Integration of microbial metabolomics and microbiomics uncovers a novel mechanism underlying the antidiabetic property of stachyose

Adeshirlarijaney, 2020, Considering gut microbiota in treatment of type 2 diabetes mellitus, Gut Microbes, 11, 253, 10.1080/19490976.2020.1717719 Agus, 2018, Gut Microbiota Regulation of Tryptophan Metabolism in Health and Disease, Cell Host & Microbe, 23, 716, 10.1016/j.chom.2018.05.003 Ahern, 2021, Measuring Conjugated Linoleic Acid (CLA) Production by Bifidobacteria, Methods in Molecular Biology (Clifton N.J.), 2278, 87, 10.1007/978-1-0716-1274-3_8 Amato, K. R., Arrieta, M.-C., Azad, M. B., Bailey, M. T., Broussard, J. L., Bruggeling, C. E., Claud, E. C., Costello, E. K., Davenport, E. R., Dutilh, B. E., Swain Ewald, H. A., Ewald, P., Hanlon, E. C., Julion, W., Keshavarzian, A., Maurice, C. F., Miller, G. E., Preidis, G. A., Segurel, L., … Kuzawa, C. W. (2021). The human gut microbiome and health inequities. Proceedings of the National Academy of Sciences of the United States of America, 118(25), e2017947118. https://doi.org/10.1073/pnas.2017947118. Aragozzini, 1979, Indole-3-lactic acid as a tryptophan metabolite produced by Bifidobacterium spp, Applied and Environmental Microbiology, 38, 544, 10.1128/aem.38.3.544-546.1979 Brody, 2020, The gut microbiome, Nature, 577, S5, 10.1038/d41586-020-00194-2 Cai, 2022, Gut microbiota-derived bile acids in intestinal immunity, inflammation, and tumorigenesis, Cell Host & Microbe, 30, 289, 10.1016/j.chom.2022.02.004 Campbell, 2020, Bacterial metabolism of bile acids promotes generation of peripheral regulatory T cells, Nature, 581, 475, 10.1038/s41586-020-2193-0 Cao, 2020, Stachyose Improves the Effects of Berberine on Glucose Metabolism by Regulating Intestinal Microbiota and Short-Chain Fatty Acids in Spontaneous Type 2 Diabetic KKAy Mice, Frontiers in Pharmacology, 11, 10.3389/fphar.2020.578943 Cervantes-Barragan, 2017, Lactobacillus reuteri induces gut intraepithelial CD4+CD8αα+ T cells. Science, 357, 806 Chávez-Talavera, 2017, Bile Acid Control of Metabolism and Inflammation in Obesity, Type 2 Diabetes, Dyslipidemia, and Nonalcoholic Fatty Liver Disease, Gastroenterology, 152, 1679, 10.1053/j.gastro.2017.01.055 Culpepper, 2019, Three probiotic strains exert different effects on plasma bile acid profiles in healthy obese adults: Randomised, double-blind placebo-controlled crossover study, Beneficial Microbes, 10, 497, 10.3920/BM2018.0151 Dong, 2020, Intestinal microbiota-derived tryptophan metabolites are predictive of Ah receptor activity, Gut Microbes, 12, 1, 10.1080/19490976.2020.1788899 Druart, 2013, Implication of fermentable carbohydrates targeting the gut microbiota on conjugated linoleic acid production in high-fat-fed mice, The British Journal of Nutrition, 110, 998, 10.1017/S0007114513000123 Ehrlich, 2020, Indole-3-lactic acid associated with Bifidobacterium-dominated microbiota significantly decreases inflammation in intestinal epithelial cells, BMC Microbiology, 20, 357, 10.1186/s12866-020-02023-y Fan, 2021, B. adolescentis ameliorates chronic colitis by regulating Treg/Th2 response and gut microbiota remodeling, Gut Microbes, 13, 1, 10.1080/19490976.2020.1826746 Futschik, 2005, Noise-robust soft clustering of gene expression time-course data, Journal of Bioinformatics and Computational Biology, 3, 965, 10.1142/S0219720005001375 Gao, 2020, Tryptophan Metabolism: A Link Between the Gut Microbiota and Brain, Advances in Nutrition (Bethesda, Md.), 11, 709, 10.1093/advances/nmz127 Glavas, 2021, Developmental Timing of High-Fat Diet Exposure Impacts Glucose Homeostasis in Mice in a Sex-Specific Manner, Diabetes, 70, 2771, 10.2337/db21-0310 Gurung, 2020, Role of gut microbiota in type 2 diabetes pathophysiology, EBioMedicine, 51, 10.1016/j.ebiom.2019.11.051 Herrema, 2020, Intestinal microbial metabolites in human metabolism and type 2 diabetes, Diabetologia, 63, 2533, 10.1007/s00125-020-05268-4 Huang, 2022, Gut microbiota mediate melatonin signalling in association with type 2 diabetes, Diabetologia, 10.1007/s00125-022-05747-w Huang, 2022, Stachyose Alleviates Corticosterone-Induced Long-Term Potentiation Impairment via the Gut-Brain Axis, Frontiers in Pharmacology, 13 Hyland, 2022, Emerging effects of tryptophan pathway metabolites and intestinal microbiota on metabolism and intestinal function, Amino Acids, 54, 57, 10.1007/s00726-022-03123-x Karusheva, 2019, Short-term dietary reduction of branched-chain amino acids reduces meal-induced insulin secretion and modifies microbiome composition in type 2 diabetes: A randomized controlled crossover trial, The American Journal of Clinical Nutrition, 110, 1098, 10.1093/ajcn/nqz191 Komaroff, 2017, The Microbiome and Risk for Obesity and Diabetes, JAMA, 317, 355, 10.1001/jama.2016.20099 Kumar, L., & E Futschik, M. (2007). Mfuzz: A software package for soft clustering of microarray data. Bioinformation, 2(1), 5–7. https://doi.org/10.6026/97320630002005. Laurans, 2018, Genetic deficiency of indoleamine 2,3-dioxygenase promotes gut microbiota-mediated metabolic health, Nature Medicine, 24, 1113, 10.1038/s41591-018-0060-4 Lee, 2010, Indole as an intercellular signal in microbial communities, FEMS Microbiology Reviews, 34, 426, 10.1111/j.1574-6976.2009.00204.x Li, 2021, Berberine combined with stachyose improves glycometabolism and gut microbiota through regulating colonic microRNA and gene expression in diabetic rats, Life Sciences, 284, 10.1016/j.lfs.2021.119928 Li, 2021, Mixed conjugated linoleic acid sex-dependently reverses high-fat diet-induced insulin resistance via the gut-adipose axis, FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 35, e21466, 10.1096/fj.202002161RR Li, 2022, Associations between plasma tryptophan and indole-3-propionic acid levels and mortality in patients with coronary artery disease, The American Journal of Clinical Nutrition, 116, 1070, 10.1093/ajcn/nqac170 Li, 2017, Evaluation of clinical safety and beneficial effects of stachyose-enriched α-galacto-oligosaccharides on gut microbiota and bowel function in humans, Food & Function, 8, 262, 10.1039/C6FO01290F Liang, 2020, Urinary metabolomics analysis reveals the anti-diabetic effect of stachyose in high-fat diet/streptozotocin-induced type 2 diabetic rats, Carbohydrate Polymers, 229, 10.1016/j.carbpol.2019.115534 Liu, 2018, Stachyose Improves Inflammation through Modulating Gut Microbiota of High-Fat Diet/Streptozotocin-Induced Type 2 Diabetes in Rats, Molecular Nutrition & Food Research, 62, e1700954, 10.1002/mnfr.201700954 Liu, 2022, Lactiplantibacillus plantarum P9 improved gut microbial metabolites and alleviated inflammatory response in pesticide exposure cohorts, IScience, 25, 10.1016/j.isci.2022.104472 Lynch, 2016, The Human Intestinal Microbiome in Health and Disease, The New England Journal of Medicine, 375, 2369, 10.1056/NEJMra1600266 Ma, 2021, Effects of Combinations of Goat Milk and Oligosaccharides on Altering the Microbiota, Immune Responses, and Short Chain Fatty Acid Levels in the Small Intestines of Mice, Journal of Agricultural and Food Chemistry, 69, 8828, 10.1021/acs.jafc.1c03408 Moreira, 2019, CLA-supplemented diet accelerates experimental colorectal cancer by inducing TGF-β-producing macrophages and T cells, Mucosal Immunology, 12, 188, 10.1038/s41385-018-0090-8 Oh, 2021, Lactobacillus plantarum HAC01 Supplementation Improves Glycemic Control in Prediabetic Subjects: A Randomized, Double-Blind, Placebo-Controlled Trial. Nutrients, 13, 2337 Olofsson, 2022, The Metabolic Role and Therapeutic Potential of the Microbiome, Endocrine Reviews, bnac004 Pacifici, 2017, Intra Amniotic Administration of Raffinose and Stachyose Affects the Intestinal Brush Border Functionality and Alters Gut Microflora Populations, Nutrients, 9, E304, 10.3390/nu9030304 Platten, 2019, Tryptophan metabolism as a common therapeutic target in cancer, neurodegeneration and beyond, Nature Reviews. Drug Discovery, 18, 379, 10.1038/s41573-019-0016-5 Puccetti, 2021, Enteric formulated indole-3-carboxaldehyde targets the aryl hydrocarbon receptor for protection in a murine model of metabolic syndrome, International Journal of Pharmaceutics, 602, 10.1016/j.ijpharm.2021.120610 Qi, 2022, Host and gut microbial tryptophan metabolism and type 2 diabetes: An integrative analysis of host genetics, diet, gut microbiome and circulating metabolites in cohort studies, Gut, 71, 1095, 10.1136/gutjnl-2021-324053 Renga, 2022, Optimizing therapeutic outcomes of immune checkpoint blockade by a microbial tryptophan metabolite, Journal for Immunotherapy of Cancer, 10, e003725, 10.1136/jitc-2021-003725 Roager, 2018, Microbial tryptophan catabolites in health and disease, Nature Communications, 9, 3294, 10.1038/s41467-018-05470-4 Rodrigues, 2021, Transkingdom interactions between Lactobacilli and hepatic mitochondria attenuate western diet-induced diabetes, Nature Communications, 12, 101, 10.1038/s41467-020-20313-x Rothhammer, 2016, Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor, Nature Medicine, 22, 586, 10.1038/nm.4106 Ruiz, 2017, Bifidobacteria and Their Molecular Communication with the Immune System, Frontiers in Microbiology, 8, 2345, 10.3389/fmicb.2017.02345 Ruocco, 2020, Manipulation of Dietary Amino Acids Prevents and Reverses Obesity in Mice Through Multiple Mechanisms That Modulate Energy Homeostasis, Diabetes, 69, 2324, 10.2337/db20-0489 Ruuskanen, 2022, Gut Microbiome Composition Is Predictive of Incident Type 2 Diabetes in a Population Cohort of 5,572 Finnish Adults, Diabetes Care, 45, 811, 10.2337/dc21-2358 Scheithauer, 2020, Gut Microbiota as a Trigger for Metabolic Inflammation in Obesity and Type 2 Diabetes, Frontiers in Immunology, 11, 10.3389/fimmu.2020.571731 Shen, 2016, Nutrient Regulation: Conjugated Linoleic Acid’s Inflammatory and Browning Properties in Adipose Tissue, Annual Review of Nutrition, 36, 183, 10.1146/annurev-nutr-071715-050924 Song, 2020, Microbial bile acid metabolites modulate gut RORγ+ regulatory T cell homeostasis, Nature, 577, 410, 10.1038/s41586-019-1865-0 Sroka-Oleksiak, 2020, Metagenomic Analysis of Duodenal Microbiota Reveals a Potential Biomarker of Dysbiosis in the Course of Obesity and Type 2 Diabetes: A Pilot Study, Journal of Clinical Medicine, 9, E369, 10.3390/jcm9020369 Thompson, 2021, Ruminiclostridium 5, Parabacteroides distasonis, and bile acid profile are modulated by prebiotic diet and associate with facilitated sleep/clock realignment after chronic disruption of rhythms, Brain, Behavior, and Immunity, 97, 150, 10.1016/j.bbi.2021.07.006 Tuomainen, 2018, Associations of serum indolepropionic acid, a gut microbiota metabolite, with type 2 diabetes and low-grade inflammation in high-risk individuals, Nutrition & Diabetes, 8, 35, 10.1038/s41387-018-0046-9 Vangipurapu, 2020, Microbiota-Related Metabolites and the Risk of Type 2 Diabetes, Diabetes Care, 43, 1319, 10.2337/dc19-2533 Wang, S., Li, M., Lin, H., Wang, G., Xu, Y., Zhao, X., Hu, C., Zhang, Y., Zheng, R., Hu, R., Shi, L., Du, R., Su, Q., Wang, J., Chen, Y., Yu, X., Yan, L., Wang, T., Zhao, Z., … 4C Study Group. (2022). Amino acids, microbiota-related metabolites, and the risk of incident diabetes among normoglycemic Chinese adults: Findings from the 4C study. Cell Reports. Medicine, 100727. https://doi.org/10.1016/j.xcrm.2022.100727. Wang, 2022, In Vitro Fermentability of Soybean Oligosaccharides from Wastewater of Tofu Production, Polymers, 14, 1704, 10.3390/polym14091704 Wastyk, 2021, Gut-microbiota-targeted diets modulate human immune status, Cell, 184, 4137, 10.1016/j.cell.2021.06.019 White, 2019, Impact of diet–microbiota interactions on human metabolism, Nature Research Wu, 2022, Limosilactobacillus reuteri SLZX19-12 Protects the Colon from Infection by Enhancing Stability of the Gut Microbiota and Barrier Integrity and Reducing Inflammation, Microbiology Spectrum, 10, e0212421, 10.1128/spectrum.02124-21 Xue, 2022, Gut Microbially Produced Indole-3-Propionic Acid Inhibits Atherosclerosis by Promoting Reverse Cholesterol Transport and Its Deficiency Is Causally Related to Atherosclerotic Cardiovascular Disease, Circulation Research, 131, 404, 10.1161/CIRCRESAHA.122.321253 Yan, 2023, Diet-rich in wheat bran modulates tryptophan metabolism and AhR/IL-22 signalling mediated metabolic health and gut dysbacteriosis: A novel prebiotic-like activity of wheat bran, Food Research International (Ottawa, Ont.), 163 Yang, 2017, Bacterial conjugated linoleic acid production and their applications, Progress in Lipid Research, 68, 26, 10.1016/j.plipres.2017.09.002 Yang, 2018, Serum metabolite profile associated with incident type 2 diabetes in Koreans: Findings from the Korean Genome and Epidemiology Study, Scientific Reports, 8, 8207, 10.1038/s41598-018-26320-9 Yang, 2010, Isolation, characterization, and immunological effects of alpha-galacto-oligosaccharides from a new source, the herb Lycopus lucidus Turcz, Journal of Agricultural and Food Chemistry, 58, 8253, 10.1021/jf101217f Zhai, 2021, Gut-Microbial Metabolites, Probiotics and Their Roles in Type 2 Diabetes, International Journal of Molecular Sciences, 22, 12846, 10.3390/ijms222312846 Zhang, 2023, Gut Bacterial Indole-3-acetic Acid Induced Immune Promotion Mediates Preventive Effects of Fu Brick Tea Polyphenols on Experimental Colitis, Journal of Agricultural and Food Chemistry, 71, 1201, 10.1021/acs.jafc.2c06517 Zhao, 2017, Functional properties, structural studies and chemo-enzymatic synthesis of oligosaccharides, Trends in Food Science & Technology, 66, 135, 10.1016/j.tifs.2017.06.008 Zheng, 2021, Hyocholic acid species improve glucose homeostasis through a distinct TGR5 and FXR signaling mechanism, Cell Metabolism, 33, 791, 10.1016/j.cmet.2020.11.017 Zheng, 2021, Hyocholic acid species as novel biomarkers for metabolic disorders, Nature Communications, 12, 1487, 10.1038/s41467-021-21744-w