{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,4]],"date-time":"2025-11-04T23:51:02Z","timestamp":1762300262126,"version":"3.41.2"},"reference-count":72,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,1,9]],"date-time":"2023-01-09T00:00:00Z","timestamp":1673222400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Prenatal and early postnatal development are known to influence future health. We previously reported that prenatal high estradiol (HE) exposure induces insulin resistance in male mice by disrupting hypothalamus development. Because a foster dam can modify a pup\u2019s gut microbiota and affect its health later in life, we explored whether surrogate fostering could also influence glucose metabolism in HE offspring and examined mechanisms that might be involved.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We performed a surrogate fostering experiment in mice and examined the relationship between the metabolic markers associated to insulin resistance and the composition of the gut microbiota.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>HE pups raised by HE foster dams (HE-HE) developed insulin resistance, but HE pups fostered by negative control dams (NC-HE) did not. The gut microbiota composition of HE-HE mice differed from that of NC mice raised by NC foster dams (NC-NC), whereas the composition in NC-HE mice was similar to that of NC-NC mice. Compared with NC-NC mice, HE-HE mice had decreased levels of fecal short-chain fatty acids and serum intestinal hormones, increased food intake, and increased hypothalamic neuropeptide Y expression. In contrast, none of these indices differed between NC-HE and NC-NC mice. Spearman correlation analysis revealed a significant correlation between the altered gut microbiota composition and the insulin resistance-related metabolic indicators, indicating involvement of the microbiota-gut-brain axis.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>Our findings suggest that alterations in the early growth environment may prevent fetal-programmed glucose metabolic disorder <jats:italic>via<\/jats:italic> modulation of the microbiota-gut-brain axis. These findings offer direction for development of translational solutions for adult diseases associated with aberrant microbial communities in early life.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fmicb.2022.1050352","type":"journal-article","created":{"date-parts":[[2023,1,9]],"date-time":"2023-01-09T09:15:07Z","timestamp":1673255707000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":2,"title":["Surrogate fostering of mice prevents prenatal estradiol-induced insulin resistance via modulation of the microbiota-gut-brain axis"],"prefix":"10.3389","volume":"13","author":[{"given":"Huihui","family":"Wang","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chengliang","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shuping","family":"Gu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yun","family":"Sun","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2023,1,9]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"e260","DOI":"10.1002\/wdev.260","article-title":"Quantitating the cell: turning images into numbers with ImageJ","volume":"6","author":"Arena","year":"2017","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"G1288","DOI":"10.1152\/ajpgi.00341.2012","article-title":"Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice","volume":"303","author":"Asano","year":"2012","journal-title":"Am. J. Physiol. Gastrointest. Liver Physiol."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"e2101030","DOI":"10.1002\/mnfr.202101030","article-title":"Portulaca oleracea L. extract alleviated type 2 diabetes via modulating the gut microbiota and serum branched-chain amino acid metabolism","volume":"66","author":"Bao","year":"2022","journal-title":"Mol. Nutr. Food Res."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1038\/nature02725","article-title":"Developmental plasticity and human health","volume":"430","author":"Bateson","year":"2004","journal-title":"Nature"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.coemr.2020.06.005","article-title":"Metabolic and inflammatory functions of short-chain fatty acid receptors","volume":"16","author":"Bolognini","year":"2021","journal-title":"Curr. Opin. Endocr. Metab. Res."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"108939","DOI":"10.1016\/j.foodres.2019.108939","article-title":"Ethanol extract of propolis prevents high-fat diet-induced insulin resistance and obesity in association with modulation of gut microbiota in mice","volume":"130","author":"Cai","year":"2020","journal-title":"Food Res. Int."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1038\/nrendo.2015.128","article-title":"Short-chain fatty acids in control of body weight and insulin sensitivity","volume":"11","author":"Canfora","year":"2015","journal-title":"Nat. Rev. Endocrinol."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1038\/s42255-018-0017-4","article-title":"Microbial regulation of organismal energy homeostasis","volume":"1","author":"Cani","year":"2019","journal-title":"Nat. Metab."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1038\/nmeth.f.303","article-title":"QIIME allows analysis of high-throughput community sequencing data","volume":"7","author":"Caporaso","year":"2010","journal-title":"Nat. Methods"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"588079","DOI":"10.3389\/fimmu.2020.588079","article-title":"A holistic view of berberine inhibiting intestinal carcinogenesis in conventional mice based on microbiome-metabolomics analysis","volume":"11","author":"Chen","year":"2020","journal-title":"Front. Immunol."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1186\/s40168-022-01305-z","article-title":"The developing airway and gut microbiota in early life is influenced by age of older siblings","volume":"10","author":"Christensen","year":"2022","journal-title":"Microbiome"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"D633","DOI":"10.1093\/nar\/gkt1244","article-title":"Ribosomal database project: data and tools for high throughput rRNA analysis","volume":"42","author":"Cole","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"970","DOI":"10.1016\/j.coph.2013.09.010","article-title":"The hypothalamus and metabolism: integrating signals to control energy and glucose homeostasis","volume":"13","author":"Coll","year":"2013","journal-title":"Curr. Opin. Pharmacol."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"1877","DOI":"10.1152\/physrev.00018.2018","article-title":"The microbiota-gut-brain axis","volume":"99","author":"Cryan","year":"2019","journal-title":"Physiol. Rev."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1186\/s40168-015-0080-y","article-title":"Cross-fostering immediately after birth induces a permanent microbiota shift that is shaped by the nursing mother","volume":"3","author":"Daft","year":"2015","journal-title":"Microbiome"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"2325","DOI":"10.1194\/jlr.R036012","article-title":"The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism","volume":"54","author":"den Besten","year":"2013","journal-title":"J. Lipid Res."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"997","DOI":"10.1016\/j.tim.2019.08.001","article-title":"The gut microbiota in the first decade of life","volume":"27","author":"Derrien","year":"2019","journal-title":"Trends Microbiol."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"685","DOI":"10.1038\/s41587-020-0548-6","article-title":"PICRUSt2 for prediction of metagenome functions","volume":"38","author":"Douglas","year":"2020","journal-title":"Nat. Biotechnol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1007\/s11882-010-0136-9","article-title":"Fetal programming: early-life modulations that affect adult outcomes","volume":"10","author":"Drever","year":"2010","journal-title":"Curr. Allergy Asthma Rep."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1016\/j.rbmo.2018.01.006","article-title":"A demographic projection of the contribution of assisted reproductive technologies to world population growth","volume":"36","author":"Faddy","year":"2018","journal-title":"Reprod. Biomed. Online"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"531","DOI":"10.1186\/s13059-014-0531-y","article-title":"Temporal variability is a personalized feature of the human microbiome","volume":"15","author":"Flores","year":"2014","journal-title":"Genome Biol."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"2019","DOI":"10.1007\/s10482-020-01474-7","article-title":"Human gut microbiota\/microbiome in health and diseases: a review","volume":"113","author":"Gomaa","year":"2020","journal-title":"Antonie Van Leeuwenhoek"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1007\/s11154-019-09511-1","article-title":"The gut microbiota to the brain axis in the metabolic control","volume":"20","author":"Grasset","year":"2019","journal-title":"Rev. Endocr. Metab. Disord."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"173","DOI":"10.3389\/fmicb.2020.00173","article-title":"A novel antidiabetic monomers combination alleviates insulin resistance through bacteria-cometabolism-inflammation responses","volume":"11","author":"Han","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"9947","DOI":"10.1039\/d2fo01109c","article-title":"The antidiabetic effects of Bifidobacterium longum subsp. longum BL21 through regulating gut microbiota structure in type 2 diabetic mice","volume":"13","author":"Hao","year":"2022","journal-title":"Food Funct."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1016\/j.tim.2017.11.002","article-title":"Human gut microbiome: function matters","volume":"26","author":"Heintz-Buschart","year":"2018","journal-title":"Trends Microbiol."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"2189","DOI":"10.1021\/acs.jnatprod.9b00205","article-title":"Effect of 1-deoxynojirimycin isolated from mulberry leaves on glucose metabolism and gut microbiota in a streptozotocin-induced diabetic mouse model","volume":"82","author":"Hu","year":"2019","journal-title":"J. Nat. Prod."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"299","DOI":"10.3390\/ph14040299","article-title":"Fermented maillard reaction products by Lactobacillus gasseri 4M13 alters the intestinal microbiota and improves dysfunction in type 2 diabetic mice with colitis","volume":"14","author":"Jeong","year":"2021","journal-title":"Pharmaceuticals"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"7046","DOI":"10.1038\/s41598-017-07335-0","article-title":"Anti-diabetic effects of Clostridium butyricum CGMCC0313.1 through promoting the growth of gut butyrate-producing bacteria in type 2 diabetic mice","volume":"7","author":"Jia","year":"2017","journal-title":"Sci. Rep."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1017\/S095442241700018X","article-title":"Probiotics, prebiotics, synbiotics and insulin sensitivity","volume":"31","author":"Kim","year":"2018","journal-title":"Nutr. Res. Rev."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/j.npep.2018.11.004","article-title":"PYY(3-36) and exendin-4 reduce food intake and activate neuronal circuits in a synergistic manner in mice","volume":"73","author":"Kjaergaard","year":"2019","journal-title":"Neuropeptides"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"1332","DOI":"10.1016\/j.cell.2016.05.041","article-title":"From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites","volume":"165","author":"Koh","year":"2016","journal-title":"Cells"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"120770","DOI":"10.1016\/j.lfs.2022.120770","article-title":"Long-term consumption of the sugar substitute sorbitol alters gut microbiome and induces glucose intolerance in mice","volume":"305","author":"Li","year":"2022","journal-title":"Life Sci."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"421","DOI":"10.3920\/BM2016.0167","article-title":"Effects of Lactobacillus casei CCFM419 on insulin resistance and gut microbiota in type 2 diabetic mice","volume":"8","author":"Li","year":"2017","journal-title":"Benef. Microbes"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"110270","DOI":"10.1016\/j.foodres.2021.110270","article-title":"Curcumin alleviates high-fat diet-induced hepatic steatosis and obesity in association with modulation of gut microbiota in mice","volume":"143","author":"Li","year":"2021","journal-title":"Food Res. Int."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"4304","DOI":"10.1002\/jsfa.11782","article-title":"Anti-diabetic and gut microbiota modulation effects of sacha inchi (Plukenetia volubilis L.) leaf extract in streptozotocin-induced type 1 diabetic mice","volume":"102","author":"Lin","year":"2022","journal-title":"J. Sci. Food Agric."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"5935","DOI":"10.1002\/jsfa.11945","article-title":"Peanut skin procyanidins ameliorate insulin resistance via modulation of gut microbiota and gut barrier in type 2 diabetic mice","volume":"102","author":"Liu","year":"2022","journal-title":"J. Sci. Food Agric."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"406","DOI":"10.1016\/j.biortech.2014.10.123","article-title":"Dynamics of bacterial microbiota during lignocellulosic waste composting: studies upon its structure, functionality and biodiversity","volume":"175","author":"Lopez-Gonzalez","year":"2015","journal-title":"Bioresour. Technol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"916271","DOI":"10.3389\/fnut.2022.916271","article-title":"Hypoglycemic effects of Lycium barbarum polysaccharide in type 2 diabetes mellitus mice via modulating gut microbiota","volume":"9","author":"Ma","year":"2022","journal-title":"Front. Nutr."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1016\/j.jcmgh.2018.04.003","article-title":"The brain-gut-microbiome Axis","volume":"6","author":"Martin","year":"2018","journal-title":"Cell. Mol. Gastroenterol. Hepatol."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1017\/S0029665120006916","article-title":"SCFA: mechanisms and functional importance in the gut","volume":"80","author":"Martin-Gallausiaux","year":"2021","journal-title":"Proc. Nutr. Soc."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"926","DOI":"10.1172\/JCI76304","article-title":"Gut\/brain axis and the microbiota","volume":"125","author":"Mayer","year":"2015","journal-title":"J. Clin. Invest."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"E326","DOI":"10.1152\/ajpendo.00388.2020","article-title":"Gut-to-brain signals in feeding control","volume":"320","author":"Moura-Assis","year":"2021","journal-title":"Am. J. Physiol. Endocrinol. Metab."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"647","DOI":"10.1001\/jamapediatrics.2017.0378","article-title":"Association between breast milk bacterial communities and establishment and development of the infant gut microbiome","volume":"171","author":"Pannaraj","year":"2017","journal-title":"JAMA Pediatr."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.neuropharm.2012.02.004","article-title":"Hypothalamic neuropeptides and the regulation of appetite","volume":"63","author":"Parker","year":"2012","journal-title":"Neuropharmacology"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"906","DOI":"10.3389\/fimmu.2020.00906","article-title":"The genus alistipes: gut bacteria with emerging implications to inflammation, cancer, and mental health","volume":"11","author":"Parker","year":"2020","journal-title":"Front. Immunol."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.coph.2019.03.011","article-title":"The role of gut microbiota in obesity, diabetes mellitus, and effect of metformin: new insights into old diseases","volume":"49","author":"Pascale","year":"2019","journal-title":"Curr. Opin. Pharmacol."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1016\/j.cvfa.2019.02.006","article-title":"Developmental programming of fetal growth and development","volume":"35","author":"Reynolds","year":"2019","journal-title":"Vet. Clin. North Am. Food Anim. Pract."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1146\/annurev-physiol-020911-153245","article-title":"Fetal programming and metabolic syndrome","volume":"74","author":"Rinaudo","year":"2012","journal-title":"Annu. Rev. Physiol."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"e13991","DOI":"10.1111\/jfbc.13991","article-title":"Effects of L-arabinose by hypoglycemic and modulating gut microbiome in a high-fat diet-and streptozotocin-induced mouse model of type 2 diabetes mellitus","volume":"45","author":"Shen","year":"2021","journal-title":"J. Food Biochem."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"e00458","DOI":"10.7554\/eLife.00458","article-title":"Cohabiting family members share microbiota with one another and with their dogs","volume":"2","author":"Song","year":"2013","journal-title":"eLife"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"713","DOI":"10.1038\/nm.4142","article-title":"The microbiome in early life: implications for health outcomes","volume":"22","author":"Tamburini","year":"2016","journal-title":"Nat. Med."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"e00933-19","DOI":"10.1128\/mSphere.00933-19","article-title":"No consistent evidence for microbiota in murine placental and fetal tissues","volume":"5","author":"Theis","year":"2020","journal-title":"mSphere"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"e3001556","DOI":"10.1371\/journal.pbio.3001556","article-title":"Systematically assessing microbiome-disease associations identifies drivers of inconsistency in metagenomic research","volume":"20","author":"Tierney","year":"2022","journal-title":"PLoS Biol."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1007\/s00248-019-01317-7","article-title":"Effect of the nursing mother on the gut microbiome of the offspring during early mouse development","volume":"78","author":"Treichel","year":"2019","journal-title":"Microb. Ecol."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1111\/ijpo.12217","article-title":"The prenatal gut microbiome: are we colonized with bacteria in utero?","volume":"12","author":"Walker","year":"2017","journal-title":"Pediatr. Obes."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"110965","DOI":"10.1016\/j.fct.2019.110965","article-title":"Perilla oil regulates intestinal microbiota and alleviates insulin resistance through the PI3K\/AKT signaling pathway in type-2 diabetic KKAy mice","volume":"135","author":"Wang","year":"2020","journal-title":"Food Chem. Toxicol."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"3814","DOI":"10.1039\/c7fo90032e","article-title":"Correction: Lactobacillus casei CCFM419 attenuates type 2 diabetes via a gut microbiota dependent mechanism","volume":"8","author":"Wang","year":"2017","journal-title":"Food Funct."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"141086","DOI":"10.1016\/j.scitotenv.2020.141086","article-title":"Functional characteristic of microbial communities in large-scale biotreatment systems of food waste","volume":"746","author":"Wang","year":"2020","journal-title":"Sci. Total Environ."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1016\/j.tim.2019.07.010","article-title":"Maternal vertical transmission affecting early-life microbiota development","volume":"28","author":"Wang","year":"2020","journal-title":"Trends Microbiol."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"2876","DOI":"10.1021\/acs.jafc.1c07441","article-title":"Glycolipid metabolism and metagenomic analysis of the therapeutic effect of a phenolics-rich extract from noni fruit on type 2 diabetic mice","volume":"70","author":"Wang","year":"2022","journal-title":"J. Agric. Food Chem."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"677935","DOI":"10.3389\/fgene.2021.677935","article-title":"Neurogenesis potential evaluation and transcriptome analysis of fetal hypothalamic neural stem\/progenitor cells with prenatal high estradiol exposure","volume":"12","author":"Wang","year":"2021","journal-title":"Front. Genet."},{"key":"ref63","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1210\/en.2017-03017","article-title":"Prenatal high estradiol exposure induces sex-specific and dietarily reversible insulin resistance through decreased hypothalamic INSR","volume":"159","author":"Wang","year":"2018","journal-title":"Endocrinology"},{"key":"ref64","doi-asserted-by":"publisher","first-page":"204","DOI":"10.1016\/j.ijbiomac.2022.01.152","article-title":"Preventive effects of polysaccharides from Physalis alkekengi L. on dietary advanced glycation end product-induced insulin resistance in mice associated with the modulation of gut microbiota","volume":"204","author":"Wu","year":"2022","journal-title":"Int. J. Biol. Macromol."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"8797","DOI":"10.1021\/acs.jafc.1c02925","article-title":"Lactobacillus rhamnosus LRa05 ameliorate hyperglycemia through a regulating glucagon-mediated signaling pathway and gut microbiota in type 2 diabetic mice","volume":"69","author":"Wu","year":"2021","journal-title":"J. Agric. Food Chem."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"1519","DOI":"10.1039\/d1fo03646g","article-title":"Sesquiterpene glycoside isolated from loquat leaf targets gut microbiota to prevent type 2 diabetes mellitus in db\/db mice","volume":"13","author":"Wu","year":"2022","journal-title":"Food Funct."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"5479","DOI":"10.1111\/1750-3841.15963","article-title":"Auricularia auricula-judae (Bull.) polysaccharides improve type 2 diabetes in HFD\/STZ-induced mice by regulating the AKT\/AMPK signaling pathways and the gut microbiota","volume":"86","author":"Xu","year":"2021","journal-title":"J. Food Sci."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"154423","DOI":"10.1016\/j.phymed.2022.154423","article-title":"Laurolitsine ameliorates type 2 diabetes by regulating the hepatic LKB1-AMPK pathway and gut microbiota","volume":"106","author":"Yong","year":"2022","journal-title":"Phytomedicine"},{"key":"ref69","doi-asserted-by":"publisher","first-page":"e127806","DOI":"10.1172\/jci.insight.127806","article-title":"Fetal exposure to the maternal microbiota in humans and mice","volume":"4","author":"Younge","year":"2019","journal-title":"JCI Insight"},{"key":"ref70","doi-asserted-by":"publisher","first-page":"8288","DOI":"10.1039\/d1fo00882j","article-title":"Lactobacillus casei LC89 exerts antidiabetic effects through regulating hepatic glucagon response and gut microbiota in type 2 diabetic mice","volume":"12","author":"Zhang","year":"2021","journal-title":"Food Funct."},{"key":"ref71","doi-asserted-by":"publisher","first-page":"e2100907","DOI":"10.1002\/mnfr.202100907","article-title":"Heat-treated adzuki bean protein hydrolysates reduce obesity in mice fed a high-fat diet via remodeling gut microbiota and improving metabolic function","volume":"66","author":"Zhao","year":"2022","journal-title":"Mol. Nutr. Food Res."},{"key":"ref72","doi-asserted-by":"publisher","first-page":"3240","DOI":"10.3390\/nu13093240","article-title":"Adzuki bean alleviates obesity and insulin resistance induced by a high-fat diet and modulates gut microbiota in mice","volume":"13","author":"Zhao","year":"2021","journal-title":"Nutrients"}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2022.1050352\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,9]],"date-time":"2023-01-09T09:15:10Z","timestamp":1673255710000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2022.1050352\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,9]]},"references-count":72,"alternative-id":["10.3389\/fmicb.2022.1050352"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2022.1050352","relation":{},"ISSN":["1664-302X"],"issn-type":[{"type":"electronic","value":"1664-302X"}],"subject":[],"published":{"date-parts":[[2023,1,9]]},"article-number":"1050352"}}