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Dietary resistant starch improves selected brain and behavioral functions in adult and aged rodents.

ABSTRACT: Resistant starch (RS) is a dietary fiber that exerts multiple beneficial effects. The current study explored the effects of dietary RS on selected brain and behavioral functions in adult and aged rodents. Because glucokinase (GK) expression in hypothalamic arcuate nucleus and area postrema of the brainstem is important for brain glucose sensing, GK mRNA was measured by brain nuclei microdissection and PCR. Adult RS-fed rats had a higher GK mRNA than controls in both brain nuclei, an indicator of improved brain glucose sensing. Next, we tested whether dietary RS improve selected behaviors in aged mice. RS-fed aged mice exhibited (i) an increased eating responses to fasting, a behavioral indicator of improvement in aged brain glucose sensing; (ii) a longer latency to fall from an accelerating rotarod, a behavioral indicator of improved motor coordination; and (iii) a higher serum active glucagon-like peptide-1 (GLP-1). Then, GLP-1 receptor null (GLP-1RKO) mice were used to test the role of GLP-1 in brain glucose sensing, and they exhibited impaired eating responses to fasting. We conclude that in rodents (i) dietary RS improves two important indicators of brain function: glucose sensing and motor coordination, and (ii) GLP-1 is important in the optimal feeding response to a fast.

SUBMITTER: Zhou J

PROVIDER: S-EPMC3892668 | biostudies-literature | 2013 Nov

REPOSITORIES: biostudies-literature

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Dietary resistant starch improves selected brain and behavioral functions in adult and aged rodents.

Zhou June J Keenan Michael J MJ Fernandez-Kim Sun Ok SO Pistell Paul J PJ Ingram Donald K DK Li Bing B Raggio Anne M AM Shen Li L Zhang Hanjie H McCutcheon Kathleen L KL Tulley Richard T RT Blackman Marc R MR Keller Jeffrey N JN Martin Roy J RJ

Molecular nutrition & food research 20130701 11

Resistant starch (RS) is a dietary fiber that exerts multiple beneficial effects. The current study explored the effects of dietary RS on selected brain and behavioral functions in adult and aged rodents. Because glucokinase (GK) expression in hypothalamic arcuate nucleus and area postrema of the brainstem is important for brain glucose sensing, GK mRNA was measured by brain nuclei microdissection and PCR. Adult RS-fed rats had a higher GK mRNA than controls in both brain nuclei, an indicator of ...[more]

PMID: 23818307

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Project description:UNLABELLED: BACKGROUND: Animal studies show that diets containing resistant starch (RS) at levels not achievable in the human diet result in lower body weight and/or adiposity in rodents. We aimed to determine whether RS dose-dependently reduces adiposity in obesity-prone (OP) and obesity-resistant (OR) rats. METHODS: Male Sprague-Dawley rats (n=120) were fed a moderate-fat, high-energy diet for 4 wk. Rats that gained the most weight (40%) were classified as obesity-prone (OP) and obesity-resistant (OR) rats were the 40% that gained the least weight. OP and OR rats were randomly allocated to one of six groups (n=8 for each phenotype). One group was killed for baseline measurements, the other five groups were allocated to AIN-93 based diets that contained 0, 4, 8, 12 and 16% RS (as high amylose maize starch) for 4 wk. These diets were matched for total carbohydrate content. At 0, 4 and 7 wk from the start of the study insulin sensitivity was calculated by homeostasis model assessment of insulin resistance (HOMA-IR) and adiposity was determined by dual-energy X-ray absorptiometry (DXA). At 8 wk, rats were euthanized and fat pad weights, intestinal digesta short chain fatty acid (SCFA) pools and plasma gut hormone levels were determined. RESULTS: Obesity prone rats gained less weight with 4, 12 and 16% RS compared to 0% RS, but the effect in OR animals was significant only at 16% RS. Irrespective of phenotype, diets containing ?8% RS reduced adiposity compared to 0% RS. Energy intake decreased by 9.8 kJ/d for every 4% increase in RS. All diets containing RS increased total SCFA pools in the caecum and lowered plasma GIP concentrations compared to the 0% RS, whereas plasma GLP-1 and PYY were increased when the diet contained at least 8% RS. Insulin sensitivity was not affected by RS. CONCLUSION: RS in amounts that could be potentially consumed by humans were effective in reducing adiposity and weight gain in OP and OR rats, due in part to a reduction in energy intake, and changes in gut hormones and large bowel carbohydrate fermentation.

Project description:Diet can influence the composition of the human microbiome, and yet relatively few dietary ingredients have been systematically investigated with respect to their impact on the functional potential of the microbiome. Dietary resistant starch (RS) has been shown to have health benefits, but we lack a mechanistic understanding of the metabolic processes that occur in the gut during digestion of RS. Here, we collected samples during a dietary crossover study with diets containing large or small amounts of RS. We determined the impact of RS on the gut microbiome and metabolic pathways in the gut, using a combination of "omics" approaches, including 16S rRNA gene sequencing, metaproteomics, and metabolomics. This multiomics approach captured changes in the abundance of specific bacterial species, proteins, and metabolites after a diet high in resistant starch (HRS), providing key insights into the influence of dietary interventions on the gut microbiome. The combined data showed that a high-RS diet caused an increase in the ratio of Firmicutes to Bacteroidetes, including increases in relative abundances of some specific members of the Firmicutes and concurrent increases in enzymatic pathways and metabolites involved in lipid metabolism in the gut.IMPORTANCE This work was undertaken to obtain a mechanistic understanding of the complex interplay between diet and the microorganisms residing in the intestine. Although it is known that gut microbes play a key role in digestion of the food that we consume, the specific contributions of different microorganisms are not well understood. In addition, the metabolic pathways and resultant products of metabolism during digestion are highly complex. To address these knowledge gaps, we used a combination of molecular approaches to determine the identities of the microorganisms in the gut during digestion of dietary starch as well as the metabolic pathways that they carry out. Together, these data provide a more complete picture of the function of the gut microbiome in digestion, including links between an RS diet and lipid metabolism and novel linkages between specific gut microbes and their metabolites and proteins produced in the gut.

Project description:Resistant starch (RS) is fermentable by gut microbiota and effectively modulates fecal short-chain fatty acid concentrations in pigs, mice, and humans. RS may have similar beneficial effects on the canine gut but has not been well studied. The objective of this study was to evaluate the effects of 0%, 1%, 2%, 3%, and 4% dietary RS (Hi-maize 260) on apparent total tract macronutrient digestibility, fecal characteristics, fermentative end-product concentrations, and microbiota of healthy adult dogs. An incomplete 5 × 5 Latin square design with seven dogs and five experimental periods was used, with each treatment period lasting 21 d (days 0 to 17 adaptation; days 18 to 21 fresh and total fecal collection) and each dog serving as its own control. Seven dogs (mean age = 5.3 yr; mean body weight = 20 kg) were randomly allotted to one of five treatments formulated to be iso-energetic and consisting of graded amounts of 100% amylopectin cornstarch, RS, and cellulose and fed as a top dressing on the food each day. All dogs were fed the same amount of a basal diet throughout the study, and fresh water was offered ad libitum. The basal diet contained 6.25% RS (dry matter [DM] basis), contributing approximately 18.3 g of RS/d based on their daily food intake (292.5 g DM/d). Data were evaluated for linear and quadratic effects using SAS. The treatments included 0%, 1%, 2%, 3%, and 4% of an additional RS source. Because Hi-maize 260 is approximately 40% digestible and 60% indigestible starch, the dogs received the following amounts of RS daily: 0% = 18.3 g (18.3 + 0 g), 1% = 20.1 g (18.3 + 1.8 g), 2% = 21.9 g (18.3 + 3.6 g), 3% = 23.7 g (18.3 + 5.4 g), and 4% = 25.5 g (18.3 + 7.2 g). Apparent total tract DM, organic matter, crude protein, fat, and gross energy digestibilities and fecal pH were linearly decreased (P < 0.05) with increased RS consumption. Fecal output was linearly increased (P < 0.05) with increased RS consumption. Fecal scores and fecal fermentative end-product concentrations were not affected by RS consumption. Although most of the fecal microbial taxa were not altered, Faecalibacterium were increased (P < 0.05) with increased RS consumption. The decrease in fecal pH and increase in fecal Faecalibacterium would be viewed as being beneficial to gastrointestinal health. Although our results seem to indicate that RS is poorly and/or slowly fermentable in dogs, the lack of observed change may have been due to the rather high level of RS contained in the basal diet.

Project description:The increasing recognition that the gut microbiota plays a central role in behavior and cognition suggests that the manipulation of microbial taxa through diet may provide a means by which behavior may be altered in a reproducible and consistent manner in order to achieve a beneficial outcome for the host. Resistant starch continues to receive attention as a dietary intervention that can benefit the host through mechanisms that include altering the intestinal microbiota. Given the interest in dietary approaches to improve health, the aim of this study was to investigate whether the use of dietary resistant starch in mice to alter the gut microbiota also results in a change in behavior. Forty-eight 6 week-old male Swiss-Webster mice were randomly assigned to 3 treatment groups (n = 16 per group) and fed either a normal corn starch diet (NCS) or diets rich in resistant starches HA7 diet (HA7) or octenyl-succinate HA7 diet (OS-HA7) for 6 week and monitored for weight, behavior and fecal microbiota composition. Animals fed an HA7 diet displayed comparable weight gain over the feeding period to that recorded for NCS-fed animals while OS-HA7 displayed a lower weight gain as compared to either NCS or HA7 animals (ANOVA p = 0.0001; NCS:HA7 p = 0.244; HA7:OS-HA7 p<0.0001; NCS:OS-HA7 p<0.0001). Analysis of fecal microbiota using 16s rRNA gene taxonomic profiling revealed that each diet corresponded with a unique gut microbiota. The distribution of taxonomic classes was dynamic over the 6 week feeding period for each of the diets. At the end of the feeding periods, the distribution of taxa included statistically significant increases in members of the phylum Proteobacteria in OS-HA7 fed mice, while the Verrucomicrobia increased in HA7 fed mice over that of mice fed OS-HA7. At the class level, members of the class Bacilli decreased in the OS-HA7 fed group, and Actinobacteria, which includes the genus Bifidobacteria, was enriched in the HA7 fed group compared to the control diet. Behavioral analysis revealed that animals demonstrated profound anxiety-like behavior as observed by performance on the elevated-plus maze with time spent by the mice in the open arm (ANOVA p = 0.000; NCS:HA7 p = 0.004; NCS:OS-HA7 p = 1.000; HA7:OS-HA7 p = 0.0001) as well as entries in the open arm (ANOVA p = 0.039; NCS:HA7 p = 0.041; HA7:OS-HA7 p = 0.221; NCS:OS-HA7 p = 1.000). Open-field behavior, a measure of general locomotion and exploration, revealed statistically significant differences between groups in locomotion as a measure of transitions across quadrant boundaries. Additionally, the open-field assay revealed decreased exploration as well as decreased rearing in HA7 and OS-HA7 fed mice demonstrating a consistent pattern of increased anxiety-like behavior among these groups. Critically, behavior was not correlated with weight. These results indicate that diets based on resistant starch can be utilized to produce quantifiable changes in the gut microbiota and should be useful to "dial-in" a specific microbiome that is unique to a particular starch composition. However, undesirable effects can also be associated with resistant starch, including lack of weight gain and increased anxiety-like behaviors. These observations warrant careful consideration when developing diets rich in resistant starch in humans and animal models.

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Dietary resistant starch improves selected brain and behavioral functions in adult and aged rodents.

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Dietary resistant starch improves selected brain and behavioral functions in adult and aged rodents.

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