Nutrition Policy, Rats
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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.
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