Effects of energy deficit, dietary protein, and feeding on intracellular regulators of skeletal muscle proteolysis

Carbone, John W.; Margolis, Lee M.; McClung, James P.; Cao, Jay J.; Murphy, Nancy E.; Sauter, Edward R.; Combs, Gerald F.; Young, Andrew J.; Pasiakos, Stefan M.

doi:10.1096/fj.13-239228

Cited by 43Muscle metabolism and nutritionMuscle Physiology and DisordersNutrition and Health in Aging

Effects of energy deficit, dietary protein, and feeding on intracellular regulators of skeletal muscle proteolysis

Carbone, John W., Margolis, Lee M., McClung, James P., Cao, Jay J., Murphy, Nancy E., Sauter, Edward R., Combs, Gerald F., Young, Andrew J. +1 more·2013·The FASEB Journal

DOI 10.1096/fj.13-239228

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Abstract

This study was undertaken to characterize the ubiquitin proteasome system (UPS) response to varied dietary protein intake, energy deficit (ED), and consumption of a mixed meal. A randomized, controlled trial of 39 adults consuming protein at 0.8 (recommended dietary allowance [RDA]), 1.6 (2×‐RDA), or 2.4 (3×‐RDA) g · kg –1 ·· d –1 for 31 d. A 10‐d weight maintenance (WM) period was followed by 21 d of 40% ED. Ubiquitin (Ub)‐mediated proteolysis and associated gene expression were assessed in the postabsorptive (fasted) and postprandial (fed; 480 kcal, 20 g protein) states after WM and ED by using muscle biopsies, fluorescence‐based assays, immunoblot analysis, and real‐time qRT‐PCR In the assessment of UPS responses to varied protein intakes, ED, and feeding, the RDA, WM, and fasted measures served as appropriate controls. ED resulted in the up‐regulation of UPS‐associated gene expression, as mRNA expression of the atrogenes muscle RING finger‐1 (MuRF1) and atrogin‐1 were 1.2‐ and 1.3‐fold higher ( P <0.05) for ED than for WM. However, mixed‐meal consumption attenuated UPS‐mediated proteolysis, independent of energy status or dietary protein, as the activities of the 26S proteasome subunits β1, β2, and β5 were lower ( P <0.05) for fed than for fasted. Muscle protein ubiquitylation was also 45% lower ( P <0.05) for fed than for fasted, regardless of dietary protein and energy manipulations. Independent of habitual protein intake and despite increased MuRF1 and atrogin‐1 mRNA expression during ED, consuming a protein‐containing mixed meal attenuates Ub‐mediated proteolysis.—Carbone, J. W., Margolis, L. M., McClung, J. P., Cao, J. J., Murphy, N. E., Sauter, E. R., Combs, G. F., Jr., Young, A. J., Pasiakos, S. M., Effects of energy deficit, dietary protein, and feeding on intracellular regulators of skeletal muscle proteolysis. FASEB J. 27, 5104–5111 (2013). www.fasebj.org

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Consumption of a mixed meal attenuates ubiquitin-mediated proteolysis compared with fasting.
“Indeed, the consumption of a mixed meal attenuates ubiquitin‐mediated proteolysis when compared to fasted (Carbone et al., 2013).”
From The effect of acute sleep deprivation on skeletal muscle protein synthesis and the hormonal environment (2021) · cites this paper as Carbone et al., 2013

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Energy intake modulates intramuscular mTORC1 signaling and ubiquitin‐mediated proteolysis during energy deficit independent of dietary protein variations
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Ubiquitin‐proteasome‐dependent muscle proteolysis responds slowly to insulin release and refeeding in starved rats
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Authors: 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.
Affiliations: Eastern Michigan University (US)
U.S. Army Research Institute of Environmental Medicine (US)
Agricultural Research Service (US)
ORCID: Margolis, Lee M.
McClung, James P.
Cao, Jay J.
Murphy, Nancy E.
Sauter, Edward R.
Young, Andrew J.
Pasiakos, Stefan M.
Venue: The FASEB Journal
Publisher: Wiley
Published: 2013-08-21
Volume: 27
Issue: 12
Pages: 5104-5111
ISSN: 0892-6638 (ISSN-L)
1530-6860
DOI: 10.1096/fj.13-239228
OpenAlex: W2142038460
Cited by: 43
References: 38
Citations by year: 2026: 1 · 2025: 1 · 2024: 1 · 2023: 4 · 2022: 1 · 2021: 4 · 2020: 2 · 2019: 5 · 2018: 4 · 2017: 4 · 2016: 1 · 2015: 2 · 2014: 11 · 2013: 1
FWCI: 2.90
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The FASEB Journal (publishedVersion)
PubMed (publishedVersion)
Funders: Medical Research and Materiel Command
U.S. Department of Agriculture
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: skeletal muscle proteolysis, ubiquitin-proteasome system, negative energy balance, protein intake, mixed meal, muscle atrophy, MuRF1, atrogin-1, 26S proteasome, postprandial state, fasting, weight maintenance
MeSH terms: Adolescent, Adult, Body Weight, Dietary Proteins, Fasting, Female, Humans, Male, Muscle Proteins, Transcription, Genetic, Muscle, Skeletal, Ubiquitin, Caloric Restriction, SKP Cullin F-Box Protein Ligases, Proteasome Endopeptidase Complex, Ubiquitination, Proteolysis, Polycomb Repressive Complex 1, Recommended Dietary Allowances

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Effects of energy deficit, dietary protein, and feeding on intracellular regulators of skeletal muscle proteolysis

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