Lifelong dietary protein restriction accelerates skeletal muscle loss and reduces muscle fibre size by impairing proteostasis and mitochondrial homeostasis

The early life environment significantly affects the development of age-related skeletal muscle disorders. However, the long-term effects of lactational protein restriction on skeletal muscle are still poorly defined. Our study revealed that male mice nursed by dams fed a low-protein diet during lac...

Full description

Bibliographic Details
Main Authors: Ufuk Ersoy, Ioannis Kanakis, Moussira Alameddine, Gibran Pedraza-Vazquez, Susan E. Ozanne, Mandy Jayne Peffers, Malcolm J. Jackson, Katarzyna Goljanek-Whysall, Aphrodite Vasilaki
Format: Article
Language:English
Published: Elsevier 2024-02-01
Series:Redox Biology
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213231723003816
_version_ 1797400844585402368
author Ufuk Ersoy
Ioannis Kanakis
Moussira Alameddine
Gibran Pedraza-Vazquez
Susan E. Ozanne
Mandy Jayne Peffers
Malcolm J. Jackson
Katarzyna Goljanek-Whysall
Aphrodite Vasilaki
author_facet Ufuk Ersoy
Ioannis Kanakis
Moussira Alameddine
Gibran Pedraza-Vazquez
Susan E. Ozanne
Mandy Jayne Peffers
Malcolm J. Jackson
Katarzyna Goljanek-Whysall
Aphrodite Vasilaki
author_sort Ufuk Ersoy
collection DOAJ
description The early life environment significantly affects the development of age-related skeletal muscle disorders. However, the long-term effects of lactational protein restriction on skeletal muscle are still poorly defined. Our study revealed that male mice nursed by dams fed a low-protein diet during lactation exhibited skeletal muscle growth restriction. This was associated with a dysregulation in the expression levels of genes related to the ribosome, mitochondria and skeletal muscle development. We reported that lifelong protein restriction accelerated loss of type-IIa muscle fibres and reduced muscle fibre size by impairing mitochondrial homeostasis and proteostasis at 18 months of age. However, feeding a normal-protein diet following lactational protein restriction prevented accelerated fibre loss and fibre size reduction in later life. These findings provide novel insight into the mechanisms by which lactational protein restriction hinders skeletal muscle growth and includes evidence that lifelong dietary protein restriction accelerated skeletal muscle loss in later life.
first_indexed 2024-03-09T02:01:30Z
format Article
id doaj.art-25f44b1fbbb048248ed57023c8688ef9
institution Directory Open Access Journal
issn 2213-2317
language English
last_indexed 2024-03-09T02:01:30Z
publishDate 2024-02-01
publisher Elsevier
record_format Article
series Redox Biology
spelling doaj.art-25f44b1fbbb048248ed57023c8688ef92023-12-08T04:45:22ZengElsevierRedox Biology2213-23172024-02-0169102980Lifelong dietary protein restriction accelerates skeletal muscle loss and reduces muscle fibre size by impairing proteostasis and mitochondrial homeostasisUfuk Ersoy0Ioannis Kanakis1Moussira Alameddine2Gibran Pedraza-Vazquez3Susan E. Ozanne4Mandy Jayne Peffers5Malcolm J. Jackson6Katarzyna Goljanek-Whysall7Aphrodite Vasilaki8Department of Musculoskeletal & Ageing Science, Institute of Life Course & Medical Sciences (ILCaMS), The MRC - Versus Arthritis Centre for Integrated Research Into Musculoskeletal Ageing (CIMA), University of Liverpool, Liverpool, UKDepartment of Musculoskeletal & Ageing Science, Institute of Life Course & Medical Sciences (ILCaMS), The MRC - Versus Arthritis Centre for Integrated Research Into Musculoskeletal Ageing (CIMA), University of Liverpool, Liverpool, UK; Chester Medical School, Faculty of Medicine and Life Sciences, University of Chester, Chester, UKDepartment of Musculoskeletal & Ageing Science, Institute of Life Course & Medical Sciences (ILCaMS), The MRC - Versus Arthritis Centre for Integrated Research Into Musculoskeletal Ageing (CIMA), University of Liverpool, Liverpool, UKDepartment of Physiology, School of Medicine and REMEDI, CMNHS, University of Galway, Galway, IrelandMRC Metabolic Diseases Unit, Wellcome Trust-MRC Institute of Metabolic Science, Addenbrooke's Treatment Centre, Addenbrooke's Hospital, University of Cambridge Metabolic Research Laboratories, Cambridge, UKDepartment of Musculoskeletal & Ageing Science, Institute of Life Course & Medical Sciences (ILCaMS), The MRC - Versus Arthritis Centre for Integrated Research Into Musculoskeletal Ageing (CIMA), University of Liverpool, Liverpool, UKDepartment of Musculoskeletal & Ageing Science, Institute of Life Course & Medical Sciences (ILCaMS), The MRC - Versus Arthritis Centre for Integrated Research Into Musculoskeletal Ageing (CIMA), University of Liverpool, Liverpool, UKDepartment of Musculoskeletal & Ageing Science, Institute of Life Course & Medical Sciences (ILCaMS), The MRC - Versus Arthritis Centre for Integrated Research Into Musculoskeletal Ageing (CIMA), University of Liverpool, Liverpool, UK; Department of Physiology, School of Medicine and REMEDI, CMNHS, University of Galway, Galway, IrelandDepartment of Musculoskeletal & Ageing Science, Institute of Life Course & Medical Sciences (ILCaMS), The MRC - Versus Arthritis Centre for Integrated Research Into Musculoskeletal Ageing (CIMA), University of Liverpool, Liverpool, UK; Corresponding author. Institute of Life Course and Medical Sciences, William Henry Duncan Building, 6 West Derby Street, Liverpool, L7 8TX, UK.The early life environment significantly affects the development of age-related skeletal muscle disorders. However, the long-term effects of lactational protein restriction on skeletal muscle are still poorly defined. Our study revealed that male mice nursed by dams fed a low-protein diet during lactation exhibited skeletal muscle growth restriction. This was associated with a dysregulation in the expression levels of genes related to the ribosome, mitochondria and skeletal muscle development. We reported that lifelong protein restriction accelerated loss of type-IIa muscle fibres and reduced muscle fibre size by impairing mitochondrial homeostasis and proteostasis at 18 months of age. However, feeding a normal-protein diet following lactational protein restriction prevented accelerated fibre loss and fibre size reduction in later life. These findings provide novel insight into the mechanisms by which lactational protein restriction hinders skeletal muscle growth and includes evidence that lifelong dietary protein restriction accelerated skeletal muscle loss in later life.http://www.sciencedirect.com/science/article/pii/S2213231723003816Skeletal muscleSarcopeniaMaternal nutritionProtein restrictionProteostasisMitochondrial homeostasis
spellingShingle Ufuk Ersoy
Ioannis Kanakis
Moussira Alameddine
Gibran Pedraza-Vazquez
Susan E. Ozanne
Mandy Jayne Peffers
Malcolm J. Jackson
Katarzyna Goljanek-Whysall
Aphrodite Vasilaki
Lifelong dietary protein restriction accelerates skeletal muscle loss and reduces muscle fibre size by impairing proteostasis and mitochondrial homeostasis
Redox Biology
Skeletal muscle
Sarcopenia
Maternal nutrition
Protein restriction
Proteostasis
Mitochondrial homeostasis
title Lifelong dietary protein restriction accelerates skeletal muscle loss and reduces muscle fibre size by impairing proteostasis and mitochondrial homeostasis
title_full Lifelong dietary protein restriction accelerates skeletal muscle loss and reduces muscle fibre size by impairing proteostasis and mitochondrial homeostasis
title_fullStr Lifelong dietary protein restriction accelerates skeletal muscle loss and reduces muscle fibre size by impairing proteostasis and mitochondrial homeostasis
title_full_unstemmed Lifelong dietary protein restriction accelerates skeletal muscle loss and reduces muscle fibre size by impairing proteostasis and mitochondrial homeostasis
title_short Lifelong dietary protein restriction accelerates skeletal muscle loss and reduces muscle fibre size by impairing proteostasis and mitochondrial homeostasis
title_sort lifelong dietary protein restriction accelerates skeletal muscle loss and reduces muscle fibre size by impairing proteostasis and mitochondrial homeostasis
topic Skeletal muscle
Sarcopenia
Maternal nutrition
Protein restriction
Proteostasis
Mitochondrial homeostasis
url http://www.sciencedirect.com/science/article/pii/S2213231723003816
work_keys_str_mv AT ufukersoy lifelongdietaryproteinrestrictionacceleratesskeletalmusclelossandreducesmusclefibresizebyimpairingproteostasisandmitochondrialhomeostasis
AT ioanniskanakis lifelongdietaryproteinrestrictionacceleratesskeletalmusclelossandreducesmusclefibresizebyimpairingproteostasisandmitochondrialhomeostasis
AT moussiraalameddine lifelongdietaryproteinrestrictionacceleratesskeletalmusclelossandreducesmusclefibresizebyimpairingproteostasisandmitochondrialhomeostasis
AT gibranpedrazavazquez lifelongdietaryproteinrestrictionacceleratesskeletalmusclelossandreducesmusclefibresizebyimpairingproteostasisandmitochondrialhomeostasis
AT susaneozanne lifelongdietaryproteinrestrictionacceleratesskeletalmusclelossandreducesmusclefibresizebyimpairingproteostasisandmitochondrialhomeostasis
AT mandyjaynepeffers lifelongdietaryproteinrestrictionacceleratesskeletalmusclelossandreducesmusclefibresizebyimpairingproteostasisandmitochondrialhomeostasis
AT malcolmjjackson lifelongdietaryproteinrestrictionacceleratesskeletalmusclelossandreducesmusclefibresizebyimpairingproteostasisandmitochondrialhomeostasis
AT katarzynagoljanekwhysall lifelongdietaryproteinrestrictionacceleratesskeletalmusclelossandreducesmusclefibresizebyimpairingproteostasisandmitochondrialhomeostasis
AT aphroditevasilaki lifelongdietaryproteinrestrictionacceleratesskeletalmusclelossandreducesmusclefibresizebyimpairingproteostasisandmitochondrialhomeostasis