Exercise Prevents Weight Gain and Alters the Gut Microbiota in a Mouse Model of High Fat Diet-Induced Obesity

Evans, Christian C.; LePard, Kathy J.; Kwak, Jeff; Stancukas, Mary C.; Laskowski, Samantha; Dougherty, Joseph D.; Moulton, Laura J.; Glawe, A.; Wang, Yunwei; Leone, Vanessa; Antonopoulos, Dionysios A.; Smith, Dan; Chang, Eugene B.; Ciancio, Mae J.

doi:10.1371/journal.pone.0092193

Cited by 482 publications

(463 citation statements)

References 68 publications

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“…Thus, it can be seen that voluntary exercise partially, but significantly induces changes in the gut microbiota. Previously, voluntary exercise for 12 weeks was shown to prevent weight gain and was associated with a relative increase in Bacteroidetes in HFD-fed mice 2) . However, it was unclear whether or not the exercise habit (voluntary exercise) was transmitted via the altered gut microbiota.…”

Section: Resultsmentioning

confidence: 97%

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Altered gut microbiota by voluntary exercise induces high physical activity in high-fat diet mice

Oyanagi

Uchida

Kremenik

et al. 2018

JPFSM

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In the present study, we determined whether or not exercise-induced high physical activity could be transmitted via altered gut microbiota. We collected cecal material from male C57BL/6N mice for 12 weeks under two conditions: voluntary wheel running (EX) and sedentary condition (SED). After depleting endogenous gut microbiota, cecal microbiota transplantation (CMT) was initiated in the recipient mice by placing cecal contents of either EX or SED mice into the oral cavity directly with the feeding of a high-fat diet (HFD). After a breeding period of 8 weeks, the physical activity test of the HFD (EX-CMT and SED-CMT) mice was examined. Although EX donor mice were attenuated with increasing body mass and body fat, and induced hypertrophy of the heart was compared with SED donor mice, those parameters did not show any difference between EX-CMT and SED-CMT mice. Nevertheless, high physical activity was observed in EX-CMT mice compared to SED-CMT mice (p < 0.01). These results suggest that exercise-induced high physical activity might be transmitted to un-exercised HFD mice via its altered gut microbiota.

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Section: Resultsmentioning

confidence: 97%

“…In addition, recent studies investigating the effects of physical exercise in experimental animal models have shown that it might induce changes in the gut microbiota [2][3][4] .…”

Section: Introductionmentioning

confidence: 99%

Altered gut microbiota by voluntary exercise induces high physical activity in high-fat diet mice

Oyanagi

Uchida

Kremenik

et al. 2018

JPFSM

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“…These two families contain bacteria associated with butyrate-production and are found in low-abundance in sedentary women, hypertensive Dahl salt-sensitive rats, and HFD mice fecal microbiota. 30 , 139 , 140 …”

Section: Discussionmentioning

confidence: 99%

Prenatal androgen exposure causes hypertension and gut microbiota dysbiosis

et al. 2018

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Background: Conditions of excess androgen in women, such as polycystic ovary syndrome (PCOS), often exhibit intergenerational transmission. One way in which the risk for PCOS may be increased in daughters of affected women is through exposure to elevated androgens in utero. Hyperandrogenemic conditions have serious health consequences, including increased risk for hypertension and cardiovascular disease. Recently, gut dysbiosis has been found to induce hypertension in rats, such that blood pressure can be normalized through fecal microbial transplant. Therefore, we hypothesized that the hypertension seen in PCOS has early origins in gut dysbiosis caused by in utero exposure to excess androgen. We investigated this hypothesis with a model of prenatal androgen (PNA) exposure and maternal hyperandrogenemia by single-injection of testosterone cypionate or sesame oil vehicle (VEH) to pregnant dams in late gestation. We then completed a gut microbiota and cardiometabolic profile of the adult female offspring. Results: The metabolic assessment revealed that adult PNA rats had increased body weight and increased mRNA expression of adipokines: adipocyte binding protein 2, adiponectin, and leptin in inguinal white adipose tissue. Radiotelemetry analysis revealed hypertension with decreased heart rate in PNA animals. The fecal microbiota profile of PNA animals contained higher relative abundance of bacteria associated with steroid hormone synthesis, Nocardiaceae and Clostridiaceae, and lower abundance of Akkermansia, Bacteroides, Lactobacillus, Clostridium. The PNA animals also had an increased relative abundance of bacteria associated with biosynthesis and elongation of unsaturated short chain fatty acids (SCFAs). Conclusions: We found that prenatal exposure to excess androgen negatively impacted cardiovascular function by increasing systolic and diastolic blood pressure and decreasing heart rate. Prenatal androgen was also associated with gut microbial dysbiosis and altered abundance of bacteria involved in metabolite production of short chain fatty acids. These results suggest that early-life exposure to hyperandrogenemia in daughters of women with PCOS may lead to long-term alterations in gut microbiota and cardiometabolic function.

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“…Furthermore, PTE treatment caused a reduction in both Lachnospiraceae and Ruminococcaceae populations, which positively correlate with obesity, in subjects fed a HFD [66,67]. In addition, PTE treatment restored the HFD-mediated reduction in the S24-7 population (a Bacteroidetes phylum), an effect also observed when subjects’ physical activity levels are increased [68]. …”

Section: Discussionmentioning

confidence: 99%

Polygala tenuifolia extract inhibits lipid accumulation in 3T3-L1 adipocytes and high-fat diet–induced obese mouse model and affects hepatic transcriptome and gut microbiota profiles

Wang

Yen

Cheng

et al. 2017

Food & Nutrition Research

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Obesity, the excessive accumulation of lipids in the body, is closely associated with many prevalent human disorders. Continued efforts to identify plant extracts that exhibit anti-obesity effects have drawn much attention. This study investigated whether a Polygala tenuifolia extract (PTE) possesses anti-obesity activity and how PTE may affect liver gene expression and gut microbiota. We used 3T3-L1 adipocytes and a high-fat diet–induced obese mouse model to determine the effects of PTE on lipid accumulation. Next-generation sequencing analysis of liver gene expression and gut microbiota profiles following PTE treatment were conducted to elucidate possible mechanisms. We found that treatment of fully differentiated 3T3-L1 adipocytes with PTE inhibited lipid accumulation in the cells through reducing lipid formation and triglyceride content and by increasing lipase activity. No cytotoxicity was observed from the PTE treatment. After 5 weeks of treatment with PTE, the increased body weight, elevated serum triglyceride content, and liver steatosis in the high-fat diet–induced obese mice were each reduced. Liver transcriptomic analysis revealed that expression of genes involved in lipid and cholesterol metabolism was significantly altered. The low-grade chronic inflammation of obesity caused by a high-fat diet was also decreased after PTE treatment. In addition, treatment with PTE improved the relatively low Bacteroidetes/Firmicutes ratio in the gut of high-fat diet–fed mice through enrichment of the Proteobacteria population and reduction of the Deferribacteres population. In conclusion, treatment with PTE inhibited lipid accumulation by inducing the expression of the master transcription factor PPARα, attenuated the low-grade chronic inflammation of obesity, and also altered gut microbiota profiles. These results indicate that PTE has the potential to be developed into an anti-obesity food supplement and therapy. Abbreviations: Abcg5: ATP-binding cassette subfamily G member 5; ALT: alanine aminotransferase; AMPK: adenosine monophosphate-activated protein kinase; AST: aspartate aminotransferase; B/F: Bacteroidetes to Firmicutes [ratio]; C/EBPα: CCAAT/enhancer-binding protein alpha; CR: creatinine; Cyp51: cytochrome P450 family 51; DMEM: Dulbecco’s modified Eagle’s medium; Fabp5: fatty acid-binding protein 5; FBS: fetal bovine serum; Fdps: farnesyl diphosphate synthase; Glc: Glucose; HFD: high-fat diet; GO: gene ontology; HPRT: hypoxanthine guanine phosphoribosyl transferase; IBMS: 3-isobutyl-1-methylxanthine; Idi1: isopentenyl-diphosphate delta isomerase 1; IL-1β: interleukin-1-beta; Lpin1: phosphatidic acid phosphohydrolase; LPS: lipopolysaccharide; Mvd: mevalonate diphosphate decarboxylase; ND: normal diet; OTU: operational taxonomic units; Pcsk9: proprotein convertase subtilisin/kexin 9; Pctp: phosphatidylcholine transfer protein; PPARα: peroxisome proliferator-activated receptor alpha; PPARγ: peroxisome proliferator-activated receptor gamma; PTE: Polygala tenuifolia extract; Saa1: serum amyloid A1; SD: ...

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Exercise Prevents Weight Gain and Alters the Gut Microbiota in a Mouse Model of High Fat Diet-Induced Obesity

Cited by 482 publications

References 68 publications

Altered gut microbiota by voluntary exercise induces high physical activity in high-fat diet mice

Altered gut microbiota by voluntary exercise induces high physical activity in high-fat diet mice

Prenatal androgen exposure causes hypertension and gut microbiota dysbiosis

Polygala tenuifolia extract inhibits lipid accumulation in 3T3-L1 adipocytes and high-fat diet–induced obese mouse model and affects hepatic transcriptome and gut microbiota profiles

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