Melatonin Potentiates Exercise-Induced Increases in Skeletal Muscle PGC-1α and Optimizes Glycogen Replenishment

Compelling evidence has demonstrated the effect of melatonin on exhaustive exercise tolerance and its modulatory role in muscle energy substrates at the end of exercise. In line with this, PGC-1α and NRF-1 also seem to act on physical exercise tolerance and metabolic recovery after exercise. However...

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Main Authors: Vinícius Silva Faria, Fúlvia Barros Manchado-Gobatto, Pedro Paulo Menezes Scariot, Alessandro Moura Zagatto, Wladimir Rafael Beck
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2022.803126/full
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author Vinícius Silva Faria
Fúlvia Barros Manchado-Gobatto
Pedro Paulo Menezes Scariot
Alessandro Moura Zagatto
Wladimir Rafael Beck
author_facet Vinícius Silva Faria
Fúlvia Barros Manchado-Gobatto
Pedro Paulo Menezes Scariot
Alessandro Moura Zagatto
Wladimir Rafael Beck
author_sort Vinícius Silva Faria
collection DOAJ
description Compelling evidence has demonstrated the effect of melatonin on exhaustive exercise tolerance and its modulatory role in muscle energy substrates at the end of exercise. In line with this, PGC-1α and NRF-1 also seem to act on physical exercise tolerance and metabolic recovery after exercise. However, the literature still lacks reports on these proteins after exercise until exhaustion for animals treated with melatonin. Thus, the aim of the current study was to determine the effects of acute melatonin administration on muscle PGC-1α and NRF-1, and its modulatory role in glycogen and triglyceride contents in rats subjected to exhaustive swimming exercise at an intensity corresponding to the anaerobic lactacidemic threshold (iLAn). In a randomized controlled trial design, thirty-nine Wistar rats were allocated into four groups: control (CG = 10), rats treated with melatonin (MG = 9), rats submitted to exercise (EXG = 10), and rats treated with melatonin and submitted to exercise (MEXG = 10). Forty-eight hours after the graded exercise test, the animals received melatonin (10 mg/kg) or vehicles 30 min prior to time to exhaustion test in the iLAn (tlim). Three hours after tlim the animals were euthanized, followed by muscle collection for specific analyses: soleus muscles for immunofluorescence, gluteus maximus, red and white gastrocnemius for the assessment of glycogen and triglyceride contents, and liver for the measurement of glycogen content. Student t-test for independent samples, two-way ANOVA, and Newman keuls post hoc test were used. MEXG swam 120.3% more than animals treated with vehicle (EXG; p < 0.01). PGC-1α and NRF-1 were higher in MEXG with respect to the CG (p < 0.05); however, only PGC-1α was higher for MEXG when compared to EXG. Melatonin reduced the triglyceride content in gluteus maximus, red and white gastrocnemius (F = 6.66, F = 4.51, and F = 6.02, p < 0.05). The glycogen content in red gastrocnemius was higher in MEXG than in CG (p = 0.01), but not in EXG (p > 0.05). In conclusion, melatonin was found to enhance exercise tolerance, potentiate exercise-mediated increases in PGC-1α, decrease muscle triglyceride content and increase muscle glycogen 3 h after exhaustive exercise, rapidly providing a better cellular metabolic environment for future efforts.
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spelling doaj.art-f8d3eda031e04f9e850cb3024285b9ca2022-12-22T00:11:23ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2022-04-011310.3389/fphys.2022.803126803126Melatonin Potentiates Exercise-Induced Increases in Skeletal Muscle PGC-1α and Optimizes Glycogen ReplenishmentVinícius Silva Faria0Fúlvia Barros Manchado-Gobatto1Pedro Paulo Menezes Scariot2Alessandro Moura Zagatto3Wladimir Rafael Beck4Laboratory of Endocrine Physiology and Physical Exercise, Department of Physiological Sciences, Federal University of São Carlos—UFSCar, São Carlos, BrazilLaboratory of Applied Sport Physiology, School of Applied Sciences, University of Campinas—UNICAMP, Limeira, BrazilLaboratory of Applied Sport Physiology, School of Applied Sciences, University of Campinas—UNICAMP, Limeira, BrazilLaboratory of Physiology and Sports Performance, Department of Physical Education, School of Science—Bauru Campus, São Paulo State University—UNESP, Bauru, BrazilLaboratory of Endocrine Physiology and Physical Exercise, Department of Physiological Sciences, Federal University of São Carlos—UFSCar, São Carlos, BrazilCompelling evidence has demonstrated the effect of melatonin on exhaustive exercise tolerance and its modulatory role in muscle energy substrates at the end of exercise. In line with this, PGC-1α and NRF-1 also seem to act on physical exercise tolerance and metabolic recovery after exercise. However, the literature still lacks reports on these proteins after exercise until exhaustion for animals treated with melatonin. Thus, the aim of the current study was to determine the effects of acute melatonin administration on muscle PGC-1α and NRF-1, and its modulatory role in glycogen and triglyceride contents in rats subjected to exhaustive swimming exercise at an intensity corresponding to the anaerobic lactacidemic threshold (iLAn). In a randomized controlled trial design, thirty-nine Wistar rats were allocated into four groups: control (CG = 10), rats treated with melatonin (MG = 9), rats submitted to exercise (EXG = 10), and rats treated with melatonin and submitted to exercise (MEXG = 10). Forty-eight hours after the graded exercise test, the animals received melatonin (10 mg/kg) or vehicles 30 min prior to time to exhaustion test in the iLAn (tlim). Three hours after tlim the animals were euthanized, followed by muscle collection for specific analyses: soleus muscles for immunofluorescence, gluteus maximus, red and white gastrocnemius for the assessment of glycogen and triglyceride contents, and liver for the measurement of glycogen content. Student t-test for independent samples, two-way ANOVA, and Newman keuls post hoc test were used. MEXG swam 120.3% more than animals treated with vehicle (EXG; p < 0.01). PGC-1α and NRF-1 were higher in MEXG with respect to the CG (p < 0.05); however, only PGC-1α was higher for MEXG when compared to EXG. Melatonin reduced the triglyceride content in gluteus maximus, red and white gastrocnemius (F = 6.66, F = 4.51, and F = 6.02, p < 0.05). The glycogen content in red gastrocnemius was higher in MEXG than in CG (p = 0.01), but not in EXG (p > 0.05). In conclusion, melatonin was found to enhance exercise tolerance, potentiate exercise-mediated increases in PGC-1α, decrease muscle triglyceride content and increase muscle glycogen 3 h after exhaustive exercise, rapidly providing a better cellular metabolic environment for future efforts.https://www.frontiersin.org/articles/10.3389/fphys.2022.803126/fullperoxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α)nuclear respiratory factor 1 (NRF-1)energy metabolism (MeSH ID: D004734)aerobic exerciseN-acetyl-5-methoxytryptaminerecovery
spellingShingle Vinícius Silva Faria
Fúlvia Barros Manchado-Gobatto
Pedro Paulo Menezes Scariot
Alessandro Moura Zagatto
Wladimir Rafael Beck
Melatonin Potentiates Exercise-Induced Increases in Skeletal Muscle PGC-1α and Optimizes Glycogen Replenishment
Frontiers in Physiology
peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α)
nuclear respiratory factor 1 (NRF-1)
energy metabolism (MeSH ID: D004734)
aerobic exercise
N-acetyl-5-methoxytryptamine
recovery
title Melatonin Potentiates Exercise-Induced Increases in Skeletal Muscle PGC-1α and Optimizes Glycogen Replenishment
title_full Melatonin Potentiates Exercise-Induced Increases in Skeletal Muscle PGC-1α and Optimizes Glycogen Replenishment
title_fullStr Melatonin Potentiates Exercise-Induced Increases in Skeletal Muscle PGC-1α and Optimizes Glycogen Replenishment
title_full_unstemmed Melatonin Potentiates Exercise-Induced Increases in Skeletal Muscle PGC-1α and Optimizes Glycogen Replenishment
title_short Melatonin Potentiates Exercise-Induced Increases in Skeletal Muscle PGC-1α and Optimizes Glycogen Replenishment
title_sort melatonin potentiates exercise induced increases in skeletal muscle pgc 1α and optimizes glycogen replenishment
topic peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α)
nuclear respiratory factor 1 (NRF-1)
energy metabolism (MeSH ID: D004734)
aerobic exercise
N-acetyl-5-methoxytryptamine
recovery
url https://www.frontiersin.org/articles/10.3389/fphys.2022.803126/full
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