Alteration of gastric microbiota and transcriptome in a rat with gastric intestinal metaplasia induced by deoxycholic acid
ObjectiveBile reflux plays a key role in the development of gastric intestinal metaplasia (GIM), an independent risk factor of gastric cancer. Here, we aimed to explore the biological mechanism of GIM induced by bile reflux in a rat model.MethodsRats were treated with 2% sodium salicylate and allowe...
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Frontiers Media S.A.
2023-05-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1160821/full |
| _version_ | 1797834749876633600 |
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| author | Zijing Xu Ling Xiao Shuaishuai Wang Yuqin Cheng Jianping Wu Yufen Meng Kaifan Bao Junfeng Zhang Chun Cheng |
| author_facet | Zijing Xu Ling Xiao Shuaishuai Wang Yuqin Cheng Jianping Wu Yufen Meng Kaifan Bao Junfeng Zhang Chun Cheng |
| author_sort | Zijing Xu |
| collection | DOAJ |
| description | ObjectiveBile reflux plays a key role in the development of gastric intestinal metaplasia (GIM), an independent risk factor of gastric cancer. Here, we aimed to explore the biological mechanism of GIM induced by bile reflux in a rat model.MethodsRats were treated with 2% sodium salicylate and allowed to freely drink 20 mmol/L sodium deoxycholate for 12 weeks, and GIM was confirmed by histopathological analysis. Gastric microbiota was profiled according to the 16S rDNA V3–V4 region, gastric transcriptome was sequenced, and serum bile acids (BAs) were analyzed by targeted metabolomics. Spearman's correlation analysis was used in constructing the network among gastric microbiota, serum BAs, and gene profiles. Real-time polymerase chain reaction (RT-PCR) measured the expression levels of nine genes in the gastric transcriptome.ResultsIn the stomach, deoxycholic acid (DCA) decreased the microbial diversity but promoted the abundances of several bacterial genera, such as Limosilactobacillus, Burkholderia–Caballeronia–Paraburkholderia, and Rikenellaceae RC9 gut group. Gastric transcriptome showed that the genes enriched in gastric acid secretion were significantly downregulated, whereas the genes enriched in fat digestion and absorption were obviously upregulated in GIM rats. The GIM rats had four promoted serum BAs, namely cholic acid (CA), DCA, taurocholic acid, and taurodeoxycholic acid. Further correlation analysis showed that the Rikenellaceae RC9 gut group was significantly positively correlated with DCA and RGD1311575 (capping protein-inhibiting regulator of actin dynamics), and RGD1311575 was positively correlated with Fabp1 (fatty acid-binding protein, liver), a key gene involved in fat digestion and absorption. Finally, the upregulated expression of Dgat1 (diacylglycerol acyltransferase 1) and Fabp1 related to fat digestion and absorption was identified by RT-PCR and IHC.ConclusionDCA-induced GIM enhanced gastric fat digestion and absorption function and impaired gastric acid secretion function. The DCA–Rikenellaceae RC9 gut group–RGD1311575/Fabp1 axis might play a key role in the mechanism of bile reflux-related GIM. |
| first_indexed | 2024-04-09T14:42:27Z |
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| id | doaj.art-89b77dc3a182459fa819d7f4eef354e5 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-09T14:42:27Z |
| publishDate | 2023-05-01 |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-89b77dc3a182459fa819d7f4eef354e52023-05-03T05:02:46ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-05-011410.3389/fmicb.2023.11608211160821Alteration of gastric microbiota and transcriptome in a rat with gastric intestinal metaplasia induced by deoxycholic acidZijing Xu0Ling Xiao1Shuaishuai Wang2Yuqin Cheng3Jianping Wu4Yufen Meng5Kaifan Bao6Junfeng Zhang7Chun Cheng8School of Medicine & Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, Jiangsu, ChinaSchool of Medicine & Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, Jiangsu, ChinaSchool of Medicine & Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, Jiangsu, ChinaSchool of Medicine & Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, Jiangsu, ChinaLaboratory Animal Center, Nanjing University of Chinese Medicine, Nanjing, Jiangsu, ChinaSchool of Medicine & Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, Jiangsu, ChinaSchool of Medicine & Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, Jiangsu, ChinaSchool of Medicine & Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, Jiangsu, ChinaSchool of Medicine & Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, Jiangsu, ChinaObjectiveBile reflux plays a key role in the development of gastric intestinal metaplasia (GIM), an independent risk factor of gastric cancer. Here, we aimed to explore the biological mechanism of GIM induced by bile reflux in a rat model.MethodsRats were treated with 2% sodium salicylate and allowed to freely drink 20 mmol/L sodium deoxycholate for 12 weeks, and GIM was confirmed by histopathological analysis. Gastric microbiota was profiled according to the 16S rDNA V3–V4 region, gastric transcriptome was sequenced, and serum bile acids (BAs) were analyzed by targeted metabolomics. Spearman's correlation analysis was used in constructing the network among gastric microbiota, serum BAs, and gene profiles. Real-time polymerase chain reaction (RT-PCR) measured the expression levels of nine genes in the gastric transcriptome.ResultsIn the stomach, deoxycholic acid (DCA) decreased the microbial diversity but promoted the abundances of several bacterial genera, such as Limosilactobacillus, Burkholderia–Caballeronia–Paraburkholderia, and Rikenellaceae RC9 gut group. Gastric transcriptome showed that the genes enriched in gastric acid secretion were significantly downregulated, whereas the genes enriched in fat digestion and absorption were obviously upregulated in GIM rats. The GIM rats had four promoted serum BAs, namely cholic acid (CA), DCA, taurocholic acid, and taurodeoxycholic acid. Further correlation analysis showed that the Rikenellaceae RC9 gut group was significantly positively correlated with DCA and RGD1311575 (capping protein-inhibiting regulator of actin dynamics), and RGD1311575 was positively correlated with Fabp1 (fatty acid-binding protein, liver), a key gene involved in fat digestion and absorption. Finally, the upregulated expression of Dgat1 (diacylglycerol acyltransferase 1) and Fabp1 related to fat digestion and absorption was identified by RT-PCR and IHC.ConclusionDCA-induced GIM enhanced gastric fat digestion and absorption function and impaired gastric acid secretion function. The DCA–Rikenellaceae RC9 gut group–RGD1311575/Fabp1 axis might play a key role in the mechanism of bile reflux-related GIM.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1160821/fullgastric intestinal metaplasiamicrobiotabile acidstranscriptomecorrelation analysis |
| spellingShingle | Zijing Xu Ling Xiao Shuaishuai Wang Yuqin Cheng Jianping Wu Yufen Meng Kaifan Bao Junfeng Zhang Chun Cheng Alteration of gastric microbiota and transcriptome in a rat with gastric intestinal metaplasia induced by deoxycholic acid Frontiers in Microbiology gastric intestinal metaplasia microbiota bile acids transcriptome correlation analysis |
| title | Alteration of gastric microbiota and transcriptome in a rat with gastric intestinal metaplasia induced by deoxycholic acid |
| title_full | Alteration of gastric microbiota and transcriptome in a rat with gastric intestinal metaplasia induced by deoxycholic acid |
| title_fullStr | Alteration of gastric microbiota and transcriptome in a rat with gastric intestinal metaplasia induced by deoxycholic acid |
| title_full_unstemmed | Alteration of gastric microbiota and transcriptome in a rat with gastric intestinal metaplasia induced by deoxycholic acid |
| title_short | Alteration of gastric microbiota and transcriptome in a rat with gastric intestinal metaplasia induced by deoxycholic acid |
| title_sort | alteration of gastric microbiota and transcriptome in a rat with gastric intestinal metaplasia induced by deoxycholic acid |
| topic | gastric intestinal metaplasia microbiota bile acids transcriptome correlation analysis |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1160821/full |
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