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      Dietary inulin alleviates diverse stages of type 2 diabetes mellitus via anti-inflammation and modulating gut microbiota in db/db mice

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          Abstract

          Type 2 diabetes mellitus (T2DM) is closely correlated with chronic low-grade inflammation and gut dysbiosis.

          Abstract

          Type 2 diabetes mellitus (T2DM) is closely correlated with chronic low-grade inflammation and gut dysbiosis. Prebiotic inulin (INU) is conducive to modulate gut dysbiosis. However, the impact of dietary inulin on the diverse stages of T2DM remains largely unknown. In the present study, according to the fasting blood glucose (FBG) and oral glucose tolerance tests (OGTT), mice were randomly divided into six groups (15 mice per group): pre-diabetic group (PDM group); inulin-treated pre-diabetic group (INU/PDM group); early diabetic group (EDM group); inulin-treated early diabetic group (INU/EDM group); diabetic group (DM group); inulin-treated diabetic group (INU/DM group). All animal experiments were approved by the Ethics Committee of the General Hospital of Ningxia Medical University (No. 2016-232). After 6 weeks of inulin intervention, the mice were euthanized and the associated indicators were investigated. Dietary inulin significantly reduced FBG, body weights (BWs), glycated hemoglobin (GHb), blood lipid, plasma lipopolysaccharide (LPS), interleukin (IL)-6, tumor necrosis factor (TNF)-α and IL-17A in the three inulin-treated groups compared to the untreated groups. But for IL-17A, there remained no significant difference between the PDM group and the INU/PDM group. Moreover, the anti-inflammatory IL-10 showed significant alteration in the INU/PDM and INU/EDM groups, but no significant alteration in the INU/DM group. Sequencing analysis of the gut microbiota showed an elevation in the relative abundance of Cyanobacteria and Bacteroides and a reduction in the relative abundance of Ruminiclostridium_6 in three inulin-treated different stages of T2DM groups, as well as a reduction in the relative abundance of Deferribacteres and Tenericutes in the INU/DM group. A reduction in the relative abundance of Mucispirillum was detected in the INU/PDM and INU/EDM groups. Correlation analysis revealed that Cyanobacteria and Bacteroides abundance were positively correlated with IL-10; Deferribacteres, Tenericutes, Mucispirillum and Ruminiclostridium_6 abundance were closely related to IL-6, TNF-α or IL-17A respectively. Additionally, Mucispirillum and Ruminiclostridium_6 abundance were positively correlated with LPS. Taken together, dietary inulin alleviated the diverse stages of T2DM via suppressing inflammation and modulating gut microbiota.

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          Most cited references36

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          Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study.

          A subclinical inflammatory reaction has been shown to precede the onset of type 2 (non-insulin-dependent) diabetes. We therefore examined prospectively the effects of the central inflammatory cytokines interleukin (IL)-1beta, IL-6, and tumor necrosis factor-alpha (TNF-alpha) on the development of type 2 diabetes. We designed a nested case-control study within the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam study including 27,548 individuals. Case subjects were defined to be those who were free of type 2 diabetes at baseline and subsequently developed type 2 diabetes during a 2.3-year follow-up period. A total of 192 cases of incident type 2 diabetes were identified and matched with 384 non-disease-developing control subjects. IL-6 and TNF-alpha levels were found to be elevated in participants with incident type 2 diabetes, whereas IL-1beta plasma levels did not differ between the groups. Analysis of single cytokines revealed IL-6 as an independent predictor of type 2 diabetes after adjustment for age, sex, BMI, waist-to-hip ratio (WHR), sports, smoking status, educational attainment, alcohol consumption, and HbA(1c) (4th vs. the 1st quartile: odds ratio [OR] 2.6, 95% CI 1.2-5.5). The association between TNF-alpha and future type 2 diabetes was no longer significant after adjustment for BMI or WHR. Interestingly, combined analysis of the cytokines revealed a significant interaction between IL-1beta and IL-6. In the fully adjusted model, participants with detectable levels of IL-1beta and elevated levels of IL-6 had an independently increased risk to develop type 2 diabetes (3.3, 1.7-6.8), whereas individuals with increased concentrations of IL-6 but undetectable levels of IL-1beta had no significantly increased risk, both compared with the low-level reference group. These results were confirmed in an analysis including only individuals with HbA(1c) <5.8% at baseline. Our data suggest that the pattern of circulating inflammatory cytokines modifies the risk for type 2 diabetes. In particular, a combined elevation of IL-1beta and IL-6, rather than the isolated elevation of IL-6 alone, independently increases the risk of type 2 diabetes. These data strongly support the hypothesis that a subclinical inflammatory reaction has a role in the pathogenesis of type 2 diabetes.
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            Butyrate and other short-chain fatty acids as modulators of immunity: what relevance for health?

            High-fiber diets have been shown to reduce plasma concentrations of inflammation markers. Increased production of fermentation-derived short-chain fatty acids (SCFAs) is one of the factors that could exert these positive effects. This review examines the effects of SCFAs on immune cells and discusses the relevance of their effects on systemic inflammation, as frequently seen in obesity. SCFAs have been shown to reduce chemotaxis and cell adhesion; this effect is dependent on type and concentration of SCFA. In spite of conflicting results, especially butyrate seems to have an anti-inflammatory effect, mediated by signaling pathways like nuclear factor-κB and inhibition of histone deacetylase. The discrepancies in the results could be explained by differences in cell types used and their proliferative and differentiation status. SCFAs show anti-inflammatory effects and seem to have the potency to prevent infiltration of immune cells from the bloodstream in, for example, the adipose tissue. In addition, their ability to inhibit the proliferation and activation of T cells and to prevent adhesion of antigen-presenting cells could be important as it recently has been shown that obesity-associated inflammation might be antigen-dependent. More studies with concentrations in micromolar range are needed to approach more physiological concentrations.
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              Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis.

              Human inflammatory bowel disease and experimental colitis models in mice are associated with shifts in intestinal microbiota composition, but it is unclear at what taxonomic/phylogenetic level such microbiota dynamics can be indicative for health or disease. Here, we report that dextran sodium sulfate (DSS)-induced colitis is accompanied by major shifts in the composition and function of the intestinal microbiota of STAT1(-/-) and wild-type mice, as determined by 454 pyrosequencing of bacterial 16S rRNA (gene) amplicons, metatranscriptomics and quantitative fluorescence in situ hybridization of selected phylotypes. The bacterial families Ruminococcaceae, Bacteroidaceae, Enterobacteriaceae, Deferribacteraceae and Verrucomicrobiaceae increased in relative abundance in DSS-treated mice. Comparative 16S rRNA sequence analysis at maximum possible phylogenetic resolution identified several indicator phylotypes for DSS treatment, including the putative mucin degraders Akkermansia and Mucispirillum. The analysis additionally revealed strongly contrasting abundance changes among phylotypes of the same family, particularly within the Lachnospiraceae. These extensive phylotype-level dynamics were hidden when reads were grouped at higher taxonomic levels. Metatranscriptomic analysis provided insights into functional shifts in the murine intestinal microbiota, with increased transcription of genes associated with regulation and cell signaling, carbohydrate metabolism and respiration and decreased transcription of flagellin genes during inflammation. These findings (i) establish the first in-depth inventory of the mouse gut microbiota and its metatranscriptome in the DSS colitis model, (ii) reveal that family-level microbial community analyses are insufficient to reveal important colitis-associated microbiota shifts and (iii) support a scenario of shifting intra-family structure and function in the phylotype-rich and phylogenetically diverse Lachnospiraceae in DSS-treated mice.
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                Author and article information

                Journal
                FFOUAI
                Food & Function
                Food Funct.
                Royal Society of Chemistry (RSC)
                2042-6496
                2042-650X
                April 17 2019
                2019
                : 10
                : 4
                : 1915-1927
                Affiliations
                [1 ]Clinical Medical College
                [2 ]Ningxia Medical University
                [3 ]Yinchuan 750004
                [4 ]China
                [5 ]Endocrinology Department
                [6 ]General Hospital of Ningxia Medical University
                [7 ]Department of Pathogenic Biology and Medical Immunology
                [8 ]School of Basic Medical Sciences
                [9 ]College of Traditional Chinese Medicine
                [10 ]The Center for Reproductive Medicine
                Article
                10.1039/C8FO02265H
                30869673
                5fe4bd32-80a0-423a-adb2-2b279fa461e3
                © 2019

                http://rsc.li/journals-terms-of-use

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