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Metabolites
Special Issues
Muscle Metabolic Response and Adaptation to Exercise, Diet, and Environment
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Muscle Metabolic Response and Adaptation to Exercise, Diet, and Environment

A special issue of Metabolites (ISSN 2218-1989). This special issue belongs to the section "Animal Metabolism".

Deadline for manuscript submissions: 30 August 2025 | Viewed by 6202

Special Issue Editor

Dr. Susumu Muroya

E-Mail Website
Guest Editor
NARO Institute of Livestock and Grassland Science, Tsukuba, Ibaraki, Japan
Interests: muscle biology; meat biochemistry; epigenetics; metabolomics; animal science

Special Issue Information

Dear Colleagues,

Skeletal muscle plays a crucial role as a locomotor organ and as a modulator of systemic energy homeostasis in animals. Dysregulation of muscle metabolism in humans leads to the development of serious diseases such as diabetes and sarcopenia. In farm animals, excessive pursuit of productivity sometimes causes disruption of energy homeostasis as exhibited in undesirable products such as abnormal chicken meat quality derived from disturbed mitophagy and/or redox metabolism. The optimized muscle metabolism is important for an increase in muscle mass during animal development and growth. Therefore, a better understanding of mechanisms underlying developmental regulation of metabolisms and adaptation of skeletal muscle metabolism to various inputs including diet, exercise, and environment stress contributes to further improvement of human health, animal welfare and productivity, and meat quality.

Recent metabolomics technologies, in combination with the development of bioinformatics and imaging mass spectrometry, has provided great benefits in the approach to unexplored muscle metabolisms. With these backgrounds, this Special Issue aims to share and discuss research topics focusing on molecular mechanisms of the metabolic response of skeletal muscle tissue and cells in the view of genes, transcripts, proteins, metabolites, and epigenetic factors, when exposed to various nutritional conditions and physiological stress-inducing environments. Papers addressing mechanisms of metabolic adaptation and disturbance, especially in terms of mitochondria, energy homeostasis, lipid metabolism, and redox metabolism, including cell culture studies, could be the desired topics in this issue. Meanwhile, other studies regarding skeletal muscle growth, maturation, aging, disease, and farm animal intramuscular fat and postmortem muscle aging are also welcome. Most of these studies may be conducted by use of metabolomics and integrative multi-omics approaches, but also cutting-edge studies targeting a specific key metabolite and inter-organ crosstalk around muscle in the above-mentioned fields are also acceptable.

Dr. Susumu Muroya
Guest Editor

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Metabolites is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • skeletal muscle
  • metabolomics
  • mitochondria
  • energy metabolism
  • lipid metabolism
  • nutrition
  • feeding
  • environment
  • exercise
  • stress

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Published Papers (2 papers)

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Research

18 pages, 5035 KiB  
Article
Depth of Interbreed Difference in Postmortem Bovine Muscle Determined by CE-FT/MS and LC-FT/MS Metabolomics
by Susumu Muroya, Yuta Horiuchi, Kazuki Iguchi, Takuma Higuchi, Shuji Sakamoto, Koichi Ojima and Kazutsugu Matsukawa
Metabolites 2024, 14(5), 261; https://doi.org/10.3390/metabo14050261 - 1 May 2024
Viewed by 1824
Abstract
Japanese Brown (JBR) cattle have moderately marbled beef compared to the highly marbled beef of Japanese Black (JBL) cattle; however, their skeletal muscle properties remain poorly characterized. To unveil interbreed metabolic differences over the previous results, we explored the metabolome network changes before [...] Read more.
Japanese Brown (JBR) cattle have moderately marbled beef compared to the highly marbled beef of Japanese Black (JBL) cattle; however, their skeletal muscle properties remain poorly characterized. To unveil interbreed metabolic differences over the previous results, we explored the metabolome network changes before and after postmortem 7-day aging in the trapezius muscle of the two cattle breeds by employing a deep and high-coverage metabolomics approach. Using both capillary electrophoresis (CE) and ultra-high-performance liquid chromatography (UHPLC)–Fourier transform mass spectrometry (FT/MS), we detected 522 and 384 annotated peaks, respectively, across all muscle samples. The CE-based results showed that the cattle were clearly separated by breed and postmortem age in multivariate analyses. The metabolism related to glutathione, glycolysis, vitamin K, taurine, and arachidonic acid was enriched with differentially abundant metabolites in aged muscles, in addition to amino acid (AA) metabolisms. The LC-based results showed that the levels of bile-acid-related metabolites, such as tauroursodeoxycholic acid (TUDCA), were high in fresh JBR muscle and that acylcarnitines were enriched in aged JBR muscle, compared to JBL muscle. Postmortem aging resulted in an increase in fatty acids and a decrease in acylcarnitine in the muscles of both cattle breeds. In addition, metabolite set enrichment analysis revealed that JBR muscle was distinctive in metabolisms related to pyruvate, glycerolipid, cardiolipin, and mitochondrial energy production, whereas the metabolisms related to phosphatidylethanolamine, nucleotide triphosphate, and AAs were characteristic of JBL. This suggests that the interbreed differences in postmortem trapezius muscle are associated with carnitine/acylcarnitine transport, β-oxidation, tricarboxylic acid cycle, and mitochondrial membrane stability, in addition to energy substrate and AA metabolisms. These interbreed differences may characterize beef quality traits such as the flavor intensity and oxidative stability. Full article
(This article belongs to the Special Issue Muscle Metabolic Response and Adaptation to Exercise, Diet, and Environment)
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Figure 1

Figure 1
<p>Hierarchical clustering analysis (<b>A</b>) and principal component analysis (PCA) (<b>B</b>) results using CE-FT/MS metabolomics profiles in the postmortem <span class="html-italic">trapezius</span> muscle of Japanese Brown (JBR; JBR1-3) and Japanese Black (JBL; JBL1-3) cattle. The muscle samples at a specific time point (day 0 and 7) were allocated to each breed. (<b>A</b>) In the heatmap, the row displays the metabolite, and the column represents the sample. Metabolites with relatively low and high levels are displayed in light blue and brown, respectively. The brightness of each color corresponds to the magnitude of the difference when compared to the average value. (<b>B</b>) In the PCA score plot, the muscle samples of day 0 (circle) and day 7 (triangle) are indicated for JBR (green) and JBL (red) cattle.</p> Full article ">Figure 2
<p>PCA score plots of CE-FT/MS metabolomics data of the <span class="html-italic">trapezius</span> muscle of JBR (in green) and JBL (in red) cattle on day 0 (<b>A</b>) and day 7 (<b>B</b>).</p> Full article ">Figure 3
<p>Volcano plot of CE-FT/MS metabolomics results of the <span class="html-italic">trapezius</span> muscle of JBR and JBL cattle on day 0 (<b>A</b>) and day 7 (<b>B</b>). The metabolites highly contributing to JBR and JBL (fold change &gt; 1.5, <span class="html-italic">p</span> &lt; 0.10) are indicated.</p> Full article ">Figure 4
<p>MSEA results for the metabolomic difference between JBR and JBL on day 0 (<b>A</b>) and 7 (<b>B</b>) postmortem. Enrichment ratio is computed by (observed hits)/(expected hits). Different metabolisms between the days at <span class="html-italic">p</span> &lt; 0.05 are indicated in light red.</p> Full article ">Figure 5
<p>PCA score plots of LC-FT/MS metabolomics data of the <span class="html-italic">trapezius</span> muscle of JBR (in green) and JBL (in red) cattle on day 0 (<b>A</b>) and day 7 (<b>B</b>).</p> Full article ">Figure 6
<p>Volcano plot of LC-FT/MS metabolomics results of the <span class="html-italic">trapezius</span> muscle of JBR and JBL cattle on day 0 (<b>A</b>) and day 7 (<b>B</b>). The metabolites highly contributing to JBR and JBL (fold change &gt; 1.5, <span class="html-italic">p</span> &lt; 0.10) are indicated.</p> Full article ">Figure 7
<p>Result of MSEA for metabolomic differences between days 0 and 7 postmortem in JBR (<b>A</b>) and JBL (<b>B</b>) cattle. Enrichment ratio is computed by (observed hits)/(expected hits). The different metabolisms between the two breeds are indicated in light red.</p> Full article ">Figure 8
<p>PCA score plots of LC-FT/MS metabolomics data of the <span class="html-italic">trapezius</span> muscle on day 0 (in red) and day 7 (in green) in JBR (<b>A</b>) and JBL (<b>B</b>) cattle.</p> Full article ">Figure 9
<p>Volcano plot of LC-FT/MS metabolomics results of the <span class="html-italic">trapezius</span> muscle of JBR (<b>A</b>) and JBL (<b>B</b>) cattle. The metabolites highly contributing to day 0 and day 7 (fold change &gt; 1.5, <span class="html-italic">p</span> &lt; 0.10) are indicated.</p> Full article ">Figure 10
<p>Hypothetical scheme of interbreed differences in the postmortem metabolism of the <span class="html-italic">trapezius</span> muscle between JBR and JBL cattle. The metabolites that differed between the JBR and JBL muscles on day 0 and day 7 are indicated in blue and red, respectively. ↑ and ↓ indicate a high and low level in JBR muscle compared to JBL muscle, respectively. VL; long and very long-chain FAs (VLCFAs), Cart; carnitine.</p> Full article ">
15 pages, 3475 KiB  
Article
Moderate Effects of Hypoxic Training at Low and Supramaximal Intensities on Skeletal Muscle Metabolic Gene Expression in Mice
by Svitlana Drozdovska, Nadège Zanou, Jessica Lavier, Lucia Mazzolai, Grégoire P. Millet and Maxime Pellegrin
Metabolites 2023, 13(10), 1103; https://doi.org/10.3390/metabo13101103 - 21 Oct 2023
Cited by 1 | Viewed by 3588
Abstract
The muscle molecular adaptations to different exercise intensities in combination with hypoxia are not well understood. This study investigated the effect of low- and supramaximal-intensity hypoxic training on muscle metabolic gene expression in mice. C57BL/6 mice were divided into two groups: sedentary and [...] Read more.
The muscle molecular adaptations to different exercise intensities in combination with hypoxia are not well understood. This study investigated the effect of low- and supramaximal-intensity hypoxic training on muscle metabolic gene expression in mice. C57BL/6 mice were divided into two groups: sedentary and training. Training consisted of 4 weeks at low or supramaximal intensity, either in normoxia or hypoxia (FiO2 = 0.13). The expression levels of genes involved in the hypoxia signaling pathway (Hif1a and Vegfa), the metabolism of glucose (Gys1, Glut4, Hk2, Pfk, and Pkm1), lactate (Ldha, Mct1, Mct4, Pdh, and Pdk4) and lipid (Cd36, Fabp3, Ucp2, Hsl, and Mcad), and mitochondrial energy metabolism and biogenesis (mtNd1, mtNd6, CytC, CytB, Pgc1a, Pgc1β, Nrf1, Tfam, and Cs) were determined in the gastrocnemius muscle. No physical performance improvement was observed between groups. In normoxia, supramaximal intensity training caused upregulation of major genes involved in the transport of glucose and lactate, fatty acid oxidation, and mitochondrial biogenesis, while low intensity training had a minor effect. The exposure to hypoxia changed the expression of some genes in the sedentary mice but had a moderate effect in trained mice compared to respective normoxic mice. In hypoxic groups, low-intensity training increased the mRNA levels of Mcad and Cs, while supramaximal intensity training decreased the mRNA levels of Mct1 and Mct4. The results indicate that hypoxic training, regardless of exercise intensity, has a moderate effect on muscle metabolic gene expression in healthy mice. Full article
(This article belongs to the Special Issue Muscle Metabolic Response and Adaptation to Exercise, Diet, and Environment)
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Figure 1

Figure 1
<p>Schematic illustration of the two training protocols. LIT-trained mice ran 40 min at 40% of maximal aerobic speed (MAS) (<b>A</b>). HIIT-trained mice ran 4 sets composed of 10 s sprints at 150% of MAS interspersed by 20 s rest, and a 5 min pause between the sets (<b>B</b>). Each training session was preceded by a 10 min warm-up and ended with a cool-down period.</p> Full article ">Figure 2
<p>Treadmill physical performance of normoxic and hypoxic SED, LIT, and SIT mice. Treadmill test was performed by increasing speed by 2 cm/s every 3 min until exhaustion.</p> Full article ">Figure 3
<p>The qRT-PCR analysis of <span class="html-italic">Hif1a</span> (<b>A</b>) and one of its target genes, <span class="html-italic">Vegfa</span> (<b>B</b>). Gene expression levels are normalized to the housekeeping gene (<span class="html-italic">18s</span>) and relative to SED in normoxia. Asterisks represent significance as determined by a two-way ANOVA (* <span class="html-italic">p</span> &lt; 0.05; ** <span class="html-italic">p</span> &lt; 0.01). Gene abbreviations are: <span class="html-italic">Hif1a</span> (hypoxia-inducible factor-1α); <span class="html-italic">Vegfa</span> (vascular endothelial growth factor A).</p> Full article ">Figure 4
<p>The qRT-PCR analysis of the indicated genes involved in glycogen synthesis (<b>A</b>), glucose transport (<b>B</b>), and glycolysis (<b>C</b>–<b>E</b>). Gene expression levels are normalized to the housekeeping gene (<span class="html-italic">18s</span>), and relative to SED in normoxia. Asterisks represent significance as determined by a two-way ANOVA (* <span class="html-italic">p</span> &lt; 0.05; ** <span class="html-italic">p</span> &lt; 0.01; *** <span class="html-italic">p</span> &lt; 0.001; **** <span class="html-italic">p</span> &lt; 0.0001). Gene abbreviations are: <span class="html-italic">Gys1</span> (glycogen synthase 1); <span class="html-italic">Glut4</span> (solute carrier family 2 member 4); <span class="html-italic">Hk2</span> (hexokinase 2); <span class="html-italic">Pfk</span> (phosphofructokinase); <span class="html-italic">Pkm1</span> (pyruvate kinase muscle 1).</p> Full article ">Figure 5
<p>The qRT-PCR analysis of the indicated genes related to lactate transport (<b>A</b>,<b>B</b>) and production (<b>C</b>–<b>E</b>). Gene expression levels are normalized to the housekeeping gene (<span class="html-italic">18s</span>) and relative to SED in normoxia. Asterisks represent significance as determined by a two-way ANOVA (** <span class="html-italic">p</span> &lt; 0.01; *** <span class="html-italic">p</span> &lt; 0.001; **** <span class="html-italic">p</span> &lt; 0.0001). Gene abbreviations are: <span class="html-italic">Mct1</span> (monocarboxylate transporter 1); <span class="html-italic">Mct4</span> (monocarboxylate transporter 4); <span class="html-italic">Ldha</span> (lactate dehydrogenase A); <span class="html-italic">Pdh</span> (pyruvate dehydrogenase); <span class="html-italic">Pdk4</span> (pyruvate dehydrogenase kinase 4).</p> Full article ">Figure 6
<p>The qRT-PCR analysis of the indicated genes responsible for mitochondrial biogenesis (<b>A</b>–<b>D</b>) and Krebs cycle (<b>E</b>). Gene expression levels are normalized to the housekeeping gene (<span class="html-italic">18s</span>) and relative to SED in normoxia. Asterisks represent significance as determined by a two-way ANOVA (* <span class="html-italic">p</span> &lt; 0.05; ** <span class="html-italic">p</span> &lt; 0.01; *** <span class="html-italic">p</span> &lt; 0.001). Gene abbreviations are: <span class="html-italic">Pgc1a</span> (peroxisome proliferator-activated receptor gamma coactivator 1-alpha); <span class="html-italic">Pgc1b</span> (peroxisome proliferator-activated receptor gamma coactivator 1-beta); <span class="html-italic">Nrf1</span> (nuclear respiratory factor 1); <span class="html-italic">Tfam</span> (mitochondrial transcription factor A); <span class="html-italic">Cs</span> (citrate synthase).</p> Full article ">Figure 7
<p>The qRT-PCR analysis of the indicated genes encoding mitochondrial respiratory chain complex (<b>A</b>–<b>D</b>). Gene expression levels are normalized to the housekeeping gene (<span class="html-italic">18s</span>) and relative to SED in normoxia. Asterisks represent significance as determined by a two-way ANOVA (** <span class="html-italic">p</span> &lt; 0.01). Gene abbreviations are: <span class="html-italic">mtNd1</span> (mitochondrial NADH dehydrogenase 1); <span class="html-italic">mtNd6</span> (mitochondrial NADH dehydrogenase 6); <span class="html-italic">Cytc</span> (mitochondrial cytochrome C); <span class="html-italic">Cytb</span> (mitochondrial cytochrome B).</p> Full article ">Figure 8
<p>Gene expression analysis of the indicated gene involved in fatty acid uptake (<b>A</b>), transport (<b>B</b>), and fatty acid β-oxidation (<b>C</b>–<b>E</b>). Gene expression levels are normalized to the housekeeping gene (<span class="html-italic">18s</span>) and relative to SED in normoxia. Asterisks represent significance as determined by a two-way ANOVA (* <span class="html-italic">p</span> &lt; 0.05; ** <span class="html-italic">p</span> &lt; 0.01). Gene abbreviations are: <span class="html-italic">Cd36</span> (fatty acid translocase cluster of differentiation); <span class="html-italic">Fabp3</span> (fatty acid binding protein 3); <span class="html-italic">Ucp2</span> (uncoupling protein 2); <span class="html-italic">Hsl</span> (hormone-sensitive lipase); <span class="html-italic">Mcad</span> (medium-chain acyl-CoA dehydrogenase).</p> Full article ">
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