{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,3]],"date-time":"2026-11-03T21:09:41Z","timestamp":1793740181943,"version":"4.6.1"},"reference-count":69,"publisher":"MDPI AG","issue":"14","license":[{"start":{"date-parts":[[2022,7,6]],"date-time":"2022-07-06T00:00:00Z","timestamp":1657065600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Guangzhou Science and Technology Project","award":["201604020002"],"award-info":[{"award-number":["201604020002"]}]},{"name":"Guangzhou Science and Technology Project","award":["R01CA222490"],"award-info":[{"award-number":["R01CA222490"]}]},{"name":"National Institutes of Health","award":["201604020002"],"award-info":[{"award-number":["201604020002"]}]},{"name":"National Institutes of Health","award":["R01CA222490"],"award-info":[{"award-number":["R01CA222490"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>Obesity and malnutrition both cause dysbiosis and dampen retinoic acid (RA) signaling pathways, which play pivotal roles in biological processes. The current study evaluates a hypothesis that colitis-associated dysbiosis also has systemic negative impacts on RA signaling. Thus, we studied the effects of inflammation, under a vitamin A-sufficient condition, on RA signaling using mouse colitis models induced by dextran sulfate sodium. That data showed that intestinal inflammation resulted in reduced RA signaling in the liver, brain, gut, and adipose tissues measured by analyzing the expression of genes encoding for the synthesis, oxidation, transport, and receptor of RA. The expression of RA-regulated gut homing molecules including \u03b14\u03b27 integrin, and CCR9, along with MADCAM1 were all reduced in colitis mice revealing compromised immunity due to reduced RA signaling. The data also showed that the development of colitis was accompanied by dysbiosis featured with reduced Lactobacillaceae and Verrucomicrobiaceae but an expansion of Erysipelotrichaceae and others. Colitis resulted in reduced butyrate-producing bacteria and increased methane-generating bacteria. Additionally, dysbiosis was associated with induced Il-1\u03b2, Ifn-\u03b3, and Tnf-\u03b1 mRNA but reduced Il-22, Il-17f, and Ror\u03b3t transcripts in the colon. Together, intestinal inflammation inhibits RA signaling in multiple organs. RA is essential in regulating various biological processes, it is critical to detect RA signaling reduction in tissues even when vitamin A deficiency is absent. Moreover, probiotics can potentially prevent dysbiosis and reverse compromised RA signaling, having systemic health benefits.<\/jats:p>","DOI":"10.3390\/nu14142788","type":"journal-article","created":{"date-parts":[[2022,7,6]],"date-time":"2022-07-06T09:41:10Z","timestamp":1657100470000},"page":"2788","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Retinoic Acid Signaling Is Compromised in DSS-Induced Dysbiosis"],"prefix":"10.3390","volume":"14","author":[{"given":"Yongchun","family":"Li","sequence":"first","affiliation":[{"name":"Department of Gastroenterology, Zhujiang Hospital, Southern Medical University, Guangzhou 510282, China"},{"name":"Department of Infectious Diseases, The Six Affiliated Hospital, South China University of Technology, Foshan 528200, China"},{"name":"Department of Pathology and Laboratory Medicine, University of California Davis, Sacramento, CA 95817, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lili","family":"Sheng","sequence":"additional","affiliation":[{"name":"Department of Pathology and Laboratory Medicine, University of California Davis, Sacramento, CA 95817, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Prasant Kumar","family":"Jena","sequence":"additional","affiliation":[{"name":"Department of Pathology and Laboratory Medicine, University of California Davis, Sacramento, CA 95817, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miranda Claire","family":"Gilbert","sequence":"additional","affiliation":[{"name":"Department of Pathology and Laboratory Medicine, University of California Davis, Sacramento, CA 95817, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2243-7759","authenticated-orcid":false,"given":"Yu-Jui Yvonne","family":"Wan","sequence":"additional","affiliation":[{"name":"Department of Pathology and Laboratory Medicine, University of California Davis, Sacramento, CA 95817, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hua","family":"Mao","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, Zhujiang Hospital, Southern Medical University, Guangzhou 510282, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,7,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"942","DOI":"10.3109\/00365521.2015.1014407","article-title":"The epidemiology of inflammatory bowel disease","volume":"50","author":"Burisch","year":"2015","journal-title":"Scand. J. Gastroenterol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1785","DOI":"10.1053\/j.gastro.2011.01.055","article-title":"Epidemiology and natural history of inflammatory bowel diseases","volume":"140","author":"Cosnes","year":"2011","journal-title":"Gastroenterology"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1053\/j.gastro.2011.10.001","article-title":"Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review","volume":"142","author":"Molodecky","year":"2012","journal-title":"Gastroenterology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1038\/nrgastro.2012.156","article-title":"The role of the gut microbiota in nutrition and health","volume":"9","author":"Flint","year":"2012","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1038\/nature10213","article-title":"Human nutrition, the gut microbiome and the immune system","volume":"474","author":"Kau","year":"2011","journal-title":"Nature"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Yuille, S., Reichardt, N., Panda, S., Dunbar, H., and Mulder, I.E. (2018). Human gut bacteria as potent class I histone deacetylase inhibitors in vitro through production of butyric acid and valeric acid. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0201073"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1080\/1040841X.2017.1373063","article-title":"Epigenetic regulation in bacterial infections: Targeting histone deacetylases","volume":"44","author":"Grabiec","year":"2018","journal-title":"Crit. Rev. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"4436","DOI":"10.1128\/MCB.20.12.4436-4444.2000","article-title":"Hepatocyte-specific mutation establishes retinoid X receptor alpha as a heterodimeric integrator of multiple physiological processes in the liver","volume":"20","author":"Wan","year":"2000","journal-title":"Mol. Cell Biol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"He, Y., Gong, L., Fang, Y., Zhan, Q., Liu, H.X., Lu, Y., Guo, G.L., Lehman-McKeeman, L., Fang, J., and Wan, Y.J. (2013). The role of retinoic acid in hepatic lipid homeostasis defined by genomic binding and transcriptome profiling. BMC Genom., 14.","DOI":"10.1186\/1471-2164-14-575"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"17036","DOI":"10.1038\/celldisc.2017.36","article-title":"Retinoic acid induces white adipose tissue browning by increasing adipose vascularity and inducing beige adipogenesis of PDGFRalpha(+) adipose progenitors","volume":"3","author":"Wang","year":"2017","journal-title":"Cell Discov."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1016\/j.bcp.2014.08.018","article-title":"All-trans retinoic acid regulates hepatic bile acid homeostasis","volume":"91","author":"Yang","year":"2014","journal-title":"Biochem. Pharm."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"15893","DOI":"10.1038\/srep15893","article-title":"Obesity Leads to Tissue, but not Serum Vitamin A Deficiency","volume":"5","author":"Trasino","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2866","DOI":"10.1096\/fj.201700984RR","article-title":"Dysregulated bile acid synthesis and dysbiosis are implicated in Western diet-induced systemic inflammation, microglial activation, and reduced neuroplasticity","volume":"32","author":"Jena","year":"2018","journal-title":"FASEB J."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1241","DOI":"10.2174\/0929867311320100005","article-title":"Ion Channels as Drug Targets in Central Nervous System Disorders","volume":"20","author":"Waszkielewicz","year":"2013","journal-title":"Curr. Med. Chem."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1880","DOI":"10.4103\/1673-5374.259604","article-title":"Potential therapeutic roles of retinoids for prevention of neuroinflammation and neurodegeneration in Alzheimer\u2019s disease","volume":"14","author":"Das","year":"2019","journal-title":"Neural. Regen Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/j.jneuroim.2005.10.004","article-title":"9-Cis-retinoic acid suppresses inflammatory responses of microglia and astrocytes","volume":"171","author":"Xu","year":"2006","journal-title":"J. Neuroimmunol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.it.2016.12.006","article-title":"Retinoic Acid and Immune Homeostasis: A Balancing Act","volume":"38","author":"Erkelens","year":"2017","journal-title":"Trends Immunol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1038\/mi.2014.64","article-title":"Retinoic acid primes human dendritic cells to induce gut-homing, IL-10-producing regulatory T cells","volume":"8","author":"Bakdash","year":"2015","journal-title":"Mucosal. Immunol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/j.immuni.2015.06.009","article-title":"Retinoic Acid Differentially Regulates the Migration of Innate Lymphoid Cell Subsets to the Gut","volume":"43","author":"Kim","year":"2015","journal-title":"Immunity"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/j.immuni.2011.03.003","article-title":"Essential role for retinoic acid in the promotion of CD4(+) T cell effector responses via retinoic acid receptor alpha","volume":"34","author":"Hall","year":"2011","journal-title":"Immunity"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/j.immuni.2009.03.008","article-title":"Retinoic Acid Can Directly Promote TGF-beta-Mediated Foxp3(+) Treg Cell Conversion of Naive T Cells","volume":"30","author":"Mucida","year":"2009","journal-title":"Immunity"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.imlet.2014.06.011","article-title":"All-trans retinoic acid attenuates experimental colitis through inhibition of NF-kappaB signaling","volume":"162","author":"Hong","year":"2014","journal-title":"Immunol. Lett."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"4874809","DOI":"10.1155\/2016\/4874809","article-title":"Vitamin A Inhibits Development of Dextran Sulfate Sodium-Induced Colitis and Colon Cancer in a Mouse Model","volume":"2016","author":"Okayasu","year":"2016","journal-title":"Biomed. Res. Int."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1278","DOI":"10.1053\/j.gastro.2014.01.057","article-title":"Increased production of retinoic acid by intestinal macrophages contributes to their inflammatory phenotype in patients with Crohn\u2019s disease","volume":"146","author":"Sanders","year":"2014","journal-title":"Gastroenterology"},{"key":"ref_25","first-page":"457","article-title":"Retinoic acid suppresses intestinal mucus production and exacerbates experimental enterocolitis","volume":"5","author":"Oehlers","year":"2012","journal-title":"Dis. Model. Mech."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.immuni.2011.07.002","article-title":"The role of retinoic acid in tolerance and immunity","volume":"35","author":"Hall","year":"2011","journal-title":"Immunity"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1002\/0471142735.im1525s104","article-title":"Dextran sulfate sodium (DSS)-induced colitis in mice","volume":"104","author":"Chassaing","year":"2014","journal-title":"Curr. Protoc. Immunol."},{"key":"ref_28","first-page":"G622","article-title":"Disruption of colonic electrolyte transport in experimental colitis","volume":"268","author":"Bell","year":"1995","journal-title":"Am. J. Physiol"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1084\/jem.182.5.1281","article-title":"Antibodies to interleukin 12 abrogate established experimental colitis in mice","volume":"182","author":"Neurath","year":"1995","journal-title":"J. Exp. Med."},{"key":"ref_30","unstructured":"National Research Council Committee for the Update of the Guide for the Care and Use of Laboratory Animals (2011). The National Academies Collection: Reports funded by National Institutes of Health. Guide for the Care and Use of Laboratory Animals, National Academies Press."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1285","DOI":"10.1016\/j.addr.2010.07.003","article-title":"Retinoid pathway and cancer therapeutics","volume":"62","author":"Bushue","year":"2010","journal-title":"Adv. Drug Deliv. Rev."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1298","DOI":"10.1002\/ibd.20453","article-title":"Lymphocyte homing and its role in the pathogenesis of IBD","volume":"14","author":"Eksteen","year":"2008","journal-title":"Inflamm. Bowel. Dis."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/S1388-1981(99)00117-1","article-title":"Interactions of retinoid binding proteins and enzymes in retinoid metabolism","volume":"1440","author":"Napoli","year":"1999","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"63","DOI":"10.3390\/nu3010063","article-title":"Vitamin A metabolism: An update","volume":"3","author":"Clugston","year":"2011","journal-title":"Nutrients"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1289","DOI":"10.1080\/003655201317097146","article-title":"Reduced plasma antioxidant concentrations and increased oxidative DNA damage in inflammatory bowel disease","volume":"36","author":"Bortolan","year":"2001","journal-title":"Scand. J. Gastroenterol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1016\/j.clnu.2008.01.007","article-title":"Altered status of antioxidant vitamins and fatty acids in patients with inactive inflammatory bowel disease","volume":"27","author":"Hengstermann","year":"2008","journal-title":"Clin. Nutr."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1038\/mi.2015.82","article-title":"beta7-Integrin exacerbates experimental DSS-induced colitis in mice by directing inflammatory monocytes into the colon","volume":"9","author":"Schippers","year":"2016","journal-title":"Mucosal. Immunol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1056\/NEJMoa1215734","article-title":"Vedolizumab as induction and maintenance therapy for ulcerative colitis","volume":"369","author":"Feagan","year":"2013","journal-title":"N. Engl. J. Med."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"864","DOI":"10.1124\/jpet.109.153973","article-title":"The binding specificity and selective antagonism of vedolizumab, an anti-alpha4beta7 integrin therapeutic antibody in development for inflammatory bowel diseases","volume":"330","author":"Soler","year":"2009","journal-title":"J. Pharm. Exp."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1038\/mi.2015.68","article-title":"Regulatory T-cell depletion in the gut caused by integrin beta7 deficiency exacerbates DSS colitis by evoking aberrant innate immunity","volume":"9","author":"Zhang","year":"2016","journal-title":"Mucosal. Immunol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1038\/nri3661","article-title":"Cytokines in inflammatory bowel disease","volume":"14","author":"Neurath","year":"2014","journal-title":"Nat. Rev. Immunol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"18177","DOI":"10.3748\/wjg.v20.i48.18177","article-title":"Role of interleukin-22 in inflammatory bowel disease","volume":"20","author":"Li","year":"2014","journal-title":"World J. Gastroenterol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1016\/j.immuni.2008.11.003","article-title":"Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease","volume":"29","author":"Zenewicz","year":"2008","journal-title":"Immunity"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1117","DOI":"10.1084\/jem.20121588","article-title":"Retinoic acid expression associates with enhanced IL-22 production by gammadelta T cells and innate lymphoid cells and attenuation of intestinal inflammation","volume":"210","author":"Mielke","year":"2013","journal-title":"J. Exp. Med."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e60","DOI":"10.1038\/emi.2013.58","article-title":"IL-17 cytokines in immunity and inflammation","volume":"2","author":"Jin","year":"2013","journal-title":"Emerg Microbes Infect."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"928461","DOI":"10.1155\/2014\/928461","article-title":"Role of Th17 Cells in the Pathogenesis of Human IBD","volume":"2014","author":"Galvez","year":"2014","journal-title":"ISRN Inflamm"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2271","DOI":"10.1084\/jem.20061308","article-title":"Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides","volume":"203","author":"Liang","year":"2006","journal-title":"J. Exp. Med."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1038\/nature06764","article-title":"Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome","volume":"452","author":"Milner","year":"2008","journal-title":"Nature"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1002\/ibd.20339","article-title":"Role of the novel Th17 cytokine IL-17F in inflammatory bowel disease (IBD): Upregulated colonic IL-17F expression in active Crohn\u2019s disease and analysis of the IL17F p.His161Arg polymorphism in IBD","volume":"14","author":"Seiderer","year":"2008","journal-title":"Inflamm. Bowel. Dis."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1063","DOI":"10.1084\/jem.20071978","article-title":"Regulation of inflammatory responses by IL-17F","volume":"205","author":"Yang","year":"2008","journal-title":"J. Exp. Med."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1038\/nrgastro.2017.88","article-title":"Gut microbiota and IBD: Causation or correlation?","volume":"14","author":"Ni","year":"2017","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_52","first-page":"209","article-title":"Fecal Microbiota Transplantation: From Clostridium difficile to Inflammatory Bowel Disease","volume":"13","author":"Gianotti","year":"2017","journal-title":"Gastroenterol. Hepatol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"4","DOI":"10.4161\/gmic.19320","article-title":"The role of gut microbiota in immune homeostasis and autoimmunity","volume":"3","author":"Wu","year":"2012","journal-title":"Gut Microbes"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1111\/imr.12185","article-title":"The role of the adaptive immune system in regulation of gut microbiota","volume":"260","author":"Kato","year":"2014","journal-title":"Immunol. Rev."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Chen, W., Liu, F., Ling, Z., Tong, X., and Xiang, C. (2012). Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0039743"},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Zhu, Q., Jin, Z., Wu, W., Gao, R., Guo, B., Gao, Z., Yang, Y., and Qin, H. (2014). Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0090849"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1136\/gutjnl-2015-309333","article-title":"Dysbiotic gut microbiota causes transmissible Crohn\u2019s disease-like ileitis independent of failure in antimicrobial defence","volume":"65","author":"Schaubeck","year":"2016","journal-title":"Gut"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1093\/infdis\/jiu409","article-title":"Intestinal microbiota, microbial translocation, and systemic inflammmation in chronic HIV infection","volume":"211","author":"Dinh","year":"2015","journal-title":"J. Infect. Dis."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"7551","DOI":"10.1128\/AEM.02676-14","article-title":"Dynamics of gut microbiota in autoimmune lupus","volume":"80","author":"Zhang","year":"2014","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"4892","DOI":"10.3748\/wjg.v16.i39.4892","article-title":"Clostridium difficile infection and inflammatory bowel disease: Understanding the evolving relationship","volume":"16","author":"Navaneethan","year":"2010","journal-title":"World J. Gastroenterol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1097\/MIB.0000000000000998","article-title":"Clostridium difficile Infection and Risk of Colectomy in Patients with Inflammatory Bowel Disease: A Bias-adjusted Meta-analysis","volume":"23","author":"Chen","year":"2017","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"6371","DOI":"10.1096\/fj.201800370R","article-title":"Obesity treatment by epigallocatechin-3-gallate-regulated bile acid signaling and its enriched Akkermansia muciniphila","volume":"32","author":"Sheng","year":"2018","journal-title":"FASEB J."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"9066","DOI":"10.1073\/pnas.1219451110","article-title":"Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity","volume":"110","author":"Everard","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1519","DOI":"10.3748\/wjg.v17.i12.1519","article-title":"Potential beneficial effects of butyrate in intestinal and extraintestinal diseases","volume":"17","author":"Canani","year":"2011","journal-title":"World J. Gastroenterol"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"2099","DOI":"10.1128\/JB.186.7.2099-2106.2004","article-title":"Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon","volume":"186","author":"Louis","year":"2004","journal-title":"J. Bacteriol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1111\/j.1365-2036.2007.03562.x","article-title":"Review article: The role of butyrate on colonic function","volume":"27","author":"Hamer","year":"2008","journal-title":"Aliment. Pharm."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1079\/BJN20041150","article-title":"Contribution of acetate to butyrate formation by human faecal bacteria","volume":"91","author":"Duncan","year":"2004","journal-title":"Br. J. Nutr."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1038\/ajgsup.2012.6","article-title":"Methanogens in human health and disease","volume":"6","author":"Pimental","year":"2012","journal-title":"Am. J. Gastroenterol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1016\/0016-5085(84)90532-8","article-title":"Methane Production and Colon Cancer","volume":"87","author":"Pique","year":"1984","journal-title":"Gastroenterology"}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/14\/14\/2788\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:43:27Z","timestamp":1760139807000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/14\/14\/2788"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,6]]},"references-count":69,"journal-issue":{"issue":"14","published-online":{"date-parts":[[2022,7]]}},"alternative-id":["nu14142788"],"URL":"https:\/\/doi.org\/10.3390\/nu14142788","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,6]]}}}