Recent Advances in the Characterization of Skeletal Muscle and Whole-Body Protein Responses to Dietary Protein and Exercise during Negative Energy Balance

Carbone, John W; McClung, James P; Pasiakos, Stefan M

doi:10.1093/advances/nmy087

Cited by 93Muscle metabolism and nutritionMuscle Physiology and DisordersNutrition and Health in Aging

Recent Advances in the Characterization of Skeletal Muscle and Whole-Body Protein Responses to Dietary Protein and Exercise during Negative Energy Balance

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Carbone, John W, McClung, James P, Pasiakos, Stefan M·2019·Advances in Nutrition

DOI 10.1093/advances/nmy087PMC PMC6370268

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Abstract

In a review published in 2012, we concluded that higher-protein diets preserve muscle mass during energy deficit via stimulated mammalian target of rapamycin complex 1 signaling, coincident increased muscle protein synthesis (PS), inhibited ubiquitin-mediated proteolysis, and suppressed muscle protein breakdown (PB). Since then, there have been significant advances in understanding the fundamental effects of higher-protein diets, with or without exercise training, on muscle and whole-body protein homeostasis during negative energy balance. Therefore, an update on the evolution of this field of research is warranted to better inform recommendations on best practices for healthy weight loss and muscle preservation. We will review the most recent studies examining the effects of higher-protein diets and negative energy balance on body composition, muscle PS, muscle PB, associated intracellular regulatory pathway activities, and whole-body protein homeostasis. In addition to critically analyzing contemporary findings, knowledge gaps and opportunities for continued research will be identified. Overall, the newest research confirms that consuming higher-protein diets, particularly when coupled with resistance exercise, preserves muscle mass and maintains whole-body protein homeostasis during moderate energy deficits (i.e., normal weight loss). However, these newer findings also indicate that as the magnitude of energy deficit increases, the efficacy of higher-protein diets for mitigating losses of fat-free mass is diminished. Further, recent results suggest that alterations in muscle PS, more so than muscle PB, may be primarily responsible for changes in muscle mass that occur in response to negative energy balance.

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Higher protein diets (>2.0 g·kg−1·day−1), coupled with heavy resistance training, are important for maintaining lean mass and resting energy expenditure under periods of intentional and unintentional caloric restriction.
“higher protein diets (>2.0 g·kg−1·day−1), coupled with heavy resistance training, have been shown to be important for maintaining lean mass and resting energy expenditure under periods of intentional and unintentional caloric restriction [231,232]”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [231]
The Current Status of Knowledge and Conclusions (pages unavailable) support higher protein intake combined with resistance exercise for preserving or gaining lean mass during moderate energy deficits; the review describes a 2.4 g·kg−1·day−1 intervention. They do not establish that intake above 2.0 g·kg−1·day−1 is necessary, or that the combination maintains resting energy expenditure. The Conclusions also caution that higher protein may lose its muscle-sparing effect in more severe deficits, so the claim is too broad across periods of caloric restriction. (LLM, conf=0.90)
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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: Carbone, John W
ORCID: McClung, James P
Pasiakos, Stefan M
Venue: Advances in Nutrition
Publisher: Elsevier BV
Published: 2019-01
Volume: 10
Issue: 1
Pages: 70-79
ISSN: 2156-5376 (ISSN-L)
2161-8313
DOI: 10.1093/advances/nmy087
PMC: PMC6370268
OpenAlex: W2906807697
Cited by: 93
References: 43
Citations by year: 2026: 7 · 2025: 12 · 2024: 13 · 2023: 8 · 2022: 16 · 2021: 15 · 2020: 11 · 2019: 11
FWCI: 5.12
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 1122 d)
Locations: Advances in Nutrition (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: US Army Medical Research and Materiel Command
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: high-protein diet, negative energy balance, muscle protein synthesis, muscle protein degradation, resistance training, weight loss, mTOR signaling, ubiquitin-mediated proteolysis, body composition
MeSH terms: Diet, High-Protein, Body Composition, Dietary Proteins, Energy Metabolism, Humans, Muscle Proteins, Weight Loss, Exercise, Muscle, Skeletal

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Recent Advances in the Characterization of Skeletal Muscle and Whole-Body Protein Responses to Dietary Protein and Exercise during Negative Energy Balance

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