Dietary switch to Western diet induces hypothalamic adaptation associated with gut microbiota dysbiosis in rats

Fouesnard, Mélanie; Zoppi, Johanna; Petera, Mélanie; Gléau, Léa Le; Migné, Carole; Devime, Fabienne; Durand, Stéphanie; Bénani, Alexandre; Chaffron, Samuel; Douard, Véronique; Boudry, Gaëlle

doi:10.1038/s41366-021-00796-4

Cited by 15 publications

(14 citation statements)

References 61 publications

(69 reference statements)

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“…Cecal metabolites also correlated with hypothalamic metabolites-one notable association was seen between oxidative stress and indices of α-diversity. This demonstrates an immediate pro-inflammatory microbiome shift within 1 day of WD feeding that coincides with alterations in hypothalamic oxidative stress and hyperphagia [95]. Interestingly, in conventionally raised, but not GF, rats, RNA expression of superoxide dismutase 2, glutaredoxin, and IL-6 are increased after 2 days of WD feeding, demonstrating that the microbiota is necessary for the early pro-inflammatory effects of WD in the hypothalamus.…”

Section: Neuroinflammationmentioning

confidence: 77%

“…Besides altering sensitivity to leptin and CCK, bacterial inflammatory products produced by the obese-type microbiome are linked to inflammation and loss of function in key brain regions involved in food intake-the NTS, as previously discussed, and the hypothalamus [95][96][97]. The hypothalamus contains key anorexigenic and orexigenic neuronal populations involved in regulating appetite and energy expenditure.…”

Section: Neuroinflammationmentioning

confidence: 96%

“…WD-fed rats exhibited hyperphagia in the first week of feeding, increased weight gain, and adiposity. Metabolomic changes were observed in the hypothalamus within 2 h of diet introduction, and these changes persisted after the first day of feeding [95]. Specific alterations included hypothalamic redox homeostasis (increased oxidized glutathione, among other measures, suggests increased oxidative stress) and cell membrane remodeling processes.…”

Section: Neuroinflammationmentioning

confidence: 99%

“…Oxidative stress is another inflammatory measure that is increased in DIO rats and may be related to microbiome composition. In a study by Fouesnard et al, rats were placed on either a chow or high-energy Western diet (WD; 45% fat) for 6 weeks [95]. WD-fed rats exhibited hyperphagia in the first week of feeding, increased weight gain, and adiposity.…”

Section: Neuroinflammationmentioning

confidence: 99%

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Microbiota’s Role in Diet-Driven Alterations in Food Intake: Satiety, Energy Balance, and Reward

Rautmann

Serre

2021

Nutrients

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The gut microbiota plays a key role in modulating host physiology and behavior, particularly feeding behavior and energy homeostasis. There is accumulating evidence demonstrating a role for gut microbiota in the etiology of obesity. In human and rodent studies, obesity and high-energy feeding are most consistently found to be associated with decreased bacterial diversity, changes in main phyla relative abundances and increased presence of pro-inflammatory products. Diet-associated alterations in microbiome composition are linked with weight gain, adiposity, and changes in ingestive behavior. There are multiple pathways through which the microbiome influences food intake. This review discusses these pathways, including peripheral mechanisms such as the regulation of gut satiety peptide release and alterations in leptin and cholecystokinin signaling along the vagus nerve, as well as central mechanisms, such as the modulation of hypothalamic neuroinflammation and alterations in reward signaling. Most research currently focuses on determining the role of the microbiome in the development of obesity and using microbiome manipulation to prevent diet-induced increase in food intake. More studies are necessary to determine whether microbiome manipulation after prolonged energy-dense diet exposure and obesity can reduce intake and promote meaningful weight loss.

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Section: Neuroinflammationmentioning

confidence: 77%

Section: Neuroinflammationmentioning

confidence: 96%

Section: Neuroinflammationmentioning

confidence: 99%

Section: Neuroinflammationmentioning

confidence: 99%

See 2 more Smart Citations

Microbiota’s Role in Diet-Driven Alterations in Food Intake: Satiety, Energy Balance, and Reward

Rautmann

Serre

2021

Nutrients

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“…The translation of the WD to animal studies is accomplished by dietary formulations with significantly elevated levels of saturated fats and sucrose and has revealed similar consequences to prolonged intake of this diet. The WD has been shown to yield increased effects of neuroinflammation and impair cognition in both humans and rodents [ 26 , 29 , 30 , 31 , 32 ] and has been implicated as a causal pathway to LOAD development, especially as it relates to midlife dietary patterns [ 33 , 34 ]. Murine models have demonstrated WD exposure results in impaired glucose tolerance [ 35 ].…”

Section: Introductionmentioning

confidence: 99%

Sex Differences in Metabolic Indices and Chronic Neuroinflammation in Response to Prolonged High-Fat Diet in ApoE4 Knock-In Mice

Mattar

Majchrzak

Iannucci

et al. 2022

IJMS

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Late-onset Alzheimer’s disease (LOAD) likely results from combinations of risk factors that include both genetic predisposition and modifiable lifestyle factors. The E4 allele of apolipoprotein E (ApoE) is the most significant genetic risk factor for LOAD. A Western-pattern diet (WD) has been shown to strongly increase the risk of cardiovascular disease and diabetes, conditions which have been strongly linked to an increased risk for developing AD. Little is known about how the WD may contribute to, or enhance, the increased risk presented by possession of the ApoE4 allele. To model this interaction over the course of a lifetime, we exposed male and female homozygote ApoE4 knock-in mice and wild-type controls to nine months of a high-fat WD or standard chow diet. At eleven months of age, the mice were tested for glucose tolerance and then for general activity and spatial learning and memory. Postmortem analysis of liver function and neuroinflammation in the brain was also assessed. Our results suggest that behavior impairments resulted from the convergence of interacting metabolic alterations, made worse in a male ApoE4 mice group who also showed liver dysfunction, leading to a higher level of inflammatory cytokines in the brain. Interestingly, female ApoE4 mice on a WD revealed impairments in spatial learning and memory without the observed liver dysfunction or increase in inflammatory markers in the brain. These results suggest multiple direct and indirect pathways through which ApoE and diet-related factors interact. The striking sex difference in markers of chronic neuroinflammation in male ApoE4 mice fed the high-fat WD suggests a specific mechanism of interaction conferring significant enhanced LOAD risk for humans with the ApoE4 allele, which may differ between sexes. Additionally, our results suggest researchers exercise caution when designing and interpreting results of experiments employing a WD, being careful not to assume a WD impacts both sexes by the same mechanisms.

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Obesogenic Diet Cycling Produces Graded Effects on Cognition and Microbiota Composition in Rats

Kendig

Leigh

Hasebe

et al. 2023

Molecular Nutrition Food Res

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Scope The effects of diet cycling on cognition and fecal microbiota are not well understood. Method and Results Adult male Sprague‐Dawley rats were cycled between a high‐fat, high‐sugar “cafeteria” diet (Caf) and regular chow. The impairment in place recognition memory produced by 16 days of Caf diet was reduced by switching to chow for 11 but not 4 days. Next, rats received 16 days of Caf diet in 2, 4, 8, or 16‐day cycles, each separated by 4‐day chow cycles. Place recognition memory declined from baseline in all groups and was impaired in the 16‐ versus 2‐day group. Finally, rats received 24 days of Caf diet continuously or in 3‐day cycles separated by 2‐ or 4‐day chow cycles. Any Caf diet access impaired cognition and increased adiposity relative to controls, without altering hippocampal gene expression. Place recognition and adiposity were the strongest predictors of global microbiota composition. Overall, diets with higher Caf > chow ratios produced greater spatial memory impairments and larger shifts in gut microbiota species richness and beta diversity. Conclusion Results suggest that diet‐induced cognitive deficits worsen in proportion to unhealthy diet exposure, and that shifting to a healthy chow for at least a week is required for recovery under the conditions tested here.

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Dietary switch to Western diet induces hypothalamic adaptation associated with gut microbiota dysbiosis in rats

Cited by 15 publications

References 61 publications

Microbiota’s Role in Diet-Driven Alterations in Food Intake: Satiety, Energy Balance, and Reward

Microbiota’s Role in Diet-Driven Alterations in Food Intake: Satiety, Energy Balance, and Reward

Sex Differences in Metabolic Indices and Chronic Neuroinflammation in Response to Prolonged High-Fat Diet in ApoE4 Knock-In Mice

Obesogenic Diet Cycling Produces Graded Effects on Cognition and Microbiota Composition in Rats

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