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Effects of Early Resveratrol Intervention on Skeletal Muscle Mitochondrial Function and Redox Status in Neonatal Piglets with or without Intrauterine Growth Retardation.

ABSTRACT: Skeletal muscle mitochondrial malfunction of offspring induced by intrauterine growth retardation (IUGR) may be a contributor to growth restriction and metabolic disorder at various periods of life. This study explored the effects of IUGR and resveratrol (RSV) on mitochondrial function and redox status in the longissimus dorsi muscle (LM) of piglets during the sucking period. A total of 36 pairs of IUGR and normal birth weight male piglets were orally fed with either 80?mg RSV/kg body weight/d or 0.5% carboxymethylcellulose sodium during days 7-21 after birth. The results showed that RSV treatment improved anomalous mitochondrial morphology, increased adenosine triphosphate and glycogen contents, and enhanced nicotinamide adenine dinucleotide/reduced form of nicotinamide-adenine dinucleotide ratio in the LM of IUGR piglets. Moreover, the IUGR-induced increased malondialdehyde and protein carbonyl concentrations, abnormal mtDNA number, and suppressed genes expression of mitochondrial biogenesis such as nuclear respiratory factor 1, estrogen-related receptor alpha, and polymerase gamma in the LM were restored to some extent by RSV treatment. Additionally, RSV increased mitochondrial complex V activity in the LM of piglets. Collectively, RSV administration alleviated the LM mitochondrial dysfunction and oxidative damage of IUGR piglets.

SUBMITTER: Cheng K

PROVIDER: S-EPMC7261333 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Effects of Early Resveratrol Intervention on Skeletal Muscle Mitochondrial Function and Redox Status in Neonatal Piglets with or without Intrauterine Growth Retardation.

Cheng Kang K Wang Ting T Li Simian S Song Zhihua Z Zhang Hao H Zhang Lili L Wang Tian T

Oxidative medicine and cellular longevity 20200522

Skeletal muscle mitochondrial malfunction of offspring induced by intrauterine growth retardation (IUGR) may be a contributor to growth restriction and metabolic disorder at various periods of life. This study explored the effects of IUGR and resveratrol (RSV) on mitochondrial function and redox status in the longissimus dorsi muscle (LM) of piglets during the sucking period. A total of 36 pairs of IUGR and normal birth weight male piglets were orally fed with either 80 mg RSV/kg body weight/d o ...[more]

PMID: 32566083

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Project description:Animals with intrauterine growth retardation (IUGR) usually undergo injured postnatal growth and development during the early period after birth. Equol (Eq), an isoflavan produced by gut bacteria in response to daidzein intake, has various health benefits. Therefore, the objective of this study was to evaluate whether Eq supplementation can influence the growth performance, redox status, intestinal health and skeletal muscle development of weanling piglets with IUGR. A total of 10 normal-birth-weight (NBW) newborn female piglets and 20 newborn female piglets with IUGR were selected. After weaning at the age of 21 d, 10 NBW piglets and 10 IUGR piglets were allocated to the NBW group and IUGR group, respectively, and offered a basal diet. The other 10 IUGR piglets were allocated to the IUGR + Eq group and offered a basal diet with 50 mg of Eq per kg of diet. The whole trial lasted for 21 d. At the end of the feeding trial, all piglets were sacrificed for the collection of serum, intestinal tissues and skeletal muscles. Supplementation with Eq increased the average daily gain (ADG), average daily feed intake (ADFI), duodenal villus height to crypt depth ratio (V/C), jejunal villus height and V/C, but reduced the duodenal crypt depth in neonatal piglets with IUGR. Meanwhile, Eq supplementation elevated the activities of superoxide dismutase (SOD) and catalase (CAT) in the serum and duodenum and the activity of SOD in the jejunum, but lowered malondialdehyde (MDA) content in the serum, jejunum and ileum of piglets with IUGR. In addition, supplementation with Eq reduced diamine oxidase (DAO) activity and the levels of D-lactate and endotoxin in serum, and the tumor necrosis factor-α (TNF-α) level in jejunum and ileum, whereas the concentration of serum immunoglobulin G (IgG) and the mRNA levels of intestinal barrier-related markers in jejunum and ileum of IUGR piglets were increased. Furthermore, supplementation with Eq elevated the percentage of fast-fibers and was accompanied with higher mRNA expression of myosin heavy chain IIb (MyHC IIb) and lower mRNA levels in MyHC I in the longissimus thoracis (LT) muscle of IUGR piglets. In summary, Eq supplementation can promote antioxidant capacity, maintain intestinal health and facilitate skeletal muscle development, thus resulting in the higher growth performance of IUGR piglets.

Project description:Abnormal lipid metabolism, oxidative stress (OS), and inflammation play a pivotal role in the increased susceptibility to neonatal fatty liver diseases associated with intrauterine growth retardation (IUGR). This study was firstly conducted to investigate whether resveratrol could alleviate IUGR-induced hepatic lipid accumulation, alteration of redox and immune status in a sucking piglet model and explore the possible mechanisms at transcriptional levels. A total of 36 pairs of 7 d old male normal birth weight (NBW) and IUGR piglets were orally fed with either 80 mg resveratrol/kg body weight/d or 0.5% carboxymethylcellulose sodium for a period of 14 days, respectively. Compared with the NBW piglets, the IUGR piglets displayed compromised growth performance and liver weight, reduced plasma free fatty acid (FFA) level, increased hepatic OS, abnormal hepatic lipid accumulation and weakened hepatic immune function, and hepatic aberrant transcriptional expression of some genes such as heme oxygenase 1, superoxide dismutase 1, sterol regulatory element-binding protein 1c, stearoyl-CoA desaturase 1, liver fatty acid-binding proteins 1, toll-like receptor 4, and tumor necrosis factor alpha (TNF-α). Oral administration of resveratrol to piglets decreased the levels of FFA and total triglycerides (TG) in the plasma and hepatic TNF-α concentration, and increased glutathione reductase activity and reduced glutathione level in the liver. Resveratrol restored the increased alanine aminotransferase activity in the plasma of IUGR piglets. Treatment with resveratrol ameliorated the increased hepatic malondialdehyde, protein carbonyl, TG, and FFA concentrations induced by IUGR. Resveratrol treatment alleviated the reduced lipoprotein lipase activity and its mRNA expression as well as TNF-α gene expression in the liver of IUGR piglets. Hepatic glutathione peroxidase 1 and monocyte chemotactic protein 1 genes expression of piglets was upregulated by oral resveratrol administration. In conclusion, resveratrol administration plays a beneficial role in hepatic redox status and lipid balance of the IUGR piglets.

Project description:BackgroundIntestinal disorder is an important factor contributing to growth lag and high rates of morbidity and mortality of piglets with intrauterine growth retardation (IUGR). Resveratrol (RSV) and its derivative pterostilbene (PT) are natural stilbenes possessing various bioactivities, such as antioxidative and anti-inflammatory effects. This study compared the protective potential of RSV and PT on the intestinal redox status and gut microbiota in weanling piglets with IUGR.MethodsEighteen male piglets of normal body weight (NBW) and 54 same-sex IUGR piglets were chosen according to their birth and weaning weights. The NBW piglets accepted a basal diet, while the IUGR piglets were allotted to one of three groups according to their body weight at weaning and received a basal diet, an RSV-supplemented diet (300 mg/kg), or a PT-supplemented diet (300 mg/kg), respectively.ResultsCompared with IUGR piglets, both RSV and PT improved the IUGR-associated decrease in jejunal villus height and increases in plasma diamine oxidase activity and D-lactate level and jejunal apoptosis of piglets (P < 0.05). Administering RSV and PT also enhanced jejunal superoxide dismutase activity and the mRNA and protein expression of superoxide dismutase 2 of IUGR piglets by promoting nuclear factor erythroid 2-related factor 2 (Nrf2) nuclear translocation (P < 0.05). Comparatively, PT was more effective than RSV in elevating the villus height/crypt depth ratio and occludin mRNA and protein levels in the jejunum of IUGR piglets (P < 0.05). PT was also superior to RSV in increasing Nrf2 nuclear translocation and inhibiting malondialdehyde accumulation in the jejunum of IUGR piglets (P < 0.05). Additionally, RSV modulated the composition of cecal microbiota of IUGR piglets, as evidenced by increasing the prevalence of the phylum Bacteroidetes and the genera Prevotella, Faecalibacterium, and Parabacteroides and inhibiting the growth of the phylum Proteobacteria and its genera Escherichia and Actinobacillus (P < 0.05). Moreover, RSV significantly increased the butyrate concentration in the cecum of IUGR piglets (P < 0.05).ConclusionPT is more potent than RSV to prevent intestinal oxidative stress, while RSV has a stronger capacity to regulate gut microbiota compared to PT.

Project description:The present study used intrauterine growth restriction (IUGR) piglets as an animal model to determine the effect of Bacillus subtilis on intestinal integrity, antioxidant capacity, and microbiota in the jejunum of suckling piglets. In total, 8 normal birth weight (NBW) newborn piglets (1.62 ± 0.10 kg) and 16 newborn IUGR piglets (0.90 ± 0.08 kg) were selected and assigned to three groups. Piglets were orally gavaged with 10-mL sterile saline (NBW and IUGR groups), and IUGR piglets were orally gavaged with 10-mL/d bacterial fluid (B. subtilis diluted in sterile saline, gavage in the dose of 2 × 109 colony-forming units per kg of body weight; IBS group; n = 8). IUGR induced jejunal barrier dysfunction and redox status imbalance of piglets, and changed the abundances of bacteria in the jejunum. Treatment with B. subtilis increased (P < 0.05) the ratio of villus height to crypt depth (VH/CD) in the jejunum, decreased (P < 0.05) the plasma diamine oxidase (DAO) activity, and enhanced (P < 0.05) the gene expressions of zonula occludens-1 (ZO-1), occludin, and claudin-1 in the jejunum of IUGR piglets. Treatment with B. subtilis decreased (P < 0.05) the concentration of protein carbonyl (PC) and increased (P < 0.05) the activities of catalase (CAT) and total superoxide dismutase (T-SOD) in the jejunum of IUGR piglets. Treatment with B. subtilis also increased (P < 0.05) gene expressions of superoxide dismutase 1 (SOD1), CAT, and nuclear factor erythroid 2-related factor (Nrf2), as well as the protein expressions of heme oxygenase-1 (HO-1), SOD1, and Nrf2 in the jejunum of IUGR piglets. Treatment with B. subtilis also improved the abundances and the community structure of bacteria in the jejunum of IUGR piglets. These results suggested that IUGR damaged the jejunal barrier function and antioxidant capacity of suckling piglets, and altered the abundances of bacteria in the jejunum. Treatment with B. subtilis improved the intestinal integrity and antioxidant capacity while also improved the abundances and structure of bacteria in the jejunum of suckling piglets.

Project description:There are few studies on the mechanism of redox status imbalance and intestinal dysfunction in intrauterine growth restricted (IUGR) newborn piglets. Here, we investigated the mechanism of jejunum dysfunction in weaned piglets with IUGR and the mechanism through which dimethylglycine sodium salt (DMG-Na) supplementation improving the imbalance of their redox status. In this work, a total of 10 normal birth weight (NBW) newborn piglets and 20 IUGR newborn piglets were obtained. After weaning at 21 d, they were assigned to 3 groups (n = 10/group): NBW weaned piglets fed standard basal diets (NBWC); one IUGR weaned piglets fed standard basal diets (IUGRC); another IUGR weaned piglets from the same litter fed standard basal diets plus 0.1% DMG-Na (IUGRD). The piglets in these 3 groups were sacrificed at 49 d of age, and the blood and jejunum samples were collected immediately. The growth performance values in the IUGRC group were lower (P < 0.05) than those in the NBWC group. Jejunum histomorphological parameters, inflammatory cytokines, and digestive enzyme activity as well as serum immunoglobulin were lower (P < 0.05) in the IUGRC group than those in the NBWC group. Compared with these in the NBWC group, the redox status of serum, jejunum, and mitochondria and the expression levels of jejunum redox status-related, cell adhesion-related, and mitochondrial function-related genes and proteins were suppressed in the IUGRC group (P < 0.05). However, compared with those in the IUGRC group, the growth performance values, jejunum histomorphological parameters, inflammatory cytokines, digestive enzyme activity, serum immunoglobulin, redox status of serum, jejunum, and mitochondria, and the expression levels of jejunum redox status-related, cell adhesion-related, and mitochondrial function-related genes and proteins were improved (P < 0.05) in the IUGRD group. In conclusion, dietary DMG-Na supplementation alleviates redox status imbalance and intestinal dysfunction in IUGR weaned piglets mainly by activating the sirtuin 1 (SIRT1)/peroxisome proliferator-activated receptorγcoactivator-1α (PGC1α) pathway, thereby improving their unfavorable body state.

Project description:Intrauterine growth retardation (IUGR) delays the gut development of neonates, but effective treatment strategies are still limited. This study used newborn piglets as a model to evaluate the protective effect of polydatin (PD) against IUGR-induced intestinal injury. In total, 36 IUGR piglets and an equal number of normal birth weight (NBW) littermates were fed either a basal diet or a PD-supplemented diet from 21 to 35 days of age. Compared with NBW, IUGR induced jejunal damage and barrier dysfunction of piglets, as indicated by observable bacterial translocation, enhanced apoptosis, oxidative and immunological damage, and mitochondrial dysfunction. PD treatment decreased bacterial translocation and inhibited the IUGR-induced increases in circulating diamine oxidase activity (P = 0.039) and D-lactate content (P = 0.004). The apoptotic rate (P = 0.024) was reduced by 35.2% in the PD-treated piglets, along with increases in villus height (P = 0.033) and in ratio of villus height to crypt depth (P = 0.049). PD treatment promoted superoxide dismutase (P = 0.026) and glutathione S-transferase activities (P = 0.006) and reduced malondialdehyde (P = 0.015) and 8-hydroxy-2'-deoxyguanosine accumulation (P = 0.034) in the jejunum. The PD-treated IUGR piglets showed decreased jejunal myeloperoxidase activity (P = 0.029) and tumor necrosis factor alpha content (P = 0.035) than those received a basal diet. PD stimulated nuclear sirtuin 1 (P = 0.028) and mitochondrial citrate synthase activities (P = 0.020) and facilitated adenosine triphosphate production (P = 0.009) in the jejunum of piglets. Furthermore, PD reversed the IUGR-induced declines in mitochondrial DNA content (P = 0.048), the phosphorylation of adenosine monophosphate-activated protein kinase alpha (P = 0.027), and proliferation-activated receptor gamma coactivator 1 alpha expression (P = 0.033). Altogether, the results indicate that PD may improve jejunal integrity, mitigate mucosal oxidative and immunological damage, and facilitate mitochondrial function in IUGR piglets.

Project description:Intrauterine growth retardation (IUGR) results in intestinal dysfunction contributing to metabolic syndrome and growth lag of piglets. Bile acid (BA) presents various bioactivities, including regulation roles in antioxidant, anti-inflammation, and glucose and lipid metabolism. Forty-eight weaned piglets were allocated to four groups in a 2 × 2 factorial arrangement with the effects of BA supplementation and IUGR challenge. Twenty-four IUGR piglets and 24 normal birth weight (NBW) piglets were allocated into two groups, respectively, including the control group fed with a basal diet, and the treatment group fed a basal diet supplemented with 400 mg/kg BA. The experiment lasted 28 days. The results indicated that BA improved liver and spleen indexes in IUGR piglets, whereas decreased blood RDW-CV and RDW-SD regardless of IUGR (P < 0.05). Dietary BA supplementation decreased plasma CAT activity and liver GSH concentration regardless of IUGR, whereas increased plasma GSH and liver H2O2 and decreased liver T-AOC in weaned piglets (P < 0.05). In addition, IUGR downregulated liver Nrf1 and Nrf2 expression levels, while BA supplementation upregulated the Nrf2 expression of liver in weaned piglets (P < 0.05). Dietary BA decreased (P < 0.05) jejunal GSH concentration and ileal CAT activity regardless of IUGR. Furthermore, IUGR upregulated (P < 0.05) jejunal SOD and CAT expression levels; however, dietary BA upregulated ileal Nrf1 (P < 0.05) and Keap1 (P = 0.07) expression levels in piglets regardless of IUGR. Moreover, IUGR upregulated the liver lipid synthesis (FAS) and downregulated HSL and SCD1 expression levels, while dietary BA downregulated liver FAS and SCD1 expression levels (P < 0.05). However, BA supplementation could enhance liver gluconeogenesis by upregulating (P < 0.05) the liver G6PC and PCK1 expression levels in the NBW piglets but not in the IUGR piglets. Collectively, these findings suggest that BA could regulate the redox status of weaned piglets by regulating the Nrf2/Keap1 pathway and improving liver glucose and lipid metabolism of IUGR piglets. These findings will provide a reference for the application of BA in swine production; moreover, considering the physiological similarity between pigs and humans, these findings will provide a reference for IUGR research in humans.

Dataset Information

Effects of Early Resveratrol Intervention on Skeletal Muscle Mitochondrial Function and Redox Status in Neonatal Piglets with or without Intrauterine Growth Retardation.

Publications

Effects of Early Resveratrol Intervention on Skeletal Muscle Mitochondrial Function and Redox Status in Neonatal Piglets with or without Intrauterine Growth Retardation.

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