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1,25(OH)2D3 Deficiency-Induced Gut Microbial Dysbiosis Degrades The Zhu et al. Gut Pathog (2019) 11:8 https://doi.org/10.1186/s13099-019-0291-z Gut Pathogens RESEARCH Open Access 1,25(OH)2D3 defciency-induced gut microbial dysbiosis degrades the colonic mucus barrier in Cyp27b1 knockout mouse model Wenjing Zhu1†, Jiayao Yan2†, Chunchun Zhi4, Qianwen Zhou1 and Xiaoqin Yuan1,3* Abstract Background: The relationship between disturbances of the gut microbiota and 1,25(OH)2D3 defciency has been established both in humans and animal models with a vitamin D poor diet or a lack of sun exposure. Our prior study / has demonstrated that Cyp27b1− − (Cyp27b1 knockout) mice that could not produce 1,25(OH)2D3 had signifcant colon infammation phenotypes. However, whether and how 1,25(OH)2D3 defciency due to the genetic deletion controls the gut homeostasis and modulates the composition of the gut microbiota remains to be explored. / Results: 1,25(OH)2D3 defciency impair the composition of the gut microbiota and metabolite in Cyp27b1− − mice, including Akkermansia muciniphila, Solitalea Canadensis, Bacteroides-acidifaciens, Bacteroides plebeius and SCFA produc- tion. 1,25(OH)2D3 defciency cause the thinner colonic mucus layer and increase the translocation of the bacteria to the mesenteric lymph nodes. We also found 1,25(OH)2D3 supplement signifcantly decreased Akkermansia muciniphila / abundance in fecal samples of Cyp27b1− − mice. Conclusion: Defciency in 1,25(OH)2D3 impairs the composition of gut microbiota leading to disruption of intestinal epithelial barrier homeostasis and induction of colonic infammation. This study highlights the association between 1,25(OH)2D3 status, the gut microbiota and the colonic mucus barrier that is regarded as a primary defense against enteric pathogens. Keywords: 1,25(OH)2D3 defciency, Infammatory bowel disease, Gut microbiota, Colonic mucus barrier Background 25(OH)D < 20 ng/ml) or vitamin D- insufciency (serum Vitamin D is a prohormone that can be converted to the 25(OH)D < 30 ng/ml) is related to an increased risk of active form of 1,25-dihydroxyvitamin D3 [1,25(OH)2D3] infammatory bowel disease (IBD) [3, 4]. Several studies by 1α-hydroxylase encoded by the Cyp27b1 gene [1]. In have reported that vitamin D defciency is often observed addition to its role in regulating Ca2+ and Pi transport in patients with newly diagnosed IBD [5–7]. Conversely, and bone mineralization, 1,25(OH)2D3 also possesses high vitamin D intake can lower IBD risk [8]. In mouse various biological activities through binding vitamin D models, 1,25(OH)2D3 defciency or VDR knockout receptor (VDR), a high-afnity nuclear receptor that increased the risk of colitis [9–11]. In either trinitroben- transcriptionally regulates its target genes [2]. Tere is zene sulphonic acid (TNBS)- or dextran sodium sulphate growing epidemiological evidence demonstrating that (DSS)-induced colitis mice models, administration of vitamin D-defciency (commonly defned as serum 1,25(OH)2D3 efectively reduced the disease severity [9, 12]. Terefore, vitamin D might play a protective role *Correspondence: [email protected] for IBD. Te role vitamin D plays in the pathogenesis of †Wenjing Zhu and Jiayao Yan contributed equally to this work IBD is complex and not well defned. Some investiga- 1 Department of Anatomy, Histology and Embryology, Nanjing Medical tions have shown that 1,25(OH)2D3 has a pivotal role in University, Xuehai Building, Rm D509, 101 Longmian Avenue, Jiangning District, Nanjing 211166, China the development of IBD via regulating innate and adap- Full list of author information is available at the end of the article tive immune response [13], autophagy [14] or gut barrier © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhu et al. Gut Pathog (2019) 11:8 Page 2 of 11 integrity [15]. Our prior study revealed that Cyp27b1 dis- histological scores as compared to that of WT mice ruption induced colon infammation in mice by increas- (Fig. 1a, b). Cyp27b1−/− mice also had increased proin- ing oxidative stress and DNA damage consequently fammatory cytokines in the colonic tissue (Fig. 1c). Tus, leading to induction of cell senescence and mass genera- 1,25(OH)2D3 defciency induced colonic infammation. tion of senescence-associated secretory factors [11]. Infammatory bowel disease, i.e. Crohn’s disease and Efects of 1,25(OH)2D3 defciency on gut microbiota ulcerative colitis, is chronic relapsing and incurable Having demonstrated that the composition of the gut infammatory conditions of the bowel with an increas- microbiota was dependent on 1,25(OH)2D3, we next ing trend of incidence and prevalence [16]. IBD is one examined whether bacterial populations in WT mice of major health problems in the Western world as about were diferent from those in Cyp27b1−/− mice by 16S 0.5% of the general population are aficted with this rRNA sequencing of bacterial DNA extracted from the disease [17]. Although the pathogenic factors have not feces of these mice. Te OTU (operational taxonomic been clarifed yet, recent studies have demonstrated that units) data were used for obtaining taxonomic assign- intestinal microbiota might have an essential role in the ments of the microbiomes of the tested samples. Based on development of IBD. Many studies demonstrated a lower the phylum levels, Firmicutes and Bacteroidetes together diversity of the microbiome in IBD patients as com- represented a major part of the bacterial population in pared with healthy controls, but a higher abundance of all the samples tested. Figure 2a showed the diferences certain bacterial strains such as Enterobacteriaceae, and in the gut microbiota at the class level, in which Bacte- a stronger mucosal adherence of the bacteria [18, 19]. roidia, Erysipelotrichia, Clostridia, Verrucomicrobiae, Although the gut microbiota has a role in IBD patho- Coriobacteriia, Gammaproteobacteria, Deltaproteobac- genesis, the exact role of dysbiosis is far from clear. Gut teria, unidentifed Actinobacteria and Betaproteobacteria microbial composition could be impacted by environ- belonged to the top list of the most represented classes. mental factors including diet, age or genetic factors. In Cyp27b1−/− mice, Verrucomicrobiae and Deltaproteo- Some studies have shown that vitamin D infuenced the bacteria were enriched, and Bacteroidia was decreased function and composition of bacterial communities in with signifcant diference in the feces. Statistical analy- the gut in a protective way against dysbiosis and experi- sis revealed that Akkermansia muciniphila (A. mucin- mental IBD in mouse DSS model [20]. Our prior obser- iphila) and Solitalea canadensis were more abundant −/− −/− vation indicates that Cyp27b1 mice with 1,25(OH)2D3 in Cyp27b1 mice, especially A. muciniphila being defciency displayed severe colonic infammation at the afected to an even higher extent in Cyp27b1−/− mice age of 8–10 month [11]. In an attempt to examine the (Fig. 2b). Quantitative PCR analysis using primers spe- efect of 1,25(OH)2D3 defciency on gut microbiota in cifc to A. muciniphila further confrmed the increased the Cyp27b1−/− mice, we used 16S rRNA sequencing abundance of this bacterium in Cyp27b1−/− as com- to dissect the composition of the gut microbiota and pared to WT mice (Fig. 2c). A. muciniphila was a mucin- found gut dysbiosis in KO mice with a thinner mucus degrading bacterium, and Solitalea canadensis was also layer. Terefore, in this study we made an hypothesis reported to degrade N-glycan with enzymatic secre- that 1,25(OH)2D3 defciency may infuence gut homeo- tion [21]. We also found that Bacteroides-acidifaciens, stasis and induce the enrichment of some strains of bac- Bacteroides plebeius, Bacteroides uniformis, and Rose- teria such as A. muciniphila, Bacteroides-acidifaciens buria inulinivorans, which are assumed to yield short in the Cyp27b1−/− mice, thereby damaging the colonic chain fatty acids (SCFA), were more abundant in WT mucus barrier that would allow a greater microbial mice (Fig. 2b). Butyrate, one of SCFA, is a main energy access to the intestinal mucosa further promoting colonic source for intestinal epithelial cells. Te concentration of infammation. butyrate was decreased in the feces of Cyp27b1−/− mice as determined by gas chromatography (Fig. 2d). Tese Results observations clearly indicate that 1,25(OH)2D3 defciency Induction of colonic infammation by 1,25(OH)2D3 could impair the composition of the gut microbiota, par- defciency ticularly the relative abundance of A. muciniphila, and We have previously shown that Cyp27b1−/− (KO) mice SCFA-producing bacterium. defcient in 1,25(OH)2D3 presented with signifcant colon infammation phenotypes such as shortened colon 1,25(OH)2D3 defciency causes degradation of the colonic length, disordered mucosal structure, and infammatory mucus barrier cell infltration [11]. In accord with the increased levels Since gut microbes are important to maintain the integ- / of infammation at the age of 8–10 months, Cyp27b1− − rity of mucus barrier, one possible mechanism by which mice had an increase in spleen weight and higher defciency in 1,25(OH)2D3 causes colon infammation Zhu et al. Gut Pathog (2019) 11:8 Page 3 of 11 a 100X 200X 400X WT KO Hyperplasia Histologicalscore IECdamage %) 10 Inflammation e( 8 * or Sc 6 ve 4 ti la 2 mu 0 Cu T O W K b c ) 150 el 10 ev mg * * WT t( 8 Al KO 100 gh 6 RN ei 4 * 50 em * * nw * iv 2 ee at pl el 0 S 0 R β 6 3 1 α - - -1 L F 1 L L I MP WT KO I I HG M Fig.
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