Maturation of the medaka immune system depends on reciprocal interactions between the microbiota and the intestinal tract
The interactions between the host immune system and intestinal microorganisms have been studied in many animals, including fish. However, a detailed analysis has not been performed in medaka, an established fish model for biological studies. Here, we investigated the effect of immunodeficiency on th...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-09-01
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| Series: | Frontiers in Immunology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1259519/full |
| _version_ | 1797688088274665472 |
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| author | Hiyori Sakaguchi Yuna Sato Ryo Matsumoto Joe Gomikawa Namie Yoshida Tomohiro Suzuki Masaru Matsuda Norimasa Iwanami |
| author_facet | Hiyori Sakaguchi Yuna Sato Ryo Matsumoto Joe Gomikawa Namie Yoshida Tomohiro Suzuki Masaru Matsuda Norimasa Iwanami |
| author_sort | Hiyori Sakaguchi |
| collection | DOAJ |
| description | The interactions between the host immune system and intestinal microorganisms have been studied in many animals, including fish. However, a detailed analysis has not been performed in medaka, an established fish model for biological studies. Here, we investigated the effect of immunodeficiency on the microbiota composition and the effect of gut bacteria on intestinal epithelial development and immune responses in medaka. Chronological analysis of the intestinal microbiota of interleukin 2 receptor subunit gamma (il2rg) mutant medaka showed a gradual decrease in the evenness of operational taxonomic units, mainly caused by the increased abundance of the Aeromonadaceae family. Exposure of wild-type medaka to high doses of an intestine-derived opportunistic bacterium of the Aeromonadaceae family induced an inflammatory response, suggesting a harmful effect on adult il2rg mutants. In addition, we established germ-free conditions in larval medaka and observed large absorptive vacuoles in intestinal epithelial cells, indicating a block in epithelial maturation. Transcriptome analysis revealed a decrease in the expression of genes involved in the defense response, including the antimicrobial peptide gene hepcidin, whose expression is induced by lipopolysaccharide stimulation in normal larvae. These results show that reciprocal interactions between the microbiome and the intestinal tract are required for the maturation of the medaka immune system. |
| first_indexed | 2024-03-12T01:26:34Z |
| format | Article |
| id | doaj.art-b838c58508fb427d8374c38dab13bf7b |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-03-12T01:26:34Z |
| publishDate | 2023-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-b838c58508fb427d8374c38dab13bf7b2023-09-12T17:24:11ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-09-011410.3389/fimmu.2023.12595191259519Maturation of the medaka immune system depends on reciprocal interactions between the microbiota and the intestinal tractHiyori SakaguchiYuna SatoRyo MatsumotoJoe GomikawaNamie YoshidaTomohiro SuzukiMasaru MatsudaNorimasa IwanamiThe interactions between the host immune system and intestinal microorganisms have been studied in many animals, including fish. However, a detailed analysis has not been performed in medaka, an established fish model for biological studies. Here, we investigated the effect of immunodeficiency on the microbiota composition and the effect of gut bacteria on intestinal epithelial development and immune responses in medaka. Chronological analysis of the intestinal microbiota of interleukin 2 receptor subunit gamma (il2rg) mutant medaka showed a gradual decrease in the evenness of operational taxonomic units, mainly caused by the increased abundance of the Aeromonadaceae family. Exposure of wild-type medaka to high doses of an intestine-derived opportunistic bacterium of the Aeromonadaceae family induced an inflammatory response, suggesting a harmful effect on adult il2rg mutants. In addition, we established germ-free conditions in larval medaka and observed large absorptive vacuoles in intestinal epithelial cells, indicating a block in epithelial maturation. Transcriptome analysis revealed a decrease in the expression of genes involved in the defense response, including the antimicrobial peptide gene hepcidin, whose expression is induced by lipopolysaccharide stimulation in normal larvae. These results show that reciprocal interactions between the microbiome and the intestinal tract are required for the maturation of the medaka immune system.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1259519/fullmedakamicrobiotaimmune systemgerm-freeSCID |
| spellingShingle | Hiyori Sakaguchi Yuna Sato Ryo Matsumoto Joe Gomikawa Namie Yoshida Tomohiro Suzuki Masaru Matsuda Norimasa Iwanami Maturation of the medaka immune system depends on reciprocal interactions between the microbiota and the intestinal tract Frontiers in Immunology medaka microbiota immune system germ-free SCID |
| title | Maturation of the medaka immune system depends on reciprocal interactions between the microbiota and the intestinal tract |
| title_full | Maturation of the medaka immune system depends on reciprocal interactions between the microbiota and the intestinal tract |
| title_fullStr | Maturation of the medaka immune system depends on reciprocal interactions between the microbiota and the intestinal tract |
| title_full_unstemmed | Maturation of the medaka immune system depends on reciprocal interactions between the microbiota and the intestinal tract |
| title_short | Maturation of the medaka immune system depends on reciprocal interactions between the microbiota and the intestinal tract |
| title_sort | maturation of the medaka immune system depends on reciprocal interactions between the microbiota and the intestinal tract |
| topic | medaka microbiota immune system germ-free SCID |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1259519/full |
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