Influence of physical exercise on microRNAs in skeletal muscle regeneration, aging and diseases

Ultimo, Simona; Zauli, Giorgio; Martelli, Alberto M.; Vitale, Marco; McCubrey, James A.; Capitani, Silvano; Neri, Luca M.

doi:10.18632/oncotarget.24991

Cited by 52 publications

(32 citation statements)

References 147 publications

(187 reference statements)

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“…But then again, reproducibility in exercise biomarker studies appears relatively low throughout literature. Many different microRNAs, as well as many different cytokines have been reported to associate with various forms of exercise over the years ( Ultimo et al, 2018 ). One explanation could be that different forms and intensities of exercise can have profoundly different physiological effects.…”

Section: Discussionmentioning

confidence: 99%

Circulating Small Non-coding RNAs as Biomarkers for Recovery After Exhaustive or Repetitive Exercise

et al. 2018

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Circulating microRNAs have proven to be reliable biomarkers, due to their high stability, both in vivo in the circulation, and ex vivo during sample preparation and storage. Small nucleolar RNAs (snoRNAs) are a different type of small non-coding RNAs that can also be reliably measured in plasma, but have only been studied sporadically. In this study, we aimed to identify RNA-biomarkers that can distinguish between different exercise regimes and that entail clues about muscle repair and recovery after prolonged exhaustive endurance exercise. We compared plasma microRNA profiles between two cohorts of elite cyclists, subjected to two different types of exercise regimes, as well as a cohort of patients with peripheral artery disease (PAD) that were scheduled to undergo lower limb amputation, due to critical limb ischemia. In elite athletes, muscle tissue recovers quickly even after exhaustive exercise, whereas in PAD patients, recovery is completely impaired. Furthermore, we measured levels of a specific group of snoRNAs in the plasma of both elite cyclists and PAD patients. Using a multiplex qPCR screening, we detected a total of 179 microRNAs overall, of which, on average, 161 microRNAs were detected per sample. However, only 30 microRNAs were consistently expressed in all samples. Of these, two microRNAs, miR-29a-3p and miR193a-5p, that responded differently two different types of exercise, namely exhaustive exercise and non-exhaustive endurance exercise. Using individual rt/qPCR, we also identified a snoRNA, SNORD114.1, which was significantly upregulated in plasma in response to endurance exercise. Furthermore, two microRNAs, miR-29a-3p and miR-495-3p, were significantly differentially expressed in athletes compared to PAD patients, but only following exercise. We suggest that these two microRNAs could function as markers of impaired muscle repair and recovery. In conclusion, microRNAs miR-29a-3p and miR-193a-5p may help us distinguish between repeated exhaustive and non-exhaustive endurance exercise. MicroRNA miR-29a-3p, as well as miR-495-3p, may further mark impaired muscle recovery in patients with severe critical limb ischemia. Furthermore, we showed for the first time that a circulating snoRNA, SNORD114.1, is regulated in response to exercise and may be used as biomarker.

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Section: Discussionmentioning

confidence: 99%

Circulating Small Non-coding RNAs as Biomarkers for Recovery After Exhaustive or Repetitive Exercise

et al. 2018

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“…All these pro-inflammatory stimuli and growth factors can lead to the alteration of key cellular processes and signaling transduction pathways like MAPKs and PI3K/Akt pathways, prompting the malignant transformation of cells [23,24]. Beyond these molecular changes that alter cellular homeostasis, dietary and environmental factors are also able to induce epigenetic modifications including changes in microRNA (miRNA) expression or in genetic methylation status [25][26][27][28].…”

Section: Introductionmentioning

confidence: 99%

Identification of Modulated MicroRNAs Associated with Breast Cancer, Diet, and Physical Activity

Falzone

Grimaldi

Celentano

et al. 2020

Cancers

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Background: Several studies have shown that healthy lifestyles prevent the risk of breast cancer (BC) and are associated with better prognosis. It was hypothesized that lifestyle strategies induce microRNA (miRNA) modulation that, in turn, may lead to important epigenetic modifications. The identification of miRNAs associated with BC, diet, and physical activity may give further insights into the role played by lifestyle interventions and their efficacy for BC patients. To predict which miRNAs may be modulated by diet and physical activity in BC patients, the analyses of different miRNA expression datasets were performed. Methods: The GEO DataSets database was used to select miRNA expression datasets related to BC patients, dietary interventions, and physical exercise. Further bioinformatic approaches were used to establish the value of selected miRNAs in BC development and prognosis. Results: The analysis of datasets allowed the selection of modulated miRNAs associated with BC development, diet, and physical exercise. Seven miRNAs were also associated with the overall survival of BC patients. Conclusions: The identified miRNAs may play a role in the development of BC and may have a prognostic value in patients treated with integrative interventions including diet and physical activity. Validation of such modulated miRNAs on BC patients undergoing lifestyle strategies will be mandatory.

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“…Overall, effects on genes encoding components of the miRNA processing machinery were minor. Furthermore, we did not find major differences with regard to concentrations of a broad variety of individual miRNAs species that we analyzed based on literature data (Kirby and McCarthy, 2013; Meurer et al., 2016; Russell and Lamon, 2015; Silva et al., 2017; Silva et al., 2020; Sjögren et al., 2018; Ultimo et al., 2018; Widmann et al., 2019; cf. Table 2) (Figure 8 and data not shown).…”

Section: Resultsmentioning

confidence: 77%

Skeletal muscle effects of two different 10‐week exercise regimens, voluntary wheel running, and forced treadmill running, in mice: A pilot study

Schmitt¹,

Herzog²,

Röchner³

et al. 2020

Physiol Rep

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Physical activity and exercise induce a complex pattern of adaptation reactions in a broad variety of tissues and organs, particularly the cardiovascular and the musculoskeletal systems. The underlying mechanisms, however, specifically the molecular changes that occur in response to training, are still incompletely understood. Animal models help to systematically elucidate the mechanisms of exercise adaptation. With regard to endurance‐based running exercise in mice, two basic regimens have been established: forced treadmill running (FTR), usually consisting of several sessions per week, and voluntary wheel running (VWR). However, the effects of these two programs on skeletal muscle molecular adaptation patterns have never been directly compared. To address this issue, in a pilot study, we analyzed the effects of two ten‐week training regimens in juvenile, male, C57BL/6 mice: moderate‐intensity forced treadmill running three‐times‐a‐week, employing a protocol that has been widely used in similar studies before, and voluntary wheel running. Our data suggest that there are similarities, but also characteristic differences in the molecular responses of different skeletal muscle species to the two training regimens. In particular, we found that VWR induces a significant fiber type shift toward more type IIX fibers in the slow, oxidative soleus muscle ( p = .0053), but not in the other three muscles analyzed. In addition, while training‐induced expression patterns of the two metabolic markers Ppargc1a, encoding Pgc‐1α (peroxisome proliferator‐activated receptor gamma coactivator 1‐alpha) and Nr4a3 (nuclear receptor subfamily 4 group A member 3) were roughly similar, downregulation of the Mstn (myostatin) gene and the “atrogene” Fbox32 could only be observed in response to VWR in specific muscles, such as in the gastrocnemius ( p = .0015 for Mstn ) and in the tibialis anterior ( p = .0053 for Fbox32 ) muscles, suggesting that molecular adaptation reactions to the two training regimens show distinct characteristics.

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Influence of physical exercise on microRNAs in skeletal muscle regeneration, aging and diseases

Cited by 52 publications

References 147 publications

Circulating Small Non-coding RNAs as Biomarkers for Recovery After Exhaustive or Repetitive Exercise

Circulating Small Non-coding RNAs as Biomarkers for Recovery After Exhaustive or Repetitive Exercise

Identification of Modulated MicroRNAs Associated with Breast Cancer, Diet, and Physical Activity

Skeletal muscle effects of two different 10‐week exercise regimens, voluntary wheel running, and forced treadmill running, in mice: A pilot study

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