Exercise training enhances muscle mitochondrial metabolism in diet-resistant obesity.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Sep 2022
Historique:
received: 01 03 2022
revised: 05 07 2022
accepted: 15 07 2022
pubmed: 15 8 2022
medline: 21 9 2022
entrez: 14 8 2022
Statut: ppublish

Résumé

Current paradigms for predicting weight loss in response to energy restriction have general validity but a subset of individuals fail to respond adequately despite documented diet adherence. Patients in the bottom 20% for rate of weight loss following a hypocaloric diet (diet-resistant) have been found to have less type I muscle fibres and lower skeletal muscle mitochondrial function, leading to the hypothesis that physical exercise may be an effective treatment when diet alone is inadequate. In this study, we aimed to assess the efficacy of exercise training on mitochondrial function in women with obesity with a documented history of minimal diet-induced weight loss. From over 5000 patient records, 228 files were reviewed to identify baseline characteristics of weight loss response from women with obesity who were previously classified in the top or bottom 20% quintiles based on rate of weight loss in the first 6 weeks during which a 900 kcal/day meal replacement was consumed. A subset of 20 women with obesity were identified based on diet-resistance (n=10) and diet sensitivity (n=10) to undergo a 6-week supervised, progressive, combined aerobic and resistance exercise intervention. Diet-sensitive women had lower baseline adiposity, higher fasting insulin and triglycerides, and a greater number of ATP-III criteria for metabolic syndrome. Conversely in diet-resistant women, the exercise intervention improved body composition, skeletal muscle mitochondrial content and metabolism, with minimal effects in diet-sensitive women. In-depth analyses of muscle metabolomes revealed distinct group- and intervention- differences, including lower serine-associated sphingolipid synthesis in diet-resistant women following exercise training. Exercise preferentially enhances skeletal muscle metabolism and improves body composition in women with a history of minimal diet-induced weight loss. These clinical and metabolic mechanism insights move the field towards better personalised approaches for the treatment of distinct obesity phenotypes. Canadian Institutes of Health Research (CIHR-INMD and FDN-143278; CAN-163902; CIHR PJT-148634).

Sections du résumé

BACKGROUND BACKGROUND
Current paradigms for predicting weight loss in response to energy restriction have general validity but a subset of individuals fail to respond adequately despite documented diet adherence. Patients in the bottom 20% for rate of weight loss following a hypocaloric diet (diet-resistant) have been found to have less type I muscle fibres and lower skeletal muscle mitochondrial function, leading to the hypothesis that physical exercise may be an effective treatment when diet alone is inadequate. In this study, we aimed to assess the efficacy of exercise training on mitochondrial function in women with obesity with a documented history of minimal diet-induced weight loss.
METHODS METHODS
From over 5000 patient records, 228 files were reviewed to identify baseline characteristics of weight loss response from women with obesity who were previously classified in the top or bottom 20% quintiles based on rate of weight loss in the first 6 weeks during which a 900 kcal/day meal replacement was consumed. A subset of 20 women with obesity were identified based on diet-resistance (n=10) and diet sensitivity (n=10) to undergo a 6-week supervised, progressive, combined aerobic and resistance exercise intervention.
FINDINGS RESULTS
Diet-sensitive women had lower baseline adiposity, higher fasting insulin and triglycerides, and a greater number of ATP-III criteria for metabolic syndrome. Conversely in diet-resistant women, the exercise intervention improved body composition, skeletal muscle mitochondrial content and metabolism, with minimal effects in diet-sensitive women. In-depth analyses of muscle metabolomes revealed distinct group- and intervention- differences, including lower serine-associated sphingolipid synthesis in diet-resistant women following exercise training.
INTERPRETATION CONCLUSIONS
Exercise preferentially enhances skeletal muscle metabolism and improves body composition in women with a history of minimal diet-induced weight loss. These clinical and metabolic mechanism insights move the field towards better personalised approaches for the treatment of distinct obesity phenotypes.
FUNDING BACKGROUND
Canadian Institutes of Health Research (CIHR-INMD and FDN-143278; CAN-163902; CIHR PJT-148634).

Identifiants

pubmed: 35965199
pii: S2352-3964(22)00373-5
doi: 10.1016/j.ebiom.2022.104192
pmc: PMC9482931
pii:
doi:

Substances chimiques

Insulins 0
Sphingolipids 0
Triglycerides 0
Serine 452VLY9402
Adenosine Triphosphate 8L70Q75FXE

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104192

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no conflicts of interest.

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Auteurs

Chantal A Pileggi (CA)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada; Ottawa Institute of Systems Biology, Ottawa, Ontario, Canada; National Research Council of Canada, Digital Technologies Research Centre, Ottawa, Canada.

Denis P Blondin (DP)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada.

Breana G Hooks (BG)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada; Ottawa Institute of Systems Biology, Ottawa, Ontario, Canada; Centre for Infection, Immunity and Inflammation, Ottawa, Ontario, Canada.

Gaganvir Parmar (G)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada; Ottawa Institute of Systems Biology, Ottawa, Ontario, Canada.

Irina Alecu (I)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada; Ottawa Institute of Systems Biology, Ottawa, Ontario, Canada.

David A Patten (DA)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada; Ottawa Institute of Systems Biology, Ottawa, Ontario, Canada.

Alexanne Cuillerier (A)

Department of Cellular and Molecular Medicine, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada.

Conor O'Dwyer (C)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada.

A Brianne Thrush (AB)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada.

Morgan D Fullerton (MD)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada; Centre for Infection, Immunity and Inflammation, Ottawa, Ontario, Canada; Centre for Catalysis Research and Innovation, Ottawa, Ontario, Canada.

Steffany Al Bennett (SA)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada; Ottawa Institute of Systems Biology, Ottawa, Ontario, Canada; Centre for Catalysis Research and Innovation, Ottawa, Ontario, Canada.

Éric Doucet (É)

School of Human Kinetics, Faculty of Health Sciences, University of Ottawa, Ottawa, Ontario, Canada.

François Haman (F)

School of Human Kinetics, Faculty of Health Sciences, University of Ottawa, Ottawa, Ontario, Canada.

Miroslava Cuperlovic-Culf (M)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada; Ottawa Institute of Systems Biology, Ottawa, Ontario, Canada; National Research Council of Canada, Digital Technologies Research Centre, Ottawa, Canada.

Ruth McPherson (R)

Division of Cardiology, University of Ottawa Heart Institute, Ottawa, Ontario Canada.

Robert R M Dent (RRM)

Division of Endocrinology, Department of Medicine, University of Ottawa, Ottawa, Ontario, Canada.

Mary-Ellen Harper (ME)

Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Ontario, Canada; Ottawa Institute of Systems Biology, Ottawa, Ontario, Canada; Centre for Infection, Immunity and Inflammation, Ottawa, Ontario, Canada. Electronic address: mharper@uottawa.ca.

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