Paulo H. C. Mesquita

Oklahoma Medical Research Foundation

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Andreas N. Kavazis

Auburn University

Michael D. Roberts

SUNY Downstate Health Sciences University

Joshua S. Godwin

Auburn University

Bradley A. Ruple

Auburn University

Mason C. McIntosh

Auburn University

Shelby C. Osburn

Auburn University

Kaelin C. Young

Auburn University

Ramy K. A. Sayed

Sohag University

Kent W. Jorgenson

University of Wisconsin–Madison

Troy A. Hornberger

University of Wisconsin–Madison

Cooperative Institutions

Auburn University

Universidade Federal de Minas Gerais

Universidade Federal de São Carlos

Applied Sciences Laboratory (United States)

Edward Via College of Osteopathic Medicine

Universidade de São Paulo

Washburn University

Sohag University

University of Wisconsin–Madison

McMaster University

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Acute and chronic effects of resistance training on skeletal muscle markers of mitochondrial remodeling in older adults

Physiological Reports (2020)

Paulo H. C. Mesquita Donald A. Lamb Hailey A. Parry Johnathon H. Moore Morgan A. Smith

We investigated the acute and chronic effects of resistance training (RT) on skeletal muscle markers of mitochondrial content and remodeling in older, untrained adults. Sixteen participants (n = 6 males, n = 10 females; age = 59 ± 4 years) completed 10 weeks of full-body RT (2 day/week). Muscle biopsies from the vastus lateralis were obtained prior to RT (Pre), 24 hr following the first training session (Acute), and 72 hr following the last training session (Chronic). Protein levels of mitochondrial electron transport chain complexes I–V (+39 to +180%, p ≤ .020) and markers of mitochondrial fusion Mfn1 (+90%, p = .003), Mfn2 (+110%, p < .001), and Opa1 (+261%, p = .004) increased following chronic RT. Drp1 protein levels also increased (+134%, p = .038), while Fis1 protein levels did not significantly change (−5%, p = .584) following chronic RT. Interestingly, protein markers of mitochondrial biogenesis (i.e., PGC-1α, TFAM, and NRF1) or mitophagy (i.e., Pink1 and Parkin) were not significantly altered (p > .050) after 10 weeks of RT. In summary, chronic RT promoted increases in content of electron transport chain proteins (i.e., increased protein levels of all five OXPHOS complexes) and increase in the levels of proteins related to mitochondrial dynamics (i.e., increase in fusion protein markers) in skeletal muscle of older adults. These results suggest that chronic RT could be a useful strategy to increase mitochondrial protein content in older individuals.

MFN2

FIS1

MFN1

PINK1

TFAM

NRF1

DNM1L

10.14814/phy2.14526

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Citations (46)

Resistance training diminishes mitochondrial adaptations to subsequent endurance training in healthy untrained men

The Journal of Physiology (2023)

Paulo H. C. Mesquita Joshua S. Godwin Bradley A. Ruple Casey L. Sexton Mason C. McIntosh

Abstract We investigated the effects of performing a period of resistance training (RT) on the performance and molecular adaptations to a subsequent period of endurance training (ET). Twenty‐five young adults were divided into an RT+ET group ( n = 13), which underwent 7 weeks of RT followed by 7 weeks of ET, and an ET‐only group ( n = 12), which performed 7 weeks of ET. Body composition, endurance performance and muscle biopsies were collected before RT (T1, baseline for RT+ET), before ET (T2, after RT for RT+ET and baseline for ET) and after ET (T3). Immunohistochemistry was performed to determine fibre cross‐sectional area (fCSA), myonuclear content, myonuclear domain size, satellite cell number and mitochondrial content. Western blots were used to quantify markers of mitochondrial remodelling. Citrate synthase activity and markers of ribosome content were also investigated. RT improved body composition and strength, increased vastus lateralis thickness, mixed and type II fCSA, myonuclear number, markers of ribosome content, and satellite cell content ( P < 0.050). In response to ET, both groups similarly decreased body fat percentage ( P < 0.0001) and improved endurance performance (e.g. , and speed at which the onset of blood lactate accumulation occurred, P < 0.0001). Levels of mitochondrial complexes I–IV in the ET‐only group increased 32–66%, while those in the RT+ET group increased 1–11% (time, P < 0.050). Additionally, mixed fibre relative mitochondrial content increased 15% in the ET‐only group but decreased 13% in the RT+ET group (interaction, P = 0.043). In conclusion, RT performed prior to ET had no additional benefits to ET adaptations. Moreover, prior RT seemed to impair mitochondrial adaptations to ET. image Key points Resistance training is largely underappreciated as a method to improve endurance performance, despite reports showing it may improve mitochondrial function. Although several concurrent training studies are available, in this study we investigated the effects of performing a period of resistance training on the performance and molecular adaptations to subsequent endurance training. Prior resistance training did not improve endurance performance and impaired most mitochondrial adaptations to subsequent endurance training, but this effect may have been a result of detraining from resistance training.

Endurance Training

10.1113/jp284822

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Skeletal Muscle LINE‐1 Gene Regulation and Inflammatory Response to Chronic, Voluntary Endurance Training in Rodents

The FASEB Journal (2022)

Shelby C. Osburn Paulo H. C. Mesquita Frances K. Neal Bradley A. Ruple Matthew T. Holmes

We sought to determine the effects of chronic, voluntary wheel running on Long Interspersed Nuclear Element-1 (LINE-1) mRNA expression and promoter methylation, as well as markers of the cGAS-STING inflammatory pathway, in skeletal muscle.LINE-1 mRNA expression will increase with age, and exercise will mitigate this increase. This difference in expression will be driven through changes in promoter methylation. The cGAS-STING inflammatory pathway will be upregulated with age and downregulated with rats that exercise-trained.Plantaris and soleus skeletal muscles were collected from female Lewis rats that belonged to one of three groups: a young control group (CTL; n=10; 6 mos old), an aged sedentary group (SED; n=12; 15 mos old), and an aged exercise group with access to a running wheel for 9 months (EX; n=12; 15 mos old). RNA, DNA, and protein were isolated from the tissues for analysis. Analysis included RT-qPCR for LINE-1 mRNA expression, methylated DNA Immunoprecipitation (MeDIP) to assess the methylation status of the LINE-1 promoter via RT-qPCR, and Western blotting for markers of the cGAS-STING pathway and 4Hydroxynonenal (4HNE). Two primer sets were used for RT-qPCR: L1-3 probed for the most active form of LINE-1 and L1-Tot probed for all full-length LINE-1 elements.There was no significant difference in plantaris LINE-1 mRNA expression or for L1-3 or L1-Tot. Plantaris LINE-1 promoter methylation was undetectable in most samples, so the results are not presented herein. Soleus L1-3 mRNA was significantly higher in EX compared to CTL (p=0.036) and there was a trend between SED and EX (p=0.053). L1-Tot also was trending (p=0.059), where EX was higher than CTL (p=0.025). Methylation of the LINE-1 promoter was significantly different for both L1-3 and L1-Tot (p=0.021 and p=0.028, respectively). In both instances, LINE-1 DNA in SED and EX were significantly more methylated compared to CTL. There were no differences in cGAS protein expression, p-/pan STING protein expression, or 4HNE expression.Contrary to the original hypothesis, LINE-1 mRNA expression and DNA methylation were higher in the exercise group. Additionally, chronic exercise did not affect the cGAS-STING inflammatory pathway, highlighting this pathway may be more relevant in extreme age and disease states. Previous skeletal muscle research has focused on using mixed muscle types to look at LINE-1 expression and regulation, so the differences seen between type I (soleus) and type II (plantaris) fibers is a novel finding that warrants further investigation to understand the underlying mechanisms.

Bisulfite sequencing

10.1096/fasebj.2022.36.s1.r5493

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A putative low-carbohydrate ketogenic diet elicits mild nutritional ketosis but does not impair the acute or chronic hypertrophic responses to resistance exercise in rodents

Journal of Applied Physiology (2015)

Michael D. Roberts A. Maleah Holland Wesley C. Kephart C. Brooks Mobley Petey W. Mumford

We examined whether acute and/or chronic skeletal muscle anabolism is impaired with a low-carbohydrate diet formulated to elicit ketosis (LCKD) vs. a mixed macronutrient Western diet (WD). Male Sprague-Dawley rats (9-10 wk of age, 300-325 g) were provided isoenergetic amounts of a LCKD or a WD for 6 wk. In AIM 1, basal serum and gastrocnemius assessments were performed. In AIM 2, rats were resistance exercised for one bout and were euthanized 90-270 min following exercise for gastrocnemius analyses. In AIM 3, rats voluntarily exercised daily with resistance-loaded running wheels, and hind limb muscles were analyzed for hypertrophy markers at the end of the 6-wk protocol. In AIM 1, basal levels of gastrocnemius phosphorylated (p)-rps6, p-4EBP1, and p-AMPKα were similar between diets, although serum insulin (P < 0.01), serum glucose (P < 0.001), and several essential amino acid levels (P < 0.05) were lower in LCKD-fed rats. In AIM 2, LCKD- and WD-fed rats exhibited increased postexercise muscle protein synthesis levels (P < 0.0125), but no diet effect was observed (P = 0.59). In AIM 3, chronically exercise-trained LCKD- and WD-fed rats presented similar increases in relative hind limb muscle masses compared with their sedentary counterparts (12-24%, P < 0.05), but there was no between-diet effects. Importantly, the LCKD induced "mild" nutritional ketosis, as the LCKD-fed rats in AIM 2 exhibited ∼1.5-fold greater serum β-hydroxybutyrate levels relative to WD-fed rats (diet effect P = 0.003). This study demonstrates that the tested LCKD in rodents, while only eliciting mild nutritional ketosis, does not impair the acute or chronic skeletal muscle hypertrophic responses to resistance exercise.

Ketogenic Diet

Basal (medicine)

Gastrocnemius muscle

Hindlimb

10.1152/japplphysiol.00837.2015

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Citations (27)

Relative Age Effect and ACTN3 R577X and ACE I/D Polymorphisms in Brazilian Football Players: An Association Genetic Study

Research Quarterly for Exercise and Sport (2024)

Maicon Rodrigues Albuquerque Andressa Eliza da Silva Cunha João Locke Ferreira de Araújo Rodrigo dos Santos Guimarães Michele Rafaela Cândida Ciríaco Rocha

The Relative Age Effect (RAE) suggests older athletes within an annual cohort have advantages over their younger peers. We hypothesized that younger athletes could overcome these disadvantages through favorable α-actinin-3 (

Football players

Association (psychology)

10.1080/02701367.2024.2407883

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Long-term voluntary wheel running effects on markers of long interspersed nuclear element-1 in skeletal muscle, liver, and brain tissue of female rats

AJP Cell Physiology (2022)

Shelby C. Osburn Paulo H. C. Mesquita Frances K. Neal Melissa N. Rumbley Matthew T. Holmes

We sought to determine the effects of long-term voluntary wheel running on markers of long interspersed nuclear element-1 (L1) in skeletal muscle, liver, and the hippocampus of female rats. In addition, markers of the cGAS-STING DNA-sensing pathway that results in inflammation were interrogated. Female Lewis rats (n = 34) were separated into one of three groups including a 6-mo-old group to serve as a young comparator group (CTL, n = 10), a group that had access to a running wheel for voluntary wheel running (EX, n = 12), and an age-matched group that did not (SED, n = 12). Both SED and EX groups were carried out from 6 mo to 15 mo of age. There were no significant differences in L1 mRNA expression for any of the tissues between groups. Methylation of the L1 promoter in the soleus and hippocampus was significantly higher in SED and EX than in CTL group (P < 0.05). ORF1p expression was higher in older SED and EX rats than in CTL rats for every tissue (P < 0.05). There were no differences between groups for L1 mRNA or cGAS-STING pathway markers. Our results suggest there is an increased ORF1 protein expression across tissues with aging that is not mitigated by voluntary wheel running. In addition, although previous data imply that L1 methylation changes may play a role in acute exercise for L1 RNA expression, this does not seem to occur during extended periods of voluntary wheel running.

sed

Turnover

10.1152/ajpcell.00234.2022

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Citations (7)

Resistance training increases muscle NAD+ and NADH concentrations as well as NAMPT protein levels and global sirtuin activity in middle-aged, overweight, untrained individuals

Aging (2020)

Donald A. Lamb Johnathon H. Moore Paulo H. C. Mesquita Morgan A. Smith Christopher G. Vann

We examined if resistance training affected muscle NAD+ and NADH concentrations as well as nicotinamide phosphoribosyltransferase (NAMPT) protein levels and sirtuin (SIRT) activity markers in middle-aged, untrained (MA) individuals. MA participants (59±4 years old; n=16) completed 10 weeks of full-body resistance training (2 d/wk). Body composition, knee extensor strength, and vastus lateralis muscle biopsies were obtained prior to training (Pre) and 72 hours following the last training bout (Post). Data from trained college-aged men (22±3 years old, training age: 6±2 years old; n=15) were also obtained for comparative purposes. Muscle NAD+ (+127%, p<0.001), NADH (+99%, p=0.002), global SIRT activity (+13%, p=0.036), and NAMPT protein (+15%, p=0.014) increased from Pre to Post in MA participants. Additionally, Pre muscle NAD+ and NADH in MA participants were lower than college-aged participants (p<0.05), whereas Post values were similar between cohorts (p>0.10). Interestingly, muscle citrate synthase activity levels (i.e., mitochondrial density) increased in MA participants from Pre to Post (+183%, p<0.001), and this increase was significantly associated with increases in muscle NAD+ (r2=0.592, p=0.001). In summary, muscle NAD+, NADH, and global SIRT activity are positively affected by resistance training in middle-aged, untrained individuals. Whether these adaptations facilitated mitochondrial biogenesis remains to be determined.

Sirtuin 1

10.18632/aging.103218

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Citations (48)

Mitochondrial remodelling supports migration in white-crowned sparrows ( Zonotrichia leucophrys )

Proceedings of the Royal Society B Biological Sciences (2024)

Paulo H. C. Mesquita E. A. Rhodes Kang Nian Yap Breanna J. Mueller Geoffrey E. Hill

The migratory movements undertaken by birds are among the most energetically demanding behaviours observed in nature. Mitochondria are the source of aerobic energy production on which migration depends, but a key component of mitochondrial function, mitochondrial remodelling, has not been investigated in the context of bird migration. We measured markers of mitochondrial remodelling in the skeletal muscles of the Gambel's (migratory) and Nuttall's (non-migratory) white-crowned sparrows within and outside migratory periods. Gambel's were collected in (i) a non-migration period (baseline), (ii) preparation to depart for spring migration (pre-migration) and (iii) active autumn migration (mid-migration). Nuttall's were collected at timepoints corresponding to baseline and mid-migration in Gambel's. Across all sampling periods, we found that migratory birds had greater mitochondrial remodelling compared with non-migratory birds. Furthermore, birds from the migratory population also displayed flexibility, increasing several markers of mitochondrial remodelling (e.g. NRF1, OPA1 and Drp1) pre- and during migration. Further, the greater levels of mitochondrial remodelling and its upregulation during migration were specific to the pectoralis muscle used in flapping flight. Our study is the first to show that mitochondrial remodelling supports migration in Gambel's white-crowned sparrows, indicating a highly specific and efficient phenotype supporting the increased energetic demands of migration.

White (mutation)

10.1098/rspb.2024.2409

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Citations (2)

Do executive function performance, gaze behavior, and pupil size change during incremental acute physical exercise?

Psychophysiology (2022)

Maicon Rodrigues Albuquerque Beatriz Hooper Iasmin Oliveira de Sousa Viana Paulo H. C. Mesquita Tony Meireles Santos

Abstract Several studies have investigated the interaction between acute physical exercise and cognitive performance. However, few studies have investigated this issue during acute high‐intensity exercise. In the present study, we evaluated executive functions (EFs) during incremental exercise in three different intensities [below lactate threshold (LT), at LT, and above LT], measuring EFs performance, gaze behavior, and pupil diameter. Twenty subjects were familiarized with the EFs test and participated in a graded maximal exercise test on a cycle ergometer on the first visit. On the second visit, they performed the EFs task at rest and while exercising at three different intensities using mobile eye‐tracking glasses. Our results showed that the psychophysiological measures differed between the conditions. Regarding EFs performance, during exercise above LT, the subjects showed worse accuracy when compared with rest ( p < .001) and below LT ( p < .001). In addition, the response time (RT) at LT and above LT was shorter than in the rest condition ( p < .050). Further, RT was faster ( p = .002) in the above LT than in the below LT condition. In addition, the gaze behavior measures indicated that exercise, independently of the intensity, improves the number of fixations with shorter fixation durations compared to the rest condition ( p < .050). Additionally, we found no significant differences in average and peak pupil diameter between conditions. In conclusion, exercise at LT improves the EFs performance while exercising above LT worsens EFs performance. However, there were no significant differences in average and peak pupil diameter between conditions.

Lactate threshold

Rest (music)

10.1111/psyp.14233

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Citations (3)

Ketogenic versus Western and standard chow diets favorably alters fat deposition and serum biomarkers in rats

Journal of the International Society of Sports Nutrition (2015)

A. Maleah Holland Wesley C. Kephart Ryan P. Lowery Petey W. Mumford C. Brooks Mobley

Methods Male Sprague-Dawley rats (~9-10 weeks of age) were provided isocaloric amounts of either a KD (5.2 kcal/g, 20.2% protein, 10.3% carbohydrate, 69.5% fat; n = 50), WD (4.5 kcal/g, 15.2% protein, 42.7% carbohydrate, 42.0% fat; n = 66), or StdChow (3.1 kcal/g, 24.0% protein, 58.0% carbohydrate, 18.0% fat n = 10) for 6 weeks with daily food intake and body weights recorded. After the animals were sacrificed, 4 different fat depots were weighed and serum was collected in subsets of each diet for further investigation.

Ketogenic Diet

Clinical nutrition

10.1186/1550-2783-12-s1-p21

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