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Acute and long-term exercise adaptation of adipose tissue and skeletal muscle in humans: a matched transcriptomics approach after 8-week training-intervention

BACKGROUND: Exercise exerts many health benefits by directly inducing molecular alterations in physically utilized skeletal muscle. Molecular adaptations of subcutaneous adipose tissue (SCAT) might also contribute to the prevention of metabolic diseases. AIM: To characterize the response of human SC...

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Autores principales: Dreher, Simon I., Irmler, Martin, Pivovarova-Ramich, Olga, Kessler, Katharina, Jürchott, Karsten, Sticht, Carsten, Fritsche, Louise, Schneeweiss, Patrick, Machann, Jürgen, Pfeiffer, Andreas F. H., Hrabě de Angelis, Martin, Beckers, Johannes, Birkenfeld, Andreas L., Peter, Andreas, Niess, Andreas M., Weigert, Cora, Moller, Anja
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10113153/
https://www.ncbi.nlm.nih.gov/pubmed/36774413
http://dx.doi.org/10.1038/s41366-023-01271-y
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author Dreher, Simon I.
Irmler, Martin
Pivovarova-Ramich, Olga
Kessler, Katharina
Jürchott, Karsten
Sticht, Carsten
Fritsche, Louise
Schneeweiss, Patrick
Machann, Jürgen
Pfeiffer, Andreas F. H.
Hrabě de Angelis, Martin
Beckers, Johannes
Birkenfeld, Andreas L.
Peter, Andreas
Niess, Andreas M.
Weigert, Cora
Moller, Anja
author_facet Dreher, Simon I.
Irmler, Martin
Pivovarova-Ramich, Olga
Kessler, Katharina
Jürchott, Karsten
Sticht, Carsten
Fritsche, Louise
Schneeweiss, Patrick
Machann, Jürgen
Pfeiffer, Andreas F. H.
Hrabě de Angelis, Martin
Beckers, Johannes
Birkenfeld, Andreas L.
Peter, Andreas
Niess, Andreas M.
Weigert, Cora
Moller, Anja
author_sort Dreher, Simon I.
collection PubMed
description BACKGROUND: Exercise exerts many health benefits by directly inducing molecular alterations in physically utilized skeletal muscle. Molecular adaptations of subcutaneous adipose tissue (SCAT) might also contribute to the prevention of metabolic diseases. AIM: To characterize the response of human SCAT based on changes in transcripts and mitochondrial respiration to acute and repeated bouts of exercise in comparison to skeletal muscle. METHODS: Sedentary participants (27 ± 4 yrs) with overweight or obesity underwent 8-week supervised endurance exercise 3×1h/week at 80% VO2peak. Before, 60 min after the first and last exercise bout and 5 days post intervention, biopsies were taken for transcriptomic analyses and high-resolution respirometry (n = 14, 8 female/6 male). RESULTS: In SCAT, we found 37 acutely regulated transcripts (FC > 1.2, FDR < 10%) after the first exercise bout compared to 394, respectively, in skeletal muscle. Regulation of only 5 transcripts overlapped between tissues highlighting their differential response. Upstream and enrichment analyses revealed reduced transcripts of lipid uptake, storage and lipogenesis directly after exercise in SCAT and point to β-adrenergic regulation as potential major driver. The data also suggest an exercise-induced modulation of the circadian clock in SCAT. Neither term was associated with transcriptomic changes in skeletal muscle. No evidence for beigeing/browning was found in SCAT along with unchanged respiration. CONCLUSIONS: Adipose tissue responds completely distinct from adaptations of skeletal muscle to exercise. The acute and repeated reduction in transcripts of lipid storage and lipogenesis, interconnected with a modulated circadian rhythm, can counteract metabolic syndrome progression toward diabetes.
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spelling pubmed-101131532023-04-20 Acute and long-term exercise adaptation of adipose tissue and skeletal muscle in humans: a matched transcriptomics approach after 8-week training-intervention Dreher, Simon I. Irmler, Martin Pivovarova-Ramich, Olga Kessler, Katharina Jürchott, Karsten Sticht, Carsten Fritsche, Louise Schneeweiss, Patrick Machann, Jürgen Pfeiffer, Andreas F. H. Hrabě de Angelis, Martin Beckers, Johannes Birkenfeld, Andreas L. Peter, Andreas Niess, Andreas M. Weigert, Cora Moller, Anja Int J Obes (Lond) Article BACKGROUND: Exercise exerts many health benefits by directly inducing molecular alterations in physically utilized skeletal muscle. Molecular adaptations of subcutaneous adipose tissue (SCAT) might also contribute to the prevention of metabolic diseases. AIM: To characterize the response of human SCAT based on changes in transcripts and mitochondrial respiration to acute and repeated bouts of exercise in comparison to skeletal muscle. METHODS: Sedentary participants (27 ± 4 yrs) with overweight or obesity underwent 8-week supervised endurance exercise 3×1h/week at 80% VO2peak. Before, 60 min after the first and last exercise bout and 5 days post intervention, biopsies were taken for transcriptomic analyses and high-resolution respirometry (n = 14, 8 female/6 male). RESULTS: In SCAT, we found 37 acutely regulated transcripts (FC > 1.2, FDR < 10%) after the first exercise bout compared to 394, respectively, in skeletal muscle. Regulation of only 5 transcripts overlapped between tissues highlighting their differential response. Upstream and enrichment analyses revealed reduced transcripts of lipid uptake, storage and lipogenesis directly after exercise in SCAT and point to β-adrenergic regulation as potential major driver. The data also suggest an exercise-induced modulation of the circadian clock in SCAT. Neither term was associated with transcriptomic changes in skeletal muscle. No evidence for beigeing/browning was found in SCAT along with unchanged respiration. CONCLUSIONS: Adipose tissue responds completely distinct from adaptations of skeletal muscle to exercise. The acute and repeated reduction in transcripts of lipid storage and lipogenesis, interconnected with a modulated circadian rhythm, can counteract metabolic syndrome progression toward diabetes. Nature Publishing Group UK 2023-02-11 2023 /pmc/articles/PMC10113153/ /pubmed/36774413 http://dx.doi.org/10.1038/s41366-023-01271-y Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Dreher, Simon I.
Irmler, Martin
Pivovarova-Ramich, Olga
Kessler, Katharina
Jürchott, Karsten
Sticht, Carsten
Fritsche, Louise
Schneeweiss, Patrick
Machann, Jürgen
Pfeiffer, Andreas F. H.
Hrabě de Angelis, Martin
Beckers, Johannes
Birkenfeld, Andreas L.
Peter, Andreas
Niess, Andreas M.
Weigert, Cora
Moller, Anja
Acute and long-term exercise adaptation of adipose tissue and skeletal muscle in humans: a matched transcriptomics approach after 8-week training-intervention
title Acute and long-term exercise adaptation of adipose tissue and skeletal muscle in humans: a matched transcriptomics approach after 8-week training-intervention
title_full Acute and long-term exercise adaptation of adipose tissue and skeletal muscle in humans: a matched transcriptomics approach after 8-week training-intervention
title_fullStr Acute and long-term exercise adaptation of adipose tissue and skeletal muscle in humans: a matched transcriptomics approach after 8-week training-intervention
title_full_unstemmed Acute and long-term exercise adaptation of adipose tissue and skeletal muscle in humans: a matched transcriptomics approach after 8-week training-intervention
title_short Acute and long-term exercise adaptation of adipose tissue and skeletal muscle in humans: a matched transcriptomics approach after 8-week training-intervention
title_sort acute and long-term exercise adaptation of adipose tissue and skeletal muscle in humans: a matched transcriptomics approach after 8-week training-intervention
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10113153/
https://www.ncbi.nlm.nih.gov/pubmed/36774413
http://dx.doi.org/10.1038/s41366-023-01271-y
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