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Metabolites
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Unlocking the Mysteries of Muscle Metabolism in the Animal Sciences
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Unlocking the Mysteries of Muscle Metabolism in the Animal Sciences

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

Deadline for manuscript submissions: 28 February 2025 | Viewed by 8279

Special Issue Editors

Prof. Dr. David E. Gerrard

E-Mail Website
Guest Editor
School of Animal Sciences, Virginia Tech, Blacksburg, VA 24061, USA
Interests: muscle; metabolism; fiber type; biochemistry; mitochondria; nutrition; energy
Special Issues, Collections and Topics in MDPI journals
Dr. Sally E. Johnson

E-Mail Website
Guest Editor
School of Animal Sciences, Virginia Tech, Blacksburg, VA 24061, USA
Interests: satellite cells; exercise metabolism; muscle development

Special Issue Information

Dear Colleagues,

The sustainability and security of the meat industry is predicated on the ability to grow animals as efficiently as possible. Indeed, great progress has been realized in animal growth efficiency over the past several decades, primarily through improved nutrition and genetics, and the use of growth promotants, though the latter technology is facing some pushback. Even so, as incremental increases in efficiency become more difficult to achieve through traditional means, we must continue to delve further into the cellular mechanisms controlling growth if we wish to meet the global demands for a highly coveted, yet nutritious source of protein for the human diet. Muscle growth or meat production is a complex biological process that results from the orchestration of a hierarchy of anabolic and catabolic events that are tightly synchronized with nutrient availability. When muscle cells ‘sense’ that energy substrates and amino acids are available, protein accretion and muscle growth proceeds. Conversely, when nutrient assets are limiting, either through gaps in management strategies, or during times of redirected nutrient partitioning as is the case with compromised health status or heat stress, muscle growth is curtailed, or even reversed if the insult is severe enough. To address these varied stimuli, muscle cells utilize highly integrated signaling cascades to sense and respond to nutritional cues in their residential niches. The existence and integration of these pathways are poorly understood but identification of novel processes will further empower animal scientists to monitor changes in metabolic status of growing tissues and inevitably foster discovery of new strategies for improving the efficiency of animal growth.

Prof. Dr. David E. Gerrard
Dr. Sally E. Johnson
Guest Editors

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Keywords

  • muscle
  • amino acid metabolism
  • energy metabolism
  • metabolites
  • protein
  • growth

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Published Papers (7 papers)

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16 pages, 2098 KiB  
Article
Mitochondrial Abundance and Function Differ Across Muscle Within Species
by Con-Ning Yen, Jocelyn S. Bodmer, Jordan C. Wicks, Morgan D. Zumbaugh, Michael E. Persia, Tim H. Shi and David E. Gerrard
Metabolites 2024, 14(10), 553; https://doi.org/10.3390/metabo14100553 - 16 Oct 2024
Viewed by 691
Abstract
Background: Mitochondria are considered the powerhouse of cells, and skeletal muscle cells are no exception. However, information regarding muscle mitochondria from different species is limited. Methods: Different muscles from cattle, pigs and chickens were analyzed for mitochondrial DNA (mtDNA), protein and [...] Read more.
Background: Mitochondria are considered the powerhouse of cells, and skeletal muscle cells are no exception. However, information regarding muscle mitochondria from different species is limited. Methods: Different muscles from cattle, pigs and chickens were analyzed for mitochondrial DNA (mtDNA), protein and oxygen consumption. Results: Bovine oxidative muscle mitochondria contain greater mtDNA (p < 0.05), protein (succinate dehydrogenase, SDHA, p < 0.01; citrate synthase, CS, p < 0.01; complex I, CI, p < 0.05), and oxygen consumption (p < 0.01) than their glycolytic counterpart. Likewise, porcine oxidative muscle contains greater mtDNA (p < 0.01), mitochondrial proteins (SDHA, p < 0.05; CS, p < 0.001; CI, p < 0.01) and oxidative phosphorylation capacity (OXPHOS, p < 0.05) in comparison to glycolytic muscle. However, avian oxidative skeletal muscle showed no differences in absolute mtDNA, SDHA, CI, complex II, lactate dehydrogenase, or glyceraldehyde 3 phosphate dehydrogenase compared to their glycolytic counterpart. Even so, avian mitochondria isolated from oxidative muscles had greater OXPHOS capacity (p < 0.05) than glycolytic muscle. Conclusions: These data show avian mitochondria function is independent of absolute mtDNA content and protein abundance, and argue that multiple levels of inquiry are warranted to determine the wholistic role of mitochondria in skeletal muscle. Full article
(This article belongs to the Special Issue Unlocking the Mysteries of Muscle Metabolism in the Animal Sciences)
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18 pages, 2528 KiB  
Article
The Effects of Maternal Nutrient Restriction during Mid to Late Gestation with Realimentation on Fetal Metabolic Profiles in the Liver, Skeletal Muscle, and Blood in Sheep
by Brandon I. Smith, Manuel A. Vásquez-Hidalgo, Xiaomeng Li, Kimberly A. Vonnahme, Anna T. Grazul-Bilska, Kendall C. Swanson, Timothy E. Moore, Sarah A. Reed and Kristen E. Govoni
Metabolites 2024, 14(9), 465; https://doi.org/10.3390/metabo14090465 - 23 Aug 2024
Viewed by 924
Abstract
Poor maternal nutrition during gestation negatively affects offspring growth and metabolism. To evaluate the impact of maternal nutrient restriction and realimentation on metabolism in the fetal liver, skeletal muscle, and circulation, on day 50 of gestation, ewes (n = 48) pregnant with [...] Read more.
Poor maternal nutrition during gestation negatively affects offspring growth and metabolism. To evaluate the impact of maternal nutrient restriction and realimentation on metabolism in the fetal liver, skeletal muscle, and circulation, on day 50 of gestation, ewes (n = 48) pregnant with singletons were fed 100% (CON) or 60% (RES) of requirements until day 90 of gestation, when a subset of ewes (n = 7/treatment) were euthanized, and fetal samples were collected. The remaining ewes were maintained on a current diet (CON-CON, n = 6; RES-RES, n = 7) or switched to an alternative diet (CON-RES, RES-CON; n = 7/treatment). On day 130 of gestation, the remaining ewes were euthanized, and fetal samples were collected. Fetal liver, longissimus dorsi (LD), and blood metabolites were analyzed using LC-MS/MS, and pathway enrichment analysis was conducted using MetaboAnalyst. Then, 600, 518, and 524 metabolites were identified in the liver, LD, and blood, respectively, including 345 metabolites that were present in all three. Nutrient restriction was associated with changes in amino acid, carbohydrate, lipid, and transulfuration/methionine metabolic pathways, some of which were alleviated by realimentation. Fetal age also affected metabolite abundance. The differential abundance of metabolites involved in amino acid, methionine, betaine, and bile acid metabolism could impact fetal epigenetic regulation, protein synthesis, lipid metabolism, and signaling associated with glucose and lipid metabolism. Full article
(This article belongs to the Special Issue Unlocking the Mysteries of Muscle Metabolism in the Animal Sciences)
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17 pages, 987 KiB  
Article
Ability of Nicotinamide Riboside to Prevent Muscle Fatigue of Barrows Subjected to a Performance Test
by Hanna M. Hennesy, Morgan E. Gravely, Daniela A. Alambarrio, Savannah R. Brannen, Jonathan J. McDonald, Sarah A. Devane, Kari K. Turner, Alexander M. Stelzleni, Travis G. O’Quinn and John M. Gonzalez
Metabolites 2024, 14(8), 424; https://doi.org/10.3390/metabo14080424 - 31 Jul 2024
Viewed by 850
Abstract
The objective of this study was to determine the daily dietary nicotinamide riboside (NR) dose required to maximize the delay of subjective muscle fatigue onset. Barrows (N = 100) were assigned to one of five treatments: a conventional swine finishing diet containing [...] Read more.
The objective of this study was to determine the daily dietary nicotinamide riboside (NR) dose required to maximize the delay of subjective muscle fatigue onset. Barrows (N = 100) were assigned to one of five treatments: a conventional swine finishing diet containing 0 (CON), 15 (15NR), 30 (30NR), 45 (45NR) mg·kg body weight−1·d−1 NR, or CON supplemented with 45 mg·kg body weight−1·d−1 NR by drench or cookie dough (DRE). All treatments were administered for the final 11 days of feeding. On supplementation d 10, barrows individually experienced a performance test at 1.09 m/s until they were subjectively exhausted. Wireless electromyography (EMG) sensors were affixed to the biceps femoris (BF), tensor fascia latae (TFL), and semitendinosus (ST) to measure real-time muscle activity. There were no treatment effects for barrow speed (p = 0.57), a tendency for a treatment effect (p = 0.07) for distance, and a treatment effect (p = 0.04) on time to exhaustion. Barrows of the 15NR and DRE treatments had greater (p = 0.05) distances to exhaustion than CON barrows but did not differ from other NR barrows (p > 0.11). Barrows in the 45NR treatment did not differ (p = 0.11) in distance from 30NR barrows but tended to have a greater (p = 0.07) distance compared to CON barrows. All other treatment comparisons did not differ (p > 0.27). Barrows in the DRE treatment moved for longer (p < 0.01) than CON barrows, but all other treatments did not differ from each other (p > 0.15). There was no treatment × period interaction for all muscles’ root mean square (RMS) values (p > 0.16), but there were Period effects for all muscles (p < 0.01) and a Treatment effect (p = 0.04) in the TFL. For all muscles, period 4 had greater RMS values than all other periods (p < 0.01), who did not differ from each other (p > 0.29). In the TFL, CON barrows had greater RMS values during the performance test compared to all NR treatments (p < 0.02), who did not differ from each other (p > 0.18). Overall, NR demonstrates potential in being a useful tool in fatigue prevention, but efficient administration of the compound needs further investigation. Full article
(This article belongs to the Special Issue Unlocking the Mysteries of Muscle Metabolism in the Animal Sciences)
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14 pages, 7624 KiB  
Article
Non-Alcoholic Fatty Liver Disease Induced by Feeding Medium-Chain Fatty Acids Upregulates Cholesterol and Lipid Homeostatic Genes in Skeletal Muscle of Neonatal Pigs
by Samuel D. Gerrard, Fernando H. Biase, Joseph A. Yonke, Ravi Yadav, Anthony J. Shafron, Nishanth E. Sunny, David E. Gerrard and Samer W. El-Kadi
Metabolites 2024, 14(7), 384; https://doi.org/10.3390/metabo14070384 - 11 Jul 2024
Viewed by 1069
Abstract
Non-alcoholic fatty liver disease (NAFLD) is a range of disorders characterized by lipid accumulation in hepatocytes. Although this spectrum of disorders is associated with adult obesity, recent evidence suggests that this condition could also occur independently of obesity, even in children. Previously, we [...] Read more.
Non-alcoholic fatty liver disease (NAFLD) is a range of disorders characterized by lipid accumulation in hepatocytes. Although this spectrum of disorders is associated with adult obesity, recent evidence suggests that this condition could also occur independently of obesity, even in children. Previously, we reported that pigs fed a formula containing medium-chain fatty acids (MCFAs) developed hepatic steatosis and weighed less than those fed an isocaloric formula containing long-chain fatty acids (LCFAs). Our objective was to determine the association between NAFLD and the skeletal muscle transcriptome in response to energy and lipid intake. Neonatal pigs were fed one of three formulas: a control formula (CONT, n = 6) or one of two isocaloric high-energy formulas containing either long (LCFA, n = 6) or medium (MCFA, n = 6) chain fatty acids. Pigs were fed for 22 d, and tissues were collected. Body weight at 20 and 22 d was greater for LCFA-fed pigs than their CONT or MCFA counterparts (p < 0.005). Longissimus dorsi weight was greater for LCFA compared with MCFA, while CONT was intermediate (p < 0.05). Lean gain and protein deposition were greater for LCFA than for CONT and MCFA groups (p < 0.01). Transcriptomic analysis revealed 36 differentially expressed genes (DEGs) between MCFA and LCFA, 53 DEGs between MCFA and CONT, and 52 DEGs between LCFA and CONT (FDR < 0.2). Feeding formula high in MCFAs resulted in lower body and muscle weights. Transcriptomics data suggest that the reduction in growth was associated with a disruption in cholesterol metabolism in skeletal muscles. Full article
(This article belongs to the Special Issue Unlocking the Mysteries of Muscle Metabolism in the Animal Sciences)
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19 pages, 4982 KiB  
Article
Skeletal Muscle Metabolism Is Dynamic during Porcine Postnatal Growth
by Linnea A. Rimmer, Erika R. Geisbrecht, Michael D. Chao, Travis G. O’Quinn, Jason C. Woodworth and Morgan D. Zumbaugh
Metabolites 2024, 14(7), 357; https://doi.org/10.3390/metabo14070357 - 26 Jun 2024
Viewed by 1377
Abstract
Skeletal muscle metabolism has implications for swine feed efficiency (FE); however, it remains unclear if the metabolic profile of skeletal muscle changes during postnatal growth. To assess the metabolic changes, samples were collected from the longissimus dorsi (LD, glycolytic muscle), latissimus dorsi (LAT, [...] Read more.
Skeletal muscle metabolism has implications for swine feed efficiency (FE); however, it remains unclear if the metabolic profile of skeletal muscle changes during postnatal growth. To assess the metabolic changes, samples were collected from the longissimus dorsi (LD, glycolytic muscle), latissimus dorsi (LAT, mixed muscle), and masseter (MS, oxidative muscle) at 20, 53, 87, 120, and 180 days of age from barrows. Muscles were assessed to determine the abundance of several metabolic enzymes. Lactate dehydrogenase (LDHα) decreased in all muscles from 20 to 87 d (p < 0.01), which may be attributed to the muscles being more glycolytic at weaning from a milk-based diet. Pyruvate carboxylase (PC) increased in all muscles at 53 d compared to the other time points (p < 0.01), while pyruvate dehydrogenase α 1 (PDHα1) increased at 87 and 180 d in MS compared to LD (p < 0.05), indicating that potential changes occur in pyruvate entry into the tricarboxylic acid (TCA) cycle during growth. Isolated mitochondria from each muscle were incubated with 13C-labeled metabolites to assess isotopomer enrichment patterns of TCA intermediates. Citrate M + 2 and M + 4 derived from [13C3]-pyruvate increased at 87 d in LAT and MS mitochondria compared to LD mitochondria (p < 0.05). Regardless of the muscle, citrate M+3 increased at 87 d compared to 20, 53, and 120 d, while 180 d showed intermediate values (p < 0.01). These data support the notion that pyruvate metabolism is dynamic during growth. Our findings establish a metabolic fingerprint associated with postnatal muscle hypertrophy. Full article
(This article belongs to the Special Issue Unlocking the Mysteries of Muscle Metabolism in the Animal Sciences)
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19 pages, 2681 KiB  
Article
Daily Eicosapentaenoic Acid Infusion in IUGR Fetal Lambs Reduced Systemic Inflammation, Increased Muscle ADRβ2 Content, and Improved Myoblast Function and Muscle Growth
by Haley N. Beer, Taylor A. Lacey, Rachel L. Gibbs, Micah S. Most, Zena M. Hicks, Pablo C. Grijalva, Eileen S. Marks-Nelson, Ty B. Schmidt, Jessica L. Petersen and Dustin T. Yates
Metabolites 2024, 14(6), 340; https://doi.org/10.3390/metabo14060340 - 18 Jun 2024
Viewed by 967
Abstract
Intrauterine growth-restricted (IUGR) fetuses exhibit systemic inflammation that contributes to programmed deficits in myoblast function and muscle growth. Thus, we sought to determine if targeting fetal inflammation improves muscle growth outcomes. Heat stress-induced IUGR fetal lambs were infused with eicosapentaenoic acid (IUGR+EPA; n [...] Read more.
Intrauterine growth-restricted (IUGR) fetuses exhibit systemic inflammation that contributes to programmed deficits in myoblast function and muscle growth. Thus, we sought to determine if targeting fetal inflammation improves muscle growth outcomes. Heat stress-induced IUGR fetal lambs were infused with eicosapentaenoic acid (IUGR+EPA; n = 9) or saline (IUGR; n = 8) for 5 days during late gestation and compared to saline-infused controls (n = 11). Circulating eicosapentaenoic acid was 42% less (p < 0.05) for IUGR fetuses but was recovered in IUGR+EPA fetuses. The infusion did not improve placental function or fetal O2 but resolved the 67% greater (p < 0.05) circulating TNFα observed in IUGR fetuses. This improved myoblast function and muscle growth, as the 23% reduction (p < 0.05) in the ex vivo differentiation of IUGR myoblasts was resolved in IUGR+EPA myoblasts. Semitendinosus, longissimus dorsi, and flexor digitorum superficialis muscles were 24–39% lighter (p < 0.05) for IUGR but not for IUGR+EPA fetuses. Elevated (p < 0.05) IL6R and reduced (p < 0.05) β2 adrenoceptor content in IUGR muscle indicated enhanced inflammatory sensitivity and diminished β2 adrenergic sensitivity. Although IL6R remained elevated, β2 adrenoceptor deficits were resolved in IUGR+EPA muscle, demonstrating a unique underlying mechanism for muscle dysregulation. These findings show that fetal inflammation contributes to IUGR muscle growth deficits and thus may be an effective target for intervention. Full article
(This article belongs to the Special Issue Unlocking the Mysteries of Muscle Metabolism in the Animal Sciences)
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18 pages, 2032 KiB  
Article
Daily Injection of the β2 Adrenergic Agonist Clenbuterol Improved Muscle Glucose Metabolism, Glucose-Stimulated Insulin Secretion, and Hyperlipidemia in Juvenile Lambs Following Heat-Stress-Induced Intrauterine Growth Restriction
by Rachel L. Gibbs, James A. Wilson, Rebecca M. Swanson, Joslyn K. Beard, Zena M. Hicks, Haley N. Beer, Eileen S. Marks-Nelson, Ty B. Schmidt, Jessica L. Petersen and Dustin T. Yates
Metabolites 2024, 14(3), 156; https://doi.org/10.3390/metabo14030156 - 7 Mar 2024
Cited by 1 | Viewed by 1728
Abstract
Stress-induced fetal programming diminishes β2 adrenergic tone, which coincides with intrauterine growth restriction (IUGR) and lifelong metabolic dysfunction. We determined if stimulating β2 adrenergic activity in IUGR-born lambs would improve metabolic outcomes. IUGR lambs that received daily injections of saline or [...] Read more.
Stress-induced fetal programming diminishes β2 adrenergic tone, which coincides with intrauterine growth restriction (IUGR) and lifelong metabolic dysfunction. We determined if stimulating β2 adrenergic activity in IUGR-born lambs would improve metabolic outcomes. IUGR lambs that received daily injections of saline or the β2 agonist clenbuterol from birth to 60 days were compared with controls from pair-fed thermoneutral pregnancies. As juveniles, IUGR lambs exhibited systemic inflammation and robust metabolic dysfunction, including greater (p < 0.05) circulating TNFα, IL-6, and non-esterified fatty acids, increased (p < 0.05) intramuscular glycogen, reduced (p < 0.05) circulating IGF-1, hindlimb blood flow, glucose-stimulated insulin secretion, and muscle glucose oxidation. Daily clenbuterol fully recovered (p < 0.05) circulating TNFα, IL-6, and non-esterified fatty acids, hindlimb blood flow, muscle glucose oxidation, and intramuscular glycogen. Glucose-stimulated insulin secretion was partially recovered (p < 0.05) in clenbuterol-treated IUGR lambs, but circulating IGF-1 was not improved. Circulating triglycerides and HDL cholesterol were elevated (p < 0.05) in clenbuterol-treated IUGR lambs, despite being normal in untreated IUGR lambs. We conclude that deficient β2 adrenergic regulation is a primary mechanism for several components of metabolic dysfunction in IUGR-born offspring and thus represents a potential therapeutic target for improving metabolic outcomes. Moreover, benefits from the β2 agonist were likely complemented by its suppression of IUGR-associated inflammation. Full article
(This article belongs to the Special Issue Unlocking the Mysteries of Muscle Metabolism in the Animal Sciences)
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