Student or educator? Sign up with your school email and get 6 months of Pro free.
Cited by 107

The DOI matches its Crossref record; 39 of the 39 references it cites were found in a registry or an index.

Anabolic Resistance of Muscle Protein Turnover Comes in Various Shapes and Sizes

Paulussen, Kevin J. M., McKenna, Colleen F., Beals, Joseph W., Wilund, Kenneth R., Salvador, Amadeo F., Burd, Nicholas A.·2021·Frontiers in Nutrition

Abstract

Anabolic resistance is defined by a blunted stimulation of muscle protein synthesis rates (MPS) to common anabolic stimuli in skeletal muscle tissue such as dietary protein and exercise. Generally, MPS is the target of most exercise and feeding interventions as muscle protein breakdown rates seem to be less responsive to these stimuli. Ultimately, the blunted responsiveness of MPS to dietary protein and exercise underpins the loss of the amount and quality of skeletal muscle mass leading to decrements in physical performance in these populations. The increase of both habitual physical activity (including structured exercise that targets general fitness characteristics) and protein dense food ingestion are frontline strategies utilized to support muscle mass, performance, and health. In this paper, we discuss anabolic resistance as a common denominator underpinning muscle mass loss with aging, obesity, and other disease states. Namely, we discuss the fact that anabolic resistance exists as a dimmer switch, capable of varying from higher to lower levels of resistance, to the main anabolic stimuli of feeding and exercise depending on the population. Moreover, we review the evidence on whether increased physical activity and targeted exercise can be leveraged to restore the sensitivity of skeletal muscle tissue to dietary amino acids regardless of the population.

Overview

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fnut.2021.615849

Cites

39 of 39 references verified0 citation errors · 0 not checkable

Statistics

Verification

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.

A few free checks a day · papers already verified open instantly · results are public

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.

Citations

Cites

Research works printed but not linked: 81

  1. Janssen, 2011, The epidemiology of sarcopenia, Clin Geriatr Med, 27, 355, 10.1016/j.cger.2011.03.004 · DOI
  2. Beals, 2018, Altered anabolic signalling and reduced stimulation of myofibrillar protein synthesis after feeding and resistance exercise in people with obesity, J Physiol, 596, 5119, 10.1113/JP276210 · DOI
  3. Beals, 2016, Anabolic sensitivity of postprandial muscle protein synthesis to the ingestion of a protein-dense food is reduced in overweight and obese young adults, Am J Clin Nutr, 104, 1014, 10.3945/ajcn.116.130385 · DOI · Paper page
  4. van Vliet, 2018, Dysregulated handling of dietary protein and muscle protein synthesis after mixed-meal ingestion in maintenance hemodialysis patients, Kidney Int Rep, 3, 1403, 10.1016/j.ekir.2018.08.001 · DOI
  5. Wall, 2016, Short-term muscle disuse lowers myofibrillar protein synthesis rates and induces anabolic resistance to protein ingestion, Am J Physiol Endocrinol Metab, 310, E137, 10.1152/ajpendo.00227.2015 · DOI · Paper page
  6. Drummond, 2012, Bed rest impairs skeletal muscle amino acid transporter expression, mTORC1 signaling, and protein synthesis in response to essential amino acids in older adults, Am J Physiol Endocrinol Metab, 302, E1113, 10.1152/ajpendo.00603.2011 · DOI · Paper page
  7. Burd, 2019, Dietary protein quantity, quality, and exercise are key to healthy living: a muscle-centric perspective across the lifespan, Front Nutr, 6, 83, 10.3389/fnut.2019.00083 · DOI
  8. Moore, 2014, Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men, J Gerontol Series A, 10.1093/gerona/glu103 · DOI · Paper page
  9. Pupim, 2006, Intradialytic oral nutrition improves protein homeostasis in chronic hemodialysis patients with deranged nutritional status, J Am Soc Nephrol, 17, 3149, 10.1681/ASN.2006040413 · DOI
  10. Wall, 2013, Disuse impairs the muscle protein synthetic response to protein ingestion in healthy men, J Clin Endocrinol Metab, 98, 4872, 10.1210/jc.2013-2098 · DOI
  11. Raj, 2007, Amino acid repletion does not decrease muscle protein catabolism during hemodialysis, Am J Physiol Endocrinol Metab, 292, E1534, 10.1152/ajpendo.00599.2006 · DOI
  12. Raj, 2004, Protein turnover and amino acid transport kinetics in end-stage renal disease, Am J Physiol Endocrinol Metab, 286, E136, 10.1152/ajpendo.00352.2003 · DOI
  13. Churchward-Venne, 2020, Dose-response effects of dietary protein on muscle protein synthesis during recovery from endurance exercise in young men: a double-blind randomized trial. The American, J Clin Nutr, 112, 303, 10.1093/ajcn/nqaa073 · DOI · Paper page
  14. Abou Sawan, 2018, Translocation and protein complex co-localization of mTOR is associated with postprandial myofibrillar protein synthesis at rest and after endurance exercise, Physiol Rep, 6, e13628, 10.14814/phy2.13628 · DOI
  15. Pennings, 2011, Exercising before protein intake allows for greater use of dietary protein-derived amino acids for de novo muscle protein synthesis in both young and elderly men, Am J Clin Nutr, 93, 322, 10.3945/ajcn.2010.29649 · DOI · Paper page
  16. Biolo, 1997, An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein, Am J Physiol Endocrinol Metab, 273, E122, 10.1152/ajpendo.1997.273.1.E122 · DOI · Paper page
  17. Koopman, 2005, Combined ingestion of protein and free leucine with carbohydrate increases postexercise muscle protein synthesis in vivo in male subjects, Am J Physiol Endocrinol Metab, 288, E645, 10.1152/ajpendo.00413.2004 · DOI · Paper page
  18. West, 2011, Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise, Am J Clin Nutr, 94, 795, 10.3945/ajcn.111.013722 · DOI · Paper page
  19. Kimball, 2016, Leucine induced dephosphorylation of Sestrin2 promotes mTORC1 activation, Cell Signal, 28, 896, 10.1016/j.cellsig.2016.03.008 · DOI · Paper page
  20. van Vliet, 2018, The muscle anabolic effect of protein ingestion during a hyperinsulinaemic euglycaemic clamp in middle-aged women is not caused by leucine alone, J Physiol, 596, 4681, 10.1113/JP276504 · DOI
  21. Wilkinson, 2013, Effects of leucine and its metabolite β-hydroxy-β-methylbutyrate on human skeletal muscle protein metabolism, J Physiol, 591, 2911, 10.1113/jphysiol.2013.253203 · DOI · Paper page
  22. Kobayashi, 2006, Modulations of muscle protein metabolism by branched-chain amino acids in normal and muscle-atrophying rats, J Nutr, 136, 234S, 10.1093/jn/136.1.234S · DOI
  23. Burd, 2019, Food-first approach to enhance the regulation of post-exercise skeletal muscle protein synthesis and remodeling, Sports Med, 49, 59, 10.1007/s40279-018-1009-y · DOI · Paper page
  24. Abou Sawan, 2018, Whole egg, but not egg white, ingestion induces mTOR colocalization with the lysosome after resistance exercise, Am J Physiol Cell Physiol, 315, C537, 10.1152/ajpcell.00225.2018 · DOI · Paper page
  25. Sheffield-Moore, 2004, Postexercise protein metabolism in older and younger men following moderate-intensity aerobic exercise, Am J Physiol Endocrinol Metab, 287, E513, 10.1152/ajpendo.00334.2003 · DOI · Paper page
  26. Børsheim, 2002, Essential amino acids and muscle protein recovery from resistance exercise, Am J Physiol Endocrinol Metab, 283, E648, 10.1152/ajpendo.00466.2001 · DOI · Paper page
  27. Stokes, 2020, Molecular transducers of human skeletal muscle remodeling under different loading states, Cell Rep, 32, 107980, 10.1016/j.celrep.2020.107980 · DOI
  28. Gillen, 2019, Low-carbohydrate training increases protein requirements of endurance athletes, Med Sci Sports Exerc, 51, 2294, 10.1249/MSS.0000000000002036 · DOI · Paper page
  29. Gorissen, 2017, Habituation to low or high protein intake does not modulate basal or postprandial muscle protein synthesis rates: a randomized trial, Am J Clin Nutr, 105, 332, 10.3945/ajcn.115.129924 · DOI · Paper page
  30. Tinline-Goodfellow, 2020, An acute reduction in habitual protein intake attenuates post exercise anabolism and may bias oxidation-derived protein requirements in resistance trained men, Front Nutr, 7, 55, 10.3389/fnut.2020.00055 · DOI
  31. Bohé, 2001, Latency and duration of stimulation of human muscle protein synthesis during continuous infusion of amino acids, J Physiol, 532, 575, 10.1111/j.1469-7793.2001.0575f.x · DOI
  32. Markofski, 2015, Effect of age on basal muscle protein synthesis and mTORC1 signaling in a large cohort of young and older men and women, Exp Gerontol, 65, 1, 10.1016/j.exger.2015.02.015 · DOI · Paper page
  33. Katsanos, 2005, Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids, Am J Clin Nutr, 82, 1065, 10.1093/ajcn/82.5.1065 · DOI · Paper page
  34. Smith, 2011, Dietary omega-3 fatty acid supplementation increases the rate of muscle protein synthesis in older adults: a randomized controlled trial, Am J Clin Nutr, 93, 402, 10.3945/ajcn.110.005611 · DOI · Paper page
  35. Bell, 2017, A whey protein-based multi-ingredient nutritional supplement stimulates gains in lean body mass and strength in healthy older men: a randomized controlled trial, PLoS ONE, 12, e0181387, 10.1371/journal.pone.0181387 · DOI · Paper page
  36. Kouw, 2017, Protein ingestion before sleep increases overnight muscle protein synthesis rates in healthy older men: a randomized controlled trial, J Nutr, 147, 2252, 10.3945/jn.117.254532 · DOI · Paper page
  37. Houston, 2008, Dietary protein intake is associated with lean mass change in older, community-dwelling adults: the Health, Aging, and Body Composition (Health ABC) Study, Am J Clin Nutr, 87, 150, 10.1093/ajcn/87.1.150 · DOI · Paper page
  38. Szwiega, 2020, Dietary leucine requirement of older men and women is higher than current recommendations, Am J Clin Nutr, 113, 410, 10.1093/ajcn/nqaa323 · DOI · Paper page
  39. Durham, 2010, Age-related anabolic resistance after endurance-type exercise in healthy humans, FASEB J, 24, 4117, 10.1096/fj.09-150177 · DOI
  40. Snijders, 2017, Muscle fibre capillarization is a critical factor in muscle fibre hypertrophy during resistance exercise training in older men, J Cachexia Sarcopenia Muscle, 8, 267, 10.1002/jcsm.12137 · DOI
  41. Kumar, 2012, Muscle protein synthetic responses to exercise: effects of age, volume, and intensity, J Gerontol Ser A Biomed Sci Med Sci, 67, 1170, 10.1093/gerona/gls141 · DOI
  42. Breen, 2013, Two weeks of reduced activity decreases leg lean mass and induces “anabolic resistance” of myofibrillar protein synthesis in healthy elderly, J Clin Endocrinol Metab, 98, 2604, 10.1210/jc.2013-1502 · DOI · Paper page
  43. Suetta, 2013, Ageing is associated with diminished muscle re-growth and myogenic precursor cell expansion early after immobility-induced atrophy in human skeletal muscle, J Physiol, 591, 3789, 10.1113/jphysiol.2013.257121 · DOI
  44. Guillet, 2009, Changes in basal and insulin and amino acid response of whole body and skeletal muscle proteins in obese men, J Clin Endocrinol Metab, 94, 3044, 10.1210/jc.2008-2216 · DOI
  45. Tran, 2018, Lower fasted-state but greater increase in muscle protein synthesis in response to elevated plasma amino acids in obesity, Obesity, 26, 1179, 10.1002/oby.22213 · DOI
  46. Chevalier, 2015, Protein and glucose metabolic responses to hyperinsulinemia, hyperglycemia, and hyperaminoacidemia in obese men, Obesity, 23, 351, 10.1002/oby.20943 · DOI
  47. Kouw, 2019, Basal and postprandial myofibrillar protein synthesis rates do not differ between lean and obese middle-aged men, J Nutr, 149, 1533, 10.1093/jn/nxz104 · DOI
  48. Williamson, 2015, Aberrant REDD1-mTORC1 responses to insulin in skeletal muscle from Type 2 diabetics, Am J Physiol Regul Integrative Compar Physiol, 309, R855, 10.1152/ajpregu.00285.2015 · DOI
  49. Bosy-Westphal, 2009, Contribution of individual organ mass loss to weight loss–associated decline in resting energy expenditure, Am J Clin Nutr, 90, 993, 10.3945/ajcn.2008.27402 · DOI · Paper page
  50. Paris, 2016, Increasing energy flux to decrease the biological drive toward weight regain after weight loss–a proof-of-concept pilot study, Clin Nutr, 11, e12, 10.1016/j.clnesp.2015.11.005 · DOI
  51. Hernández-Reyes, 2019, Changes in body composition with a hypocaloric diet combined with sedentary, moderate and high-intense physical activity: a randomized controlled trial, BMC Women's Health, 19, 167, 10.1186/s12905-019-0864-5 · DOI
  52. Wilkinson, 2008, Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle, J Physiol, 586, 3701, 10.1113/jphysiol.2008.153916 · DOI · Paper page
  53. Hulston, 2018, Resistance exercise stimulates mixed muscle protein synthesis in lean and obese young adults, Physiol Rep, 6, e13799, 10.14814/phy2.13799 · DOI
  54. Smith, 2016, High-protein intake during weight loss therapy eliminates the weight-loss-induced improvement in insulin action in obese postmenopausal women, Cell Rep, 17, 849, 10.1016/j.celrep.2016.09.047 · DOI · Paper page
  55. Anker, 2014, Muscle wasting disease: a proposal for a new disease classification, J Cachexia Sarcopenia Muscle., 5, 1, 10.1007/s13539-014-0135-0 · DOI
  56. Fearon, 2011, Definition and classification of cancer cachexia: an international consensus, Lancet Oncol, 12, 489, 10.1016/S1470-2045(10)70218-7 · DOI · Paper page
  57. Emery, 1984, Protein synthesis in muscle measured in vivo in cachectic patients with cancer, Br Med J., 289, 584, 10.1136/bmj.289.6445.584 · DOI
  58. Williams, 2012, Effect of tumor burden and subsequent surgical resection on skeletal muscle mass and protein turnover in colorectal cancer patients, Am J Clin Nutr, 96, 1064, 10.3945/ajcn.112.045708 · DOI
  59. Deutz, 2011, Muscle protein synthesis in cancer patients can be stimulated with a specially formulated medical food, Clin Nutr, 30, 759, 10.1016/j.clnu.2011.05.008 · DOI
  60. Hendriks, 2018, Amino acid loss during hemodialysis in end-stage renal disease patients, Clin Nutr, 37, S96, 10.1016/j.clnu.2018.06.1372 · DOI
  61. Horstman, 2016, Is cancer cachexia attributed to impairments in basal or postprandial muscle protein metabolism?, Nutrients, 8, 499, 10.3390/nu8080499 · DOI
  62. Raj, 2004, Coordinated increase in albumin, fibrinogen, and muscle protein synthesis during hemodialysis: role of cytokines, Am J Physiol Endocrinol Metab, 286, E658, 10.1152/ajpendo.00444.2003 · DOI
  63. Pupim, 2002, Intradialytic parenteral nutrition improves protein and energy homeostasis in chronic hemodialysis patients, J Clin Invest, 110, 483, 10.1172/JCI0215449 · DOI
  64. Veeneman, 2003, Protein intake during hemodialysis maintains a positive whole body protein balance in chronic hemodialysis patients, Am J Physiol Endocrinol Metab, 284, E954, 10.1152/ajpendo.00264.2002 · DOI
  65. Weiner, 2014, Oral intradialytic nutritional supplement use and mortality in hemodialysis patients, Am J Kidney Dis, 63, 276, 10.1053/j.ajkd.2013.08.007 · DOI
  66. Lacson, 2012, Outcomes associated with intradialytic oral nutritional supplements in patients undergoing maintenance hemodialysis: a quality improvement report, Am J Kidney Dis, 60, 591, 10.1053/j.ajkd.2012.04.019 · DOI · Paper page
  67. Benner, 2018, Effects of oral nutritional supplements on mortality, missed dialysis treatments, and nutritional markers in hemodialysis patients, J Ren Nutr, 28, 191, 10.1053/j.jrn.2017.10.002 · DOI
  68. Caglar, 2002, Therapeutic effects of oral nutritional supplementation during hemodialysis, Kidney Int, 62, 1054, 10.1046/j.1523-1755.2002.00530.x · DOI
  69. McKenna, 2019, Exercising to offset muscle mass loss in hemodialysis patients: the disconnect between intention and intervention, Semin Dial, 32, 379, 10.1111/sdi.12805 · DOI
  70. Wilund, 2020, A critical review of exercise training in hemodialysis patients: personalized activity prescriptions are needed, Exerc Sport Sci Rev, 48, 28, 10.1249/JES.0000000000000209 · DOI
  71. Draicchio, 2020, Integrin-associated ILK and PINCH1 protein content are reduced in skeletal muscle of maintenance haemodialysis patients, J Physiol, 598, 5701, 10.1113/JP280441 · DOI
  72. Wilund, 2019, A global approach to increasing physical activity and exercise in kidney care: the International Society of Renal Nutrition and Metabolism Global Renal Exercise Group, J Renal Nutr, 29, 467, 10.1053/j.jrn.2019.08.004 · DOI
  73. Ferrando, 1996, Prolonged bed rest decreases skeletal muscle and whole body protein synthesis, Am J Physiol, 270, E627, 10.1152/ajpendo.1996.270.4.E627 · DOI · Paper page
  74. Wall, 2014, Substantial skeletal muscle loss occurs during only 5 days of disuse, Acta Physiol, 210, 600, 10.1111/apha.12190 · DOI · Paper page
  75. Kilroe, 2020, Short-term muscle disuse induces a rapid and sustained decline in daily myofibrillar protein synthesis rates, Am J Physiol Endocrinol Metab, 318, E117, 10.1152/ajpendo.00360.2019 · DOI · Paper page
  76. de Rooij, 2016, Physical activity and sedentary behavior in metabolically healthy versus unhealthy obese and non-obese individuals–the Maastricht study, PLoS ONE, 11, e0154358, 10.1371/journal.pone.0154358 · DOI
  77. Tudor-Locke, 2011, How many steps/day are enough? For older adults and special populations, Int J Behav Nutr Phys Activity, 8, 80, 10.1186/1479-5868-8-80 · DOI · Paper page
  78. Shad, 2019, One week of step reduction lowers myofibrillar protein synthesis rates in young men, Med Sci Sports Exer, 2019, 2125, 10.1249/MSS.0000000000002034 · DOI
  79. Ekelund, 2016, Does physical activity attenuate, or even eliminate, the detrimental association of sitting time with mortality? A harmonised meta-analysis of data from more than 1 million men and women, Lancet, 388, 1302, 10.1016/S0140-6736(16)30370-1 · DOI · Paper page
  80. Gillen, 2020, Interrupting prolonged sitting with repeated chair stands or short walks reduces postprandial insulinemia in healthy adults, J Appl Physiol., 130, 104, 10.1152/japplphysiol.00796.2020 · DOI
  81. Jeong, 2019, Results from the randomized controlled IHOPE trial suggest no effects of oral protein supplementation and exercise training on physical function in hemodialysis patients, Kidney Int, 96, 777, 10.1016/j.kint.2019.03.018 · DOI

Cited by

See all 107

Metadata

Authors
Paulussen, K. J. M., McKenna, C. F., Beals, J. W., Wilund, K. R., Salvador, A. F., & Burd, N. A.
Venue
Frontiers in Nutrition
Published
2021-05-05
Volume
8
ISSN
2296-861X
Cited by
107
References
39

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

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.