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BMC genomics2017; 18(1); 595; doi: 10.1186/s12864-017-4007-9

Equine skeletal muscle adaptations to exercise and training: evidence of differential regulation of autophagosomal and mitochondrial components.

Abstract: A single bout of exercise induces changes in gene expression in skeletal muscle. Regular exercise results in an adaptive response involving changes in muscle architecture and biochemistry, and is an effective way to manage and prevent common human diseases such as obesity, cardiovascular disorders and type II diabetes. However, the biomolecular mechanisms underlying such responses still need to be fully elucidated. Here we performed a transcriptome-wide analysis of skeletal muscle tissue in a large cohort of untrained Thoroughbred horses (n = 51) before and after a bout of high-intensity exercise and again after an extended period of training. We hypothesized that regular high-intensity exercise training primes the transcriptome for the demands of high-intensity exercise. An extensive set of genes was observed to be significantly differentially regulated in response to a single bout of high-intensity exercise in the untrained cohort (3241 genes) and following multiple bouts of high-intensity exercise training over a six-month period (3405 genes). Approximately one-third of these genes (1025) and several biological processes related to energy metabolism were common to both the exercise and training responses. We then developed a novel network-based computational analysis pipeline to test the hypothesis that these transcriptional changes also influence the contextual molecular interactome and its dynamics in response to exercise and training. The contextual network analysis identified several important hub genes, including the autophagosomal-related gene GABARAPL1, and dynamic functional modules, including those enriched for mitochondrial respiratory chain complexes I and V, that were differentially regulated and had their putative interactions 're-wired' in the exercise and/or training responses. Here we have generated for the first time, a comprehensive set of genes that are differentially expressed in Thoroughbred skeletal muscle in response to both exercise and training. These data indicate that consecutive bouts of high-intensity exercise result in a priming of the skeletal muscle transcriptome for the demands of the next exercise bout. Furthermore, this may also lead to an extensive 're-wiring' of the molecular interactome in both exercise and training and include key genes and functional modules related to autophagy and the mitochondrion.
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Publication Date: 2017-08-09 PubMed ID: 28793853PubMed Central: PMC5551008DOI: 10.1186/s12864-017-4007-9Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research investigates genetic responses in horse muscles to high-intensity exercise. It shows that such exercise and regular training significantly alter the expression of thousands of genes, some of which relate to energy metabolism, and that these changes may affect the molecular interactions within the muscles.

Objective of the Research

The research aimed to explore the biomolecular mechanisms at play in skeletal muscles when subjected to intense exercise and training. The hypothesis was that high-intensity exercise training prepares or “primes” the transcriptome (the total of all types of transcripts including mRNAs, non-coding RNAs, and small RNAs) to meet the demands of similar intensive exercises.

Research Methodology

  • A cohort of 51 untrained Thoroughbred horses was involved in the study.
  • The horses’ skeletal muscle tissues were examined before and after a single bout of high-intensity exercise and after a period of sustained training.
  • A transcriptome-wide analysis was undertaken to monitor changes in gene expression levels.
  • A custom network-based computational analysis pipeline was developed to investigate how these transcriptional changes influence the molecular interactome (the whole set of molecular interactions in cells) and its dynamics.

Research Findings

  • High-intensity exercise and repeated bouts of such exercise through training significantly affect gene regulation, with changes observed in 3241 genes after a single exercise session, and in 3405 genes after a six-month training period.
  • Approximately a third of these changing genes, roughly 1025, and a number of biological processes related to energy metabolism, were common to both single and multiple exercise bouts.
  • The network analysis revealed key genes and functional components related to autophagy (the body’s way of cleaning out damaged cells) and mitochondrial function that underwent changes in their interactions during exercise and training.

Conclusion

The research concludes that repeated high-intensity exercise primes the skeletal muscle transcriptome for subsequent bouts of exercise. This priming also leads to extensive rearrangement or ‘re-wiring’ of molecular interactions, affecting key genes and functions related to autophagy and the mitochondrion. This extensive list of genes that are altered in their expression due to exercise and training can help in further understanding of how muscle tissues adapt to physical stress and generate energy.

Cite This Article

APA
Bryan K, McGivney BA, Farries G, McGettigan PA, McGivney CL, Gough KF, MacHugh DE, Katz LM, Hill EW. (2017). Equine skeletal muscle adaptations to exercise and training: evidence of differential regulation of autophagosomal and mitochondrial components. BMC Genomics, 18(1), 595. https://doi.org/10.1186/s12864-017-4007-9

Publication

BMC genomics
ISSN: 1471-2164
NlmUniqueID: 100965258
Country: England
Language: English
Volume: 18
Issue: 1
Pages: 595
PII: 595

Researcher Affiliations

Bryan, Kenneth
  • UCD School of Agriculture and Food Science, University College Dublin, Belfield, D04 V1W8, Ireland.
McGivney, Beatrice A
  • UCD School of Agriculture and Food Science, University College Dublin, Belfield, D04 V1W8, Ireland.
Farries, Gabriella
  • UCD School of Agriculture and Food Science, University College Dublin, Belfield, D04 V1W8, Ireland.
McGettigan, Paul A
  • UCD School of Agriculture and Food Science, University College Dublin, Belfield, D04 V1W8, Ireland.
McGivney, Charlotte L
  • UCD School of Agriculture and Food Science, University College Dublin, Belfield, D04 V1W8, Ireland.
Gough, Katie F
  • UCD School of Agriculture and Food Science, University College Dublin, Belfield, D04 V1W8, Ireland.
MacHugh, David E
  • UCD School of Agriculture and Food Science, University College Dublin, Belfield, D04 V1W8, Ireland.
  • UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Belfield, D04 V1W8, Ireland.
Katz, Lisa M
  • UCD School of Veterinary Medicine, University College Dublin, Belfield, D04 V1W8, Ireland.
Hill, Emmeline W
  • UCD School of Agriculture and Food Science, University College Dublin, Belfield, D04 V1W8, Ireland. emmeline.hill@ucd.ie.

MeSH Terms

  • Adaptation, Physiological
  • Animals
  • Autophagosomes / metabolism
  • Gene Expression Profiling
  • Horses
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • Muscle, Skeletal / cytology
  • Muscle, Skeletal / physiology
  • Physical Conditioning, Animal / physiology
  • Sequence Analysis, RNA

Conflict of Interest Statement

CONSENT FOR PUBLICATION: All authors read and approved the final manuscript COMPETING INTERESTS: None of the authors has any financial or personal relationships that could inappropriately influence or bias the content of the paper. EWH and DEM are shareholders in Plusvital Ltd., an equine nutrition and genetic testing company. Plusvital Ltd. has been granted a license for commercial use of data contained within patent applications: United States Provisional Serial Number 61/136553 and Irish patent application number 2008/0735, Patent Cooperation Treaty filing: A method for predicting athletic performance potential, September 7, 2009. EWH, DEM and LMK are named on the applications. The patent contents are not related to this manuscript. Plusvital Ltd. had no part in the research in the manuscript. PUBLISHER’S NOTE: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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