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Empagliflozin induces the transcriptional program for nutrient homeostasis in skeletal muscle in normal mice

Sodium-glucose cotransporter 2 inhibitors (SGLT2i) improve heart failure (HF) outcomes across a range of patient characteristics. A hypothesis that SGLT2i induce metabolic change similar to fasting has recently been proposed to explain their profound clinical benefits. However, it remains unclear wh...

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Autores principales: Kawakami, Ryo, Matsui, Hiroki, Matsui, Miki, Iso, Tatsuya, Yokoyama, Tomoyuki, Ishii, Hideki, Kurabayashi, Masahiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10590450/
https://www.ncbi.nlm.nih.gov/pubmed/37865720
http://dx.doi.org/10.1038/s41598-023-45390-y
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author Kawakami, Ryo
Matsui, Hiroki
Matsui, Miki
Iso, Tatsuya
Yokoyama, Tomoyuki
Ishii, Hideki
Kurabayashi, Masahiko
author_facet Kawakami, Ryo
Matsui, Hiroki
Matsui, Miki
Iso, Tatsuya
Yokoyama, Tomoyuki
Ishii, Hideki
Kurabayashi, Masahiko
author_sort Kawakami, Ryo
collection PubMed
description Sodium-glucose cotransporter 2 inhibitors (SGLT2i) improve heart failure (HF) outcomes across a range of patient characteristics. A hypothesis that SGLT2i induce metabolic change similar to fasting has recently been proposed to explain their profound clinical benefits. However, it remains unclear whether SGLT2i primarily induce this change in physiological settings. Here, we demonstrate that empagliflozin administration under ad libitum feeding did not cause weight loss but did increase transcripts of the key nutrient sensors, AMP-activated protein kinase and nicotinamide phosphoribosyltransferase, and the master regulator of mitochondrial gene expression, PGC-1α, in quadriceps muscle in healthy mice. Expression of these genes correlated with that of PPARα and PPARδ target genes related to mitochondrial metabolism and oxidative stress response, and also correlated with serum ketone body β-hydroxybutyrate. These results were not observed in the heart. Collectively, this study revealed that empagliflozin activates transcriptional programs critical for sensing and adaptation to nutrient availability intrinsic to skeletal muscle rather than the heart even in normocaloric condition. As activation of PGC-1α is sufficient for metabolic switch from fatigable, glycolytic metabolism toward fatigue-resistant, oxidative mechanism in skeletal muscle myofibers, our findings may partly explain the improvement of exercise tolerance in patients with HF receiving empagliflozin.
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spelling pubmed-105904502023-10-23 Empagliflozin induces the transcriptional program for nutrient homeostasis in skeletal muscle in normal mice Kawakami, Ryo Matsui, Hiroki Matsui, Miki Iso, Tatsuya Yokoyama, Tomoyuki Ishii, Hideki Kurabayashi, Masahiko Sci Rep Article Sodium-glucose cotransporter 2 inhibitors (SGLT2i) improve heart failure (HF) outcomes across a range of patient characteristics. A hypothesis that SGLT2i induce metabolic change similar to fasting has recently been proposed to explain their profound clinical benefits. However, it remains unclear whether SGLT2i primarily induce this change in physiological settings. Here, we demonstrate that empagliflozin administration under ad libitum feeding did not cause weight loss but did increase transcripts of the key nutrient sensors, AMP-activated protein kinase and nicotinamide phosphoribosyltransferase, and the master regulator of mitochondrial gene expression, PGC-1α, in quadriceps muscle in healthy mice. Expression of these genes correlated with that of PPARα and PPARδ target genes related to mitochondrial metabolism and oxidative stress response, and also correlated with serum ketone body β-hydroxybutyrate. These results were not observed in the heart. Collectively, this study revealed that empagliflozin activates transcriptional programs critical for sensing and adaptation to nutrient availability intrinsic to skeletal muscle rather than the heart even in normocaloric condition. As activation of PGC-1α is sufficient for metabolic switch from fatigable, glycolytic metabolism toward fatigue-resistant, oxidative mechanism in skeletal muscle myofibers, our findings may partly explain the improvement of exercise tolerance in patients with HF receiving empagliflozin. Nature Publishing Group UK 2023-10-21 /pmc/articles/PMC10590450/ /pubmed/37865720 http://dx.doi.org/10.1038/s41598-023-45390-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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Kawakami, Ryo
Matsui, Hiroki
Matsui, Miki
Iso, Tatsuya
Yokoyama, Tomoyuki
Ishii, Hideki
Kurabayashi, Masahiko
Empagliflozin induces the transcriptional program for nutrient homeostasis in skeletal muscle in normal mice
title Empagliflozin induces the transcriptional program for nutrient homeostasis in skeletal muscle in normal mice
title_full Empagliflozin induces the transcriptional program for nutrient homeostasis in skeletal muscle in normal mice
title_fullStr Empagliflozin induces the transcriptional program for nutrient homeostasis in skeletal muscle in normal mice
title_full_unstemmed Empagliflozin induces the transcriptional program for nutrient homeostasis in skeletal muscle in normal mice
title_short Empagliflozin induces the transcriptional program for nutrient homeostasis in skeletal muscle in normal mice
title_sort empagliflozin induces the transcriptional program for nutrient homeostasis in skeletal muscle in normal mice
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10590450/
https://www.ncbi.nlm.nih.gov/pubmed/37865720
http://dx.doi.org/10.1038/s41598-023-45390-y
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