The impact of postexercise essential amino acid ingestion on the ubiquitin proteasome and autophagosomal-lysosomal systems in skeletal muscle of older men

Jared M. Dickinson, Paul T. Reidy, David M. Gundermann, Michael S. Borack, Dillon K. Walker, Andrew C. D'Lugos, Elena Volpi, Blake Rasmussen

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Essential amino acid (EAA) ingestion enhances postexercise muscle protein synthesis, and, in particular, the anabolic response of older adults appears sensitive to the quantity of ingested leucine. The effect of leucine ingestion on muscle breakdown following resistance exercise (RE) is less understood. The purpose of this study was to identify the impact of postexercise leucine ingestion on the ubiquitin proteasome and autophagosomal-lysosomal systems following acute RE in older men. Subjects (72 ± 2 yr) performed RE and 1 h postexercise ingested 10 g of EAA containing a leucine quantity similar to quality protein (control, 1.8 g leucine, n = 7) or enriched in leucine (leucine, 3.5 g leucine, n = 8). Stable isotope infusion and muscle biopsies (vastus lateralis) obtained at rest and 2, 5, and 24 h postexercise were used to examine protein content (Western blot), mRNA expression (RT-quantitative PCR), and muscle protein fractional breakdown rate (FBR). Muscle-specific RING finger 1 mRNA increased in both groups at 2 and 5 h (P < 0.05). LC3 mRNA increased, and the LC3BII-to-LC3BI ratio decreased at all postexercise time points in control (P < 0.05). Conversely, LC3 mRNA only increased at 2 h, and the LC3BII-to-LC3BI ratio only decreased at 2 and 5 h in leucine (P < 0.05). Tumor necrosis factor receptor-associated factor-6 mRNA increased (P < 0.05) in control at 5 h. FBR was not statistically different between groups or from basal 24 h postexercise (P > 0.05). These data indicate that ingesting a larger quantity of leucine following RE may further reduce postexercise skeletal muscle autophagy in older men; however, it does not appear to influence the acute postexercise elevation in markers of the ubiquitin proteasome system or the breakdown of intact proteins. NEW & NOTEWORTHY The impact of postexercise leucine ingestion on processes of skeletal muscle breakdown in older adults is not well understood. Additional postexercise leucine ingestion appears to further reduce autophagy, but it does not interfere with the increase in ubiquitin proteasome system markers or the breakdown of intact proteins in skeletal muscle of older men. Postexercise leucine ingestion may promote a healthier protein pool and favorable muscle adaptations in older adults through greater accretion of myofibrillar proteins.

Original languageEnglish (US)
Pages (from-to)620-630
Number of pages11
JournalJournal of Applied Physiology
Volume122
Issue number3
DOIs
StatePublished - Mar 1 2017

Fingerprint

Essential Amino Acids
Proteasome Endopeptidase Complex
Ubiquitin
Leucine
Skeletal Muscle
Eating
Exercise
Muscles
Proteins
Muscle Proteins
Autophagy
Messenger RNA
Quadriceps Muscle
Isotopes
Quality Control
Western Blotting

Keywords

  • Autophagy
  • Fractional breakdown rate
  • Leucine
  • Protein breakdown
  • Skeletal muscle

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

The impact of postexercise essential amino acid ingestion on the ubiquitin proteasome and autophagosomal-lysosomal systems in skeletal muscle of older men. / Dickinson, Jared M.; Reidy, Paul T.; Gundermann, David M.; Borack, Michael S.; Walker, Dillon K.; D'Lugos, Andrew C.; Volpi, Elena; Rasmussen, Blake.

In: Journal of Applied Physiology, Vol. 122, No. 3, 01.03.2017, p. 620-630.

Research output: Contribution to journalArticle

Dickinson, Jared M. ; Reidy, Paul T. ; Gundermann, David M. ; Borack, Michael S. ; Walker, Dillon K. ; D'Lugos, Andrew C. ; Volpi, Elena ; Rasmussen, Blake. / The impact of postexercise essential amino acid ingestion on the ubiquitin proteasome and autophagosomal-lysosomal systems in skeletal muscle of older men. In: Journal of Applied Physiology. 2017 ; Vol. 122, No. 3. pp. 620-630.
@article{952b4d82ffee4a31877a5b30fce6386b,
title = "The impact of postexercise essential amino acid ingestion on the ubiquitin proteasome and autophagosomal-lysosomal systems in skeletal muscle of older men",
abstract = "Essential amino acid (EAA) ingestion enhances postexercise muscle protein synthesis, and, in particular, the anabolic response of older adults appears sensitive to the quantity of ingested leucine. The effect of leucine ingestion on muscle breakdown following resistance exercise (RE) is less understood. The purpose of this study was to identify the impact of postexercise leucine ingestion on the ubiquitin proteasome and autophagosomal-lysosomal systems following acute RE in older men. Subjects (72 ± 2 yr) performed RE and 1 h postexercise ingested 10 g of EAA containing a leucine quantity similar to quality protein (control, 1.8 g leucine, n = 7) or enriched in leucine (leucine, 3.5 g leucine, n = 8). Stable isotope infusion and muscle biopsies (vastus lateralis) obtained at rest and 2, 5, and 24 h postexercise were used to examine protein content (Western blot), mRNA expression (RT-quantitative PCR), and muscle protein fractional breakdown rate (FBR). Muscle-specific RING finger 1 mRNA increased in both groups at 2 and 5 h (P < 0.05). LC3 mRNA increased, and the LC3BII-to-LC3BI ratio decreased at all postexercise time points in control (P < 0.05). Conversely, LC3 mRNA only increased at 2 h, and the LC3BII-to-LC3BI ratio only decreased at 2 and 5 h in leucine (P < 0.05). Tumor necrosis factor receptor-associated factor-6 mRNA increased (P < 0.05) in control at 5 h. FBR was not statistically different between groups or from basal 24 h postexercise (P > 0.05). These data indicate that ingesting a larger quantity of leucine following RE may further reduce postexercise skeletal muscle autophagy in older men; however, it does not appear to influence the acute postexercise elevation in markers of the ubiquitin proteasome system or the breakdown of intact proteins. NEW & NOTEWORTHY The impact of postexercise leucine ingestion on processes of skeletal muscle breakdown in older adults is not well understood. Additional postexercise leucine ingestion appears to further reduce autophagy, but it does not interfere with the increase in ubiquitin proteasome system markers or the breakdown of intact proteins in skeletal muscle of older men. Postexercise leucine ingestion may promote a healthier protein pool and favorable muscle adaptations in older adults through greater accretion of myofibrillar proteins.",
keywords = "Autophagy, Fractional breakdown rate, Leucine, Protein breakdown, Skeletal muscle",
author = "Dickinson, {Jared M.} and Reidy, {Paul T.} and Gundermann, {David M.} and Borack, {Michael S.} and Walker, {Dillon K.} and D'Lugos, {Andrew C.} and Elena Volpi and Blake Rasmussen",
year = "2017",
month = "3",
day = "1",
doi = "10.1152/japplphysiol.00632.2016",
language = "English (US)",
volume = "122",
pages = "620--630",
journal = "Journal of Applied Physiology",
issn = "8750-7587",
publisher = "American Physiological Society",
number = "3",

}

TY - JOUR

T1 - The impact of postexercise essential amino acid ingestion on the ubiquitin proteasome and autophagosomal-lysosomal systems in skeletal muscle of older men

AU - Dickinson, Jared M.

AU - Reidy, Paul T.

AU - Gundermann, David M.

AU - Borack, Michael S.

AU - Walker, Dillon K.

AU - D'Lugos, Andrew C.

AU - Volpi, Elena

AU - Rasmussen, Blake

PY - 2017/3/1

Y1 - 2017/3/1

N2 - Essential amino acid (EAA) ingestion enhances postexercise muscle protein synthesis, and, in particular, the anabolic response of older adults appears sensitive to the quantity of ingested leucine. The effect of leucine ingestion on muscle breakdown following resistance exercise (RE) is less understood. The purpose of this study was to identify the impact of postexercise leucine ingestion on the ubiquitin proteasome and autophagosomal-lysosomal systems following acute RE in older men. Subjects (72 ± 2 yr) performed RE and 1 h postexercise ingested 10 g of EAA containing a leucine quantity similar to quality protein (control, 1.8 g leucine, n = 7) or enriched in leucine (leucine, 3.5 g leucine, n = 8). Stable isotope infusion and muscle biopsies (vastus lateralis) obtained at rest and 2, 5, and 24 h postexercise were used to examine protein content (Western blot), mRNA expression (RT-quantitative PCR), and muscle protein fractional breakdown rate (FBR). Muscle-specific RING finger 1 mRNA increased in both groups at 2 and 5 h (P < 0.05). LC3 mRNA increased, and the LC3BII-to-LC3BI ratio decreased at all postexercise time points in control (P < 0.05). Conversely, LC3 mRNA only increased at 2 h, and the LC3BII-to-LC3BI ratio only decreased at 2 and 5 h in leucine (P < 0.05). Tumor necrosis factor receptor-associated factor-6 mRNA increased (P < 0.05) in control at 5 h. FBR was not statistically different between groups or from basal 24 h postexercise (P > 0.05). These data indicate that ingesting a larger quantity of leucine following RE may further reduce postexercise skeletal muscle autophagy in older men; however, it does not appear to influence the acute postexercise elevation in markers of the ubiquitin proteasome system or the breakdown of intact proteins. NEW & NOTEWORTHY The impact of postexercise leucine ingestion on processes of skeletal muscle breakdown in older adults is not well understood. Additional postexercise leucine ingestion appears to further reduce autophagy, but it does not interfere with the increase in ubiquitin proteasome system markers or the breakdown of intact proteins in skeletal muscle of older men. Postexercise leucine ingestion may promote a healthier protein pool and favorable muscle adaptations in older adults through greater accretion of myofibrillar proteins.

AB - Essential amino acid (EAA) ingestion enhances postexercise muscle protein synthesis, and, in particular, the anabolic response of older adults appears sensitive to the quantity of ingested leucine. The effect of leucine ingestion on muscle breakdown following resistance exercise (RE) is less understood. The purpose of this study was to identify the impact of postexercise leucine ingestion on the ubiquitin proteasome and autophagosomal-lysosomal systems following acute RE in older men. Subjects (72 ± 2 yr) performed RE and 1 h postexercise ingested 10 g of EAA containing a leucine quantity similar to quality protein (control, 1.8 g leucine, n = 7) or enriched in leucine (leucine, 3.5 g leucine, n = 8). Stable isotope infusion and muscle biopsies (vastus lateralis) obtained at rest and 2, 5, and 24 h postexercise were used to examine protein content (Western blot), mRNA expression (RT-quantitative PCR), and muscle protein fractional breakdown rate (FBR). Muscle-specific RING finger 1 mRNA increased in both groups at 2 and 5 h (P < 0.05). LC3 mRNA increased, and the LC3BII-to-LC3BI ratio decreased at all postexercise time points in control (P < 0.05). Conversely, LC3 mRNA only increased at 2 h, and the LC3BII-to-LC3BI ratio only decreased at 2 and 5 h in leucine (P < 0.05). Tumor necrosis factor receptor-associated factor-6 mRNA increased (P < 0.05) in control at 5 h. FBR was not statistically different between groups or from basal 24 h postexercise (P > 0.05). These data indicate that ingesting a larger quantity of leucine following RE may further reduce postexercise skeletal muscle autophagy in older men; however, it does not appear to influence the acute postexercise elevation in markers of the ubiquitin proteasome system or the breakdown of intact proteins. NEW & NOTEWORTHY The impact of postexercise leucine ingestion on processes of skeletal muscle breakdown in older adults is not well understood. Additional postexercise leucine ingestion appears to further reduce autophagy, but it does not interfere with the increase in ubiquitin proteasome system markers or the breakdown of intact proteins in skeletal muscle of older men. Postexercise leucine ingestion may promote a healthier protein pool and favorable muscle adaptations in older adults through greater accretion of myofibrillar proteins.

KW - Autophagy

KW - Fractional breakdown rate

KW - Leucine

KW - Protein breakdown

KW - Skeletal muscle

UR - http://www.scopus.com/inward/record.url?scp=85014791501&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85014791501&partnerID=8YFLogxK

U2 - 10.1152/japplphysiol.00632.2016

DO - 10.1152/japplphysiol.00632.2016

M3 - Article

VL - 122

SP - 620

EP - 630

JO - Journal of Applied Physiology

JF - Journal of Applied Physiology

SN - 8750-7587

IS - 3

ER -