Time Course of Skeletal Muscle miRNA Expression after Resistance, High-Intensity Interval, and Concurrent Exercise

Abstract

IntroductionExercise-induced microRNA (miRNA) expression has been implicated in the regulation of skeletal muscle plasticity. However, the specificity and acute time course in miRNA expression after divergent exercise modes are unknown. In a randomized crossover design, we compared the acute expression profile of eight skeletal muscle miRNAs previously reported to be involved in skeletal muscle development, growth, and maintenance after a bout of either resistance exercise (RE), high-intensity interval exercise (HIIE), and concurrent resistance and high-intensity interval exercises (CE).MethodsNine untrained young men (23.9 ± 2.8 yr, 70.1 ± 14.9 kg, 177.2 ± 3.0 cm, 41.4 ± 5.2 mL·kg−1·min−1) underwent a counterbalanced crossover design in which they performed bouts of RE (2 × 10 repetitions maximum 45° leg press and leg extension exercises), HIEE (12 × 1-min sprints at V˙O2peak with 1-min rest intervals between sprints), and CE (RE followed by HIIE), separated by 1 wk. Vastus lateralis biopsies were harvested immediately before (Pre) and immediately (0 h), 4 h, and 8 h after each exercise bout.ResultsThere were similar increases (main effect of time; P < 0.05) in miR-1-3p, miR-133a-3p, miR-133b, miR-181a-3p, and miR-486 expression at 8 h from Pre with all exercise modes. Besides a main effect of time, miR-23a-3p and miR-206 presented a main effect of condition with lower expression after HIIE compared with RE and CE.ConclusionsSelect miRNAs (miR-1-3p, miR-133a-3p, miR-133b, miR-23a-3p, miR-181a-3p, miR-206, miR-486) do not exhibit an expression specificity in the acute recovery period after a single bout of RE, HIIE, or CE in skeletal muscle. Our data also indicate that RE has a higher effect on the expression of miR-23a-3p and miR-206 than HIIE. As upregulation of these miRNAs seems to be confined to the 8-h period after exercise, this may subsequently affect the expression patterns of target mRNAs forming the basis of exercise-induced adaptive responses.

Exercise-Induced Circulating microRNAs: Potential Key Factors in the Control of Breast Cancer

“…miRNA expression is modulated both acutely and chronically following exercise ( D'Souza et al, 2017 ; Mooren et al, 2014 ; Nielsen et al, 2010 ; Telles et al, 2021 ; Uhlemann et al, 2014 ; Baggish et al, 2011 ; Banzet et al, 2013 ; Tonevitsky et al, 2013 ; Aoi et al, 2013 ; Sawada et al, 2013 ; Nielsen et al, 2014 ; Baggish et al, 2014 ; Mitchelson and Qin, 2015 ; Russell et al, 2013 ; Gomes et al, 2014 ). For example, miR-133 is canonically expressed in skeletal muscle ( D'Souza et al, 2017 ; Nielsen et al, 2010 ; Telles et al, 2021 ; Mitchelson and Qin, 2015 ; Russell et al, 2013 ) and significantly increased in the bloodstream (i.e., c-miR-133) after an exercise bout ( Banzet et al, 2013 ; Baggish et al, 2014 ; Gomes et al, 2014 ; Mooren et al, 2014 ; Nielsen et al, 2014 ). Interestingly, it was demonstrated that miR-133a expression is significantly reduced in five breast cancer cell lines (MCF-7, MDA-MB-231, BT-549, SK-BR-3, and T47D) compared to a normal breast cell line HBL-100, as well as in human breast cancer tissue compared to adjacent non-cancerous breast tissue ( Cui et al, 2013 ).…”

“…Interestingly, miR-206 transfection and anti-miR-30c silencing inhibit cell growth and increase apoptosis of MCF-7 breast cancer cells. It is noteworthy that miR-206 is also canonically expressed in the skeletal muscle ( Mitchelson and Qin, 2015 ; Telles et al, 2021 ). Collectively, it is plausible to suggest that miRNAs can translocate from the muscle to the bloodstream in response to an exercise bout and regulate gene expression in pathways associated with tumor growth and suppression in breast cancer cells ( Figure 1 ) ( Dufresne et al, 2018 ).…”

“…The expression of a number of miRNAs (e.g., miR-1, -21, -23a, -133a, -133b, -181a, -206, -378, and -486) is modulated in the human skeletal muscle ( Camera et al, 2016 ; D'Souza et al, 2017 ; Davidsen et al, 2011 ; Drummond et al, 2008 ; Fyfe et al, 2016 ; Ogasawara et al, 2016 ; Telles et al, 2021 ; Russell et al, 2013 ; Rivas et al, 2014 ; Olsen et al, 2006 ) and bloodstream ( Banzet et al, 2013 ; Baggish et al, 2014 ; Gomes et al, 2014 ; Nielsen et al, 2014 ) following distinct exercise intervention modes. Interestingly, some of these miRNAs may hamper tumor development, progression, and metastasis ( Si et al, 2007 ; Zhu et al, 2008 ; Cui et al, 2013 ).…”

“…Those factors are known as myokines, a group of molecules (e.g, protein/peptides, metabolites and different species of RNAs) that regulates key cellular processes, such as cell proliferation, metabolism, and signal transduction, acting as important mediators of the systemic effects of exercise training ( Safdar et al, 2009 ; Pedersen and Febbraio, 2012 ; Hawley et al, 2014 ; Dethlefsen et al, 2016 ; Safdar et al, 2016 ; Dethlefsen et al, 2017a ; Dethlefsen et al, 2017b ; Ruiz-Casado et al, 2017 ; Safdar and Tarnopolsky, 2018 ). Among the myokines, the microRNAs (miRNAs) have been deemed as important molecules as they regulate cellular activity at the post-transcriptional level through mRNA degradation, destabilization, or repression of gene translation ( Safdar et al, 2016 ; Ha and Kim, 2014 ; Huntzinger and Izaurralde, 2011 ; Alizadeh et al, 2019 ; Camera et al, 2016 ; D'Souza et al, 2017 ; Davidsen et al, 2011 ; Drummond et al, 2008 ; Fyfe et al, 2016 ; Mooren et al, 2014 ; Nielsen et al, 2010 ; Ogasawara et al, 2016 ; Telles et al, 2021 ). In fact, miRNAs are a class of small (∼22 nucleotides) non-coding RNAs that can be produced in different tissues (e.g., skeletal muscle, adipose tissue) and released to the bloodstream (i.e., circulating miRNAs: c-miRNAs) ( Safdar et al, 2016 ; Safdar and Tarnopolsky, 2018 ; Alizadeh et al, 2019 ; D'Souza et al, 2017 ; Davidsen et al, 2011 ; Drummond et al, 2008 ; Fyfe et al, 2016 ; Nielsen et al, 2010 ; Ogasawara et al, 2016 ) usually associated with different proteins and lipoprotein complexes (e.g., protein argonaute-2, high- and low-density lipoproteins or inserted in extracellular vesicles) ( Safdar et al, 2016 ; Dufresne et al, 2018 ; Safdar and Tarnopolsky, 2018 ).…”

Bone-Regulating MicroRNAs and Resistance Exercise: A Mini-Review

“…Telles et al [31] compared skeletal muscle miRNA responses in young men to three types of acute exercise protocols; resistance exercise, high-intensity interval exercise, and both resistance and high-intensity interval exercise performed concurrently. They used a targeted approach for the miRNA analysis, selecting 8 miRNAs with known regulatory roles in skeletal muscle development.…”