Resistance training in humans and mechanical overload in rodents do not elevate muscle protein lactylation

Although several reports have hypothesized that exercise may increase skeletal muscle protein lactylation, empirical evidence in humans is lacking. Thus, we adopted a multi-faceted approach to examine if acute and subchronic resistance training (RT) altered skeletal muscle protein lactylation levels...

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Main Authors: Madison L. Mattingly, Bradley A. Ruple, Casey L. Sexton, Joshua S. Godwin, Mason C. McIntosh, Morgan A. Smith, Daniel L. Plotkin, J. Max Michel, Derick A. Anglin, Nicholas J. Kontos, Shengyi Fei, Stuart M. Phillips, C. Brooks Mobley, Ivan Vechetti, Christopher G. Vann, Michael D. Roberts
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Physiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2023.1281702/full
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author Madison L. Mattingly
Bradley A. Ruple
Casey L. Sexton
Joshua S. Godwin
Mason C. McIntosh
Morgan A. Smith
Daniel L. Plotkin
J. Max Michel
Derick A. Anglin
Nicholas J. Kontos
Shengyi Fei
Stuart M. Phillips
C. Brooks Mobley
Ivan Vechetti
Christopher G. Vann
Michael D. Roberts
author_facet Madison L. Mattingly
Bradley A. Ruple
Casey L. Sexton
Joshua S. Godwin
Mason C. McIntosh
Morgan A. Smith
Daniel L. Plotkin
J. Max Michel
Derick A. Anglin
Nicholas J. Kontos
Shengyi Fei
Stuart M. Phillips
C. Brooks Mobley
Ivan Vechetti
Christopher G. Vann
Michael D. Roberts
author_sort Madison L. Mattingly
collection DOAJ
description Although several reports have hypothesized that exercise may increase skeletal muscle protein lactylation, empirical evidence in humans is lacking. Thus, we adopted a multi-faceted approach to examine if acute and subchronic resistance training (RT) altered skeletal muscle protein lactylation levels. In mice, we also sought to examine if surgical ablation-induced plantaris hypertrophy coincided with increases in muscle protein lactylation. To examine acute responses, participants’ blood lactate concentrations were assessed before, during, and after eight sets of an exhaustive lower body RT bout (n = 10 trained college-aged men). Vastus lateralis biopsies were also taken before, 3-h post, and 6-h post-exercise to assess muscle protein lactylation. To identify training responses, another cohort of trained college-aged men (n = 14) partook in 6 weeks of lower-body RT (3x/week) and biopsies were obtained before and following the intervention. Five-month-old C57BL/6 mice were subjected to 10 days of plantaris overload (OV, n = 8) or served as age-matched sham surgery controls (Sham, n = 8). Although acute resistance training significantly increased blood lactate responses ∼7.2-fold (p < 0.001), cytoplasmic and nuclear protein lactylation levels were not significantly altered at the post-exercise time points, and no putative lactylation-dependent mRNA was altered following exercise. Six weeks of RT did not alter cytoplasmic protein lactylation (p = 0.800) despite significantly increasing VL muscle size (+3.5%, p = 0.037), and again, no putative lactylation-dependent mRNA was significantly affected by training. Plantaris muscles were larger in OV versus Sham mice (+43.7%, p < 0.001). However, cytoplasmic protein lactylation was similar between groups (p = 0.369), and nuclear protein lactylation was significantly lower in OV versus Sham mice (p < 0.001). The current null findings, along with other recent null findings in the literature, challenge the thesis that lactate has an appreciable role in promoting skeletal muscle hypertrophy.
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spelling doaj.art-f6fefc65127a4fa792b41571c17d0bf22023-09-29T04:47:42ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2023-09-011410.3389/fphys.2023.12817021281702Resistance training in humans and mechanical overload in rodents do not elevate muscle protein lactylationMadison L. Mattingly0Bradley A. Ruple1Casey L. Sexton2Joshua S. Godwin3Mason C. McIntosh4Morgan A. Smith5Daniel L. Plotkin6J. Max Michel7Derick A. Anglin8Nicholas J. Kontos9Shengyi Fei10Stuart M. Phillips11C. Brooks Mobley12Ivan Vechetti13Christopher G. Vann14Michael D. Roberts15School of Kinesiology, Auburn University, Auburn, AL, United StatesSchool of Kinesiology, Auburn University, Auburn, AL, United StatesDepartment of Physiology and Aging, University of Florida, Gainesville, FL, United StatesSchool of Kinesiology, Auburn University, Auburn, AL, United StatesSchool of Kinesiology, Auburn University, Auburn, AL, United StatesDepartment of Genetics, Standford University, Stanford, CA, United StatesSchool of Kinesiology, Auburn University, Auburn, AL, United StatesSchool of Kinesiology, Auburn University, Auburn, AL, United StatesSchool of Kinesiology, Auburn University, Auburn, AL, United StatesSchool of Kinesiology, Auburn University, Auburn, AL, United StatesDepartment of Nutrition and Health Sciences, University of Nebraska-Lincoln, Lincoln, NE, United StatesDepartment of Kinesiology, McMaster University, Hamilton, ON, CanadaSchool of Kinesiology, Auburn University, Auburn, AL, United StatesDepartment of Nutrition and Health Sciences, University of Nebraska-Lincoln, Lincoln, NE, United StatesDuke Molecular Physiology Institute, Duke University School of Medicine, Duke University, Durham, NC, United StatesSchool of Kinesiology, Auburn University, Auburn, AL, United StatesAlthough several reports have hypothesized that exercise may increase skeletal muscle protein lactylation, empirical evidence in humans is lacking. Thus, we adopted a multi-faceted approach to examine if acute and subchronic resistance training (RT) altered skeletal muscle protein lactylation levels. In mice, we also sought to examine if surgical ablation-induced plantaris hypertrophy coincided with increases in muscle protein lactylation. To examine acute responses, participants’ blood lactate concentrations were assessed before, during, and after eight sets of an exhaustive lower body RT bout (n = 10 trained college-aged men). Vastus lateralis biopsies were also taken before, 3-h post, and 6-h post-exercise to assess muscle protein lactylation. To identify training responses, another cohort of trained college-aged men (n = 14) partook in 6 weeks of lower-body RT (3x/week) and biopsies were obtained before and following the intervention. Five-month-old C57BL/6 mice were subjected to 10 days of plantaris overload (OV, n = 8) or served as age-matched sham surgery controls (Sham, n = 8). Although acute resistance training significantly increased blood lactate responses ∼7.2-fold (p < 0.001), cytoplasmic and nuclear protein lactylation levels were not significantly altered at the post-exercise time points, and no putative lactylation-dependent mRNA was altered following exercise. Six weeks of RT did not alter cytoplasmic protein lactylation (p = 0.800) despite significantly increasing VL muscle size (+3.5%, p = 0.037), and again, no putative lactylation-dependent mRNA was significantly affected by training. Plantaris muscles were larger in OV versus Sham mice (+43.7%, p < 0.001). However, cytoplasmic protein lactylation was similar between groups (p = 0.369), and nuclear protein lactylation was significantly lower in OV versus Sham mice (p < 0.001). The current null findings, along with other recent null findings in the literature, challenge the thesis that lactate has an appreciable role in promoting skeletal muscle hypertrophy.https://www.frontiersin.org/articles/10.3389/fphys.2023.1281702/fullskeletal musclehypertrophylactatelactylationposttranslational modification
spellingShingle Madison L. Mattingly
Bradley A. Ruple
Casey L. Sexton
Joshua S. Godwin
Mason C. McIntosh
Morgan A. Smith
Daniel L. Plotkin
J. Max Michel
Derick A. Anglin
Nicholas J. Kontos
Shengyi Fei
Stuart M. Phillips
C. Brooks Mobley
Ivan Vechetti
Christopher G. Vann
Michael D. Roberts
Resistance training in humans and mechanical overload in rodents do not elevate muscle protein lactylation
Frontiers in Physiology
skeletal muscle
hypertrophy
lactate
lactylation
posttranslational modification
title Resistance training in humans and mechanical overload in rodents do not elevate muscle protein lactylation
title_full Resistance training in humans and mechanical overload in rodents do not elevate muscle protein lactylation
title_fullStr Resistance training in humans and mechanical overload in rodents do not elevate muscle protein lactylation
title_full_unstemmed Resistance training in humans and mechanical overload in rodents do not elevate muscle protein lactylation
title_short Resistance training in humans and mechanical overload in rodents do not elevate muscle protein lactylation
title_sort resistance training in humans and mechanical overload in rodents do not elevate muscle protein lactylation
topic skeletal muscle
hypertrophy
lactate
lactylation
posttranslational modification
url https://www.frontiersin.org/articles/10.3389/fphys.2023.1281702/full
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