Maternal Exercise Improves High-Fat Diet-Induced Metabolic Abnormalities and Gut Microbiota Profiles in Mouse Dams and Offspring

Liyuan Zhou, Xinhua Xiao, Ming Li, Qian Zhang, Miao Yu, Jia Zheng, Mingqun Deng, Liyuan Zhou, Xinhua Xiao, Ming Li, Qian Zhang, Miao Yu, Jia Zheng, Mingqun Deng

Abstract

Early-life overnutrition programs increased risks of metabolic disorders in adulthood. Regular exercise has been widely accepted to be an effective measure to maintain metabolic health. However, the intergenerational effects of maternal exercise and the specific mechanism are largely unclear. Our objective was to investigate whether maternal exercise could alleviate the metabolic disturbances induced by early-life overnutrition in both dams and offspring and to explore the role of gut microbiota in mediating the effects. C57BL/6 female mice were randomly divided into three groups: the control group, which were fed a normal control diet; high-fat group, which received a high-fat diet; and high-fat with exercise intervention group, which was fed a high-fat diet and received a voluntary wheel running training. The diet intervention started from 3 weeks prior to mating and lasted throughout pregnancy and lactation. The exercise intervention was only prior to and during pregnancy. The male offspring got free access to normal chow diet from weaning to 24 weeks of age. Glucose tolerance test and biochemical parameters were detected in dams at weaning and offspring at 8 and 24 weeks of age. Their cecal contents were collected for the 16 s rDNA amplicon sequencing. The results showed that maternal high-fat diet resulted in significant glucose intolerance, insulin resistance, and lipid profiles disorders in both dams and offspring. Maternal exercise markedly improved insulin sensitivity in dams and metabolic disorders in offspring from young into adulthood. The decrease in unfavorable bacteria and the persistent enrichment of short-chain fatty acids-producers from mothers to adult offspring, particularly the genus Odoribacter, were all associated with the improvement of metabolism by maternal exercise. Overall, maternal exercise could significantly mitigate the detrimental effects of a maternal high-fat diet on metabolism in both dams and male offspring. The continuous alterations in gut microbiota might be a critical factor in deciphering the metabolic benefits of maternal exercise, which provides some novel evidence and targets for combating metabolic diseases.

Keywords: dams and offspring; glucose and lipid metabolism; gut microbiota; high-fat diet; intergeneration; voluntary wheel running.

Copyright © 2020 Zhou, Xiao, Li, Zhang, Yu, Zheng and Deng.

Figures

Figure 1
Figure 1
Glucose and lipid metabolism in dams at weaning. (A) Experimental scheme; (B) Average running distance per day of dams during 3 weeks before mating and throughout pregnancy; (C) Body weight in mothers at weaning; (D) Maternal blood glucose values following an intraperitoneal glucose tolerance test at weaning; (E) AUC of blood glucose values during an intraperitoneal glucose tolerance test; Insulin sensitivity analyses of dams: (F) Fasting insulin levels at weaning; and (G) HOMA-IR; Maternal serum lipid profiles at weaning: (H) TC; (I) TG; (J) LDL-C; and (K) FFA. MC, dams fed the normal control diet; MHF, dams fed the high-fat diet; MHFE, dams intervened with a high-fat diet and exercise. AUC, area under the curve; HOMA-IR, homeostasis model assessment of insulin resistance; TC, total cholesterol; TG, triacylglycerol; LDL-C, low-density lipoprotein cholesterol; FFA, free fatty acid. All of the data are expressed as means ± S.E.M. (MC, n = 8; MHF, n = 11; MHFE, n = 8 in each figure). The statistics were analyzed by one-way ANOVA and two-way ANOVA, with Turkey post hoc analyses. Mean values show significant differences between the MC group and the MHF group: *p < 0.05, **p < 0.01, ****p < 0.0001.
Figure 2
Figure 2
The alterations of gut microbiome in dams at weaning (MC, n = 8; MHF, n = 11; MHFE, n = 8 in each figure). (A) Venn diagram of the OUTs; (B) Relative abundance of the top 10 phyla; (C) Relative abundance of the top 20 species at the genus level; Different species analysis among the three groups: (D) Heatmap analysis of the different germs at the genus level; and (E) LEfSe analysis of the different intestinal microbiome from the phylum level to the genus level; Beta diversity analysis of gut microbiome: (F) PCoA plots of gut microbiome; and (G) ANOSIM analysis. MC, dams fed the normal control diet; MHF, dams fed the high-fat diet; MHFE, dams intervened with a high-fat diet and exercise.
Figure 3
Figure 3
Metabolic parameters in male offspring at 8 weeks of age. (A) Offspring body weight; (B) Blood glucose values following an intraperitoneal glucose tolerance test; (C) AUC of blood glucose levels during glucose tolerance test; Insulin sensitivity analyses of young offspring: (D) Fasting serum insulin levels; and (E) HOMA-IR; Fasting serum lipid profiles analysis in offspring at 8 weeks of age: (F) TC; (G) TG; (H) LDL-C; and (I) FFA. C, offspring of dams fed the normal control diet fed; HF, offspring of dams fed the high-fat diet; HFE, offspring of dams intervened with a high-fat diet and exercise. AUC, area under the curve; HOMA-IR, homeostasis model assessment of insulin resistance; TC, total cholesterol; TG, triacylglycerol; LDL-C, low-density lipoprotein cholesterol; FFA, free fatty acid. Data are expressed as means ± S.E.M. (C, n = 6; HF, n = 9; HFE, n = 6 in each figure). The statistics were analyzed by one-way ANOVA and two-way ANOVA, with Turkey post hoc analyses. Mean values show significant differences between C group and the HF group: *p < 0.05, **p < 0.01, ***p < 0.001; Mean values show significant differences between HF group and the HFE group during: #p < 0.05, ##p < 0.01, ###p < 0.001.
Figure 4
Figure 4
The changes of gut microbiome in male offspring at 8 weeks of age (C, n = 6; HF, n = 9; HFE, n = 6 in each figure). (A) Venn diagram of the OUTs; (B) Relative abundance of the top 10 species at the phylum level; (C) Relative abundance of the top 20 germs at the genus level; Different species analysis among the three groups: (D) Heatmap analysis of the different species at the genus level; (E) LEfSe analysis of the significantly enriched gut microbiome from the phylum level to the genus level; Beta diversity analysis of gut microbiome: (F) PCoA plots of gut microbiome; and (G) ANOSIM analysis. C, offspring of dams fed the normal control diet fed; HF, offspring of dams fed the high-fat diet; HFE, offspring of dams intervened with a high-fat diet and exercise.
Figure 5
Figure 5
Metabolic parameters in male offspring at 24 weeks of age. (A) Body weight; (B) Blood glucose values following an intraperitoneal glucose tolerance test; (C) AUC of blood glucose levels during glucose tolerance test; Insulin sensitivity analyses of offspring at 24 weeks: (D) Fasting serum insulin levels; and (E) HOMA-IR; Fasting serum lipid profiles analysis in offspring at 24 weeks of age: (F) TC; (G) TG; (H) LDL-C; and (I) FFA. OC, offspring of dams fed the normal control diet; OHF, offspring of dams fed the high-fat diet; OHFE, offspring of dams intervened with a high-fat diet and exercise. AUC, area under the curve; HOMA-IR, homeostasis model assessment of insulin resistance; TC, total cholesterol; TG, triacylglycerol; LDL-C, low-density lipoprotein cholesterol; FFA, free fatty acid. Data are expressed as means ± S.E.M. (OC, n = 8; OHF, n = 11; OHFE, n = 8 in each figure). The statistics were analyzed by one-way ANOVA and two-way ANOVA, with Turkey post hoc analyses. Mean values show significant differences between OC group and the OHF group: *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001; Mean values show significant differences between OHF group and the OHFE group: #p < 0.05, ##p < 0.01, ###p < 0.001, ####p < 0.0001.
Figure 6
Figure 6
The changes of gut microbiome in male offspring at 24 weeks of age (OC, n = 8; OHF, n = 11; OHFE, n = 8 in each figure). (A) Venn diagram of the OUTs; (B) Relative abundance of the top 10 germs at the phylum level; (C) Relative abundance of the top 20 species at the genus level; Different species analysis among the three groups: (D) Heatmap analysis of the different species at the genus level among the three group; and (E) LEfSe analysis of the significantly enriched gut microbiota from the phylum level to the genus level; Alpha diversity analysis of the gut microbiome in offspring at 24 weeks: (F) chao1; (G) observed_species; and (H) PD_whole_tree; Beta diversity analysis of gut microbiome: (I) PCoA plots of gut microbiome; and (J) ANOSIM analysis. OC, offspring of dams fed the normal control diet; OHF, offspring of dams fed the high-fat diet; OHFE, offspring of dams intervened with high-fat diet and exercise. Data are expressed as means ± S.E.M. Mean values show significant differences between the groups: *p < 0.05, **p < 0.01.
Figure 7
Figure 7
Heatmap of correlation analysis between the changed species at the genus level and glucose and lipid metabolic parameters in male offspring. (A) Correlation results in offspring at 8 weeks of age; and (B) Correlation results in offspring at 24 weeks of age. BW, body weight; BG0, blood glucose level at 0 min of GTT; BG30, blood glucose level at 30 min of GTT; BG60, blood glucose level at 60 min of GTT; BG120, blood glucose level at 120 min of GTT; AUC, area under the curve of GTT; HOMA-IR, the homeostasis model assessment of insulin resistance; TC, total cholesterol; TG, triglyceride; LDL-C, low-density lipoprotein cholesterol; and FFA, free fatty-acid. The statistics were analyzed by spearman correlation analysis. Values show significant correlation between the genera and metabolic parameters: +p < 0.05; *p < 0.01.

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