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Decreased eccentric exercise-induced macrophage infiltration in skeletal muscle after supplementation with a class of ginseng-derived steroids.

Yu SH, Huang CY, Lee SD, Hsu MF, Wang RY, Kao CL, Kuo CH - PLoS ONE (2014)

Bottom Line: Dammarane steroids (DS) are a class of chemical compounds present in Panax ginseng.In conclusion, our study provides new evidence suggesting that DS is an ergogenic component of ginseng that potentiate inflammation at baseline but that produce anti-inflammatory effects on skeletal muscle following muscle-damaging exercise.Furthermore, high doses should be avoided in formulating ginseng-based products.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Exercise Biochemistry, University of Taipei, Taipei City, Taiwan, Republic of China; Department of Leisure Industry and Health Promotion, National Ilan University, Yilan County, Taiwan, Republic of China.

ABSTRACT
Dammarane steroids (DS) are a class of chemical compounds present in Panax ginseng. Here, we evaluated the effect of 10 weeks of DS supplementation on inflammatory modulation in the soleus muscle following eccentric exercise (EE)-induced muscle damage (downhill running). Eighty rats were randomized into 4 groups of DS supplementation (saline, 20, 60, 120 mg/kg body weight). Inflammatory markers were measured at rest and again 1 h after EE. At rest, NFκB signaling, TNF-alpha and IL-6 mRNAs, 3-nitrotyrosine, glutathione peroxidase, and GCS (glutamylcysteine synthetase) levels were significantly elevated in the skeletal muscle of DS-treated rats in a dose-dependent manner. Additionally, there were no detectable increases in the number of necrotic muscle fibers or CD68+ M1 macrophages. However, muscle strength, centronucleation, IL-10 mRNA expression, and the number of CD163+ M2 macrophages increased significantly over controls with DS treatment in rat soleus muscle. Under EE-challenged conditions, significant increases in muscle fiber necrosis, CD68+ M1 macrophage distribution, and 3-nitrotyrosine were absent in rats that received low and medium doses (20 and 60 mg/kg) of DS treatment, suggesting that DS possess anti-inflammatory action protecting against a muscle-damaging challenge. However, this protective activity was diminished when a high dose of DS (120 mg/kg) was administered, suggesting that DS possess hormetic properties. In conclusion, our study provides new evidence suggesting that DS is an ergogenic component of ginseng that potentiate inflammation at baseline but that produce anti-inflammatory effects on skeletal muscle following muscle-damaging exercise. Furthermore, high doses should be avoided in formulating ginseng-based products.

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Muscle injury, macrophage invasion and oxidative stress in soleus muscle.(A) Representative histochemical analysis of muscle sections from soleus muscle with H&E staining. Arrowheads indicate immune cell invasion. Scoring is shown on the right. (B) Representative immunohistochemical staining of CD68-positive cells (brown color) in a soleus muscle section. Nucleolus was labeled with eosin staining (blue color). Original magnification was 400x, and scoring of CD68-positive cells is shown on the bottom. (C) Representative western blot showing levels of nitrotyrosine extracted from soleus muscle. Bars represent the relative quantification of nitrated protein normalized to GAPDH. In (A–C), and data are presented as the mean ± SEM. †p<0.05 compared with the sedentary group. *p<0.05 compared with the control group of sedentary or EE. Scale bar  = 50 µm.
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pone-0114649-g002: Muscle injury, macrophage invasion and oxidative stress in soleus muscle.(A) Representative histochemical analysis of muscle sections from soleus muscle with H&E staining. Arrowheads indicate immune cell invasion. Scoring is shown on the right. (B) Representative immunohistochemical staining of CD68-positive cells (brown color) in a soleus muscle section. Nucleolus was labeled with eosin staining (blue color). Original magnification was 400x, and scoring of CD68-positive cells is shown on the bottom. (C) Representative western blot showing levels of nitrotyrosine extracted from soleus muscle. Bars represent the relative quantification of nitrated protein normalized to GAPDH. In (A–C), and data are presented as the mean ± SEM. †p<0.05 compared with the sedentary group. *p<0.05 compared with the control group of sedentary or EE. Scale bar  = 50 µm.

Mentions: To evaluate the immune response to EE in skeletal muscle after downhill running, we examined leukocyte invasion and the number of necrotic muscle fibers. H&E staining and immunohistochemical staining for CD68+ (M1 macrophages) was performed in rat soleus following 10 weeks of DS supplementation at various doses (Fig. 2). Necrotic muscle fibers and CD68-positive cells were identified by cells invasion (Fig. 2A) and brown color (Fig. 2B), respectively. In non-exercised rats, there was no increase in necrotic muscle fibers (Fig. 2A) or CD68+ M1 macrophages (Fig. 2B) in skeletal muscle with DS treatment. However, levels of 3-nitrotyrosine, an oxidative damage marker, increased linearly with dosage (Fig. 2C). Following EE challenge, the number of necrotic muscle fibers increased significantly above the non-exercise control, along with leukocyte and CD68+ M1 macrophage infiltration. In rats treated with low and medium doses of DS, such increases were not observed with EE challenge (Figs. 2A and 2B). In saline control rats, 3-nitrotyrosine levels in EE-challenged muscle were significantly greater than in non-exercised muscle. However, this increase was not observed at all doses of DS treatment (Fig. 2C).


Decreased eccentric exercise-induced macrophage infiltration in skeletal muscle after supplementation with a class of ginseng-derived steroids.

Yu SH, Huang CY, Lee SD, Hsu MF, Wang RY, Kao CL, Kuo CH - PLoS ONE (2014)

Muscle injury, macrophage invasion and oxidative stress in soleus muscle.(A) Representative histochemical analysis of muscle sections from soleus muscle with H&E staining. Arrowheads indicate immune cell invasion. Scoring is shown on the right. (B) Representative immunohistochemical staining of CD68-positive cells (brown color) in a soleus muscle section. Nucleolus was labeled with eosin staining (blue color). Original magnification was 400x, and scoring of CD68-positive cells is shown on the bottom. (C) Representative western blot showing levels of nitrotyrosine extracted from soleus muscle. Bars represent the relative quantification of nitrated protein normalized to GAPDH. In (A–C), and data are presented as the mean ± SEM. †p<0.05 compared with the sedentary group. *p<0.05 compared with the control group of sedentary or EE. Scale bar  = 50 µm.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263678&req=5

pone-0114649-g002: Muscle injury, macrophage invasion and oxidative stress in soleus muscle.(A) Representative histochemical analysis of muscle sections from soleus muscle with H&E staining. Arrowheads indicate immune cell invasion. Scoring is shown on the right. (B) Representative immunohistochemical staining of CD68-positive cells (brown color) in a soleus muscle section. Nucleolus was labeled with eosin staining (blue color). Original magnification was 400x, and scoring of CD68-positive cells is shown on the bottom. (C) Representative western blot showing levels of nitrotyrosine extracted from soleus muscle. Bars represent the relative quantification of nitrated protein normalized to GAPDH. In (A–C), and data are presented as the mean ± SEM. †p<0.05 compared with the sedentary group. *p<0.05 compared with the control group of sedentary or EE. Scale bar  = 50 µm.
Mentions: To evaluate the immune response to EE in skeletal muscle after downhill running, we examined leukocyte invasion and the number of necrotic muscle fibers. H&E staining and immunohistochemical staining for CD68+ (M1 macrophages) was performed in rat soleus following 10 weeks of DS supplementation at various doses (Fig. 2). Necrotic muscle fibers and CD68-positive cells were identified by cells invasion (Fig. 2A) and brown color (Fig. 2B), respectively. In non-exercised rats, there was no increase in necrotic muscle fibers (Fig. 2A) or CD68+ M1 macrophages (Fig. 2B) in skeletal muscle with DS treatment. However, levels of 3-nitrotyrosine, an oxidative damage marker, increased linearly with dosage (Fig. 2C). Following EE challenge, the number of necrotic muscle fibers increased significantly above the non-exercise control, along with leukocyte and CD68+ M1 macrophage infiltration. In rats treated with low and medium doses of DS, such increases were not observed with EE challenge (Figs. 2A and 2B). In saline control rats, 3-nitrotyrosine levels in EE-challenged muscle were significantly greater than in non-exercised muscle. However, this increase was not observed at all doses of DS treatment (Fig. 2C).

Bottom Line: Dammarane steroids (DS) are a class of chemical compounds present in Panax ginseng.In conclusion, our study provides new evidence suggesting that DS is an ergogenic component of ginseng that potentiate inflammation at baseline but that produce anti-inflammatory effects on skeletal muscle following muscle-damaging exercise.Furthermore, high doses should be avoided in formulating ginseng-based products.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Exercise Biochemistry, University of Taipei, Taipei City, Taiwan, Republic of China; Department of Leisure Industry and Health Promotion, National Ilan University, Yilan County, Taiwan, Republic of China.

ABSTRACT
Dammarane steroids (DS) are a class of chemical compounds present in Panax ginseng. Here, we evaluated the effect of 10 weeks of DS supplementation on inflammatory modulation in the soleus muscle following eccentric exercise (EE)-induced muscle damage (downhill running). Eighty rats were randomized into 4 groups of DS supplementation (saline, 20, 60, 120 mg/kg body weight). Inflammatory markers were measured at rest and again 1 h after EE. At rest, NFκB signaling, TNF-alpha and IL-6 mRNAs, 3-nitrotyrosine, glutathione peroxidase, and GCS (glutamylcysteine synthetase) levels were significantly elevated in the skeletal muscle of DS-treated rats in a dose-dependent manner. Additionally, there were no detectable increases in the number of necrotic muscle fibers or CD68+ M1 macrophages. However, muscle strength, centronucleation, IL-10 mRNA expression, and the number of CD163+ M2 macrophages increased significantly over controls with DS treatment in rat soleus muscle. Under EE-challenged conditions, significant increases in muscle fiber necrosis, CD68+ M1 macrophage distribution, and 3-nitrotyrosine were absent in rats that received low and medium doses (20 and 60 mg/kg) of DS treatment, suggesting that DS possess anti-inflammatory action protecting against a muscle-damaging challenge. However, this protective activity was diminished when a high dose of DS (120 mg/kg) was administered, suggesting that DS possess hormetic properties. In conclusion, our study provides new evidence suggesting that DS is an ergogenic component of ginseng that potentiate inflammation at baseline but that produce anti-inflammatory effects on skeletal muscle following muscle-damaging exercise. Furthermore, high doses should be avoided in formulating ginseng-based products.

Show MeSH
Related in: MedlinePlus