Interactions between host and intestinal crypt-resided biofilms are controlled by epithelial fucosylation
Summary: As highly organized consortia of bacteria, biofilms have long been implicated in aggravating inflammation. However, our understanding regarding in vivo host-biofilm interactions in the complex tissue environments remains limited. Here, we show a unique pattern of crypt occupation by mucus-a...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-07-01
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| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124723007659 |
| _version_ | 1797787222572793856 |
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| author | Xue-Kun Guo Jiali Wang Vincent P. van Hensbergen Jintao Liu Huji Xu Xiaoyu Hu |
| author_facet | Xue-Kun Guo Jiali Wang Vincent P. van Hensbergen Jintao Liu Huji Xu Xiaoyu Hu |
| author_sort | Xue-Kun Guo |
| collection | DOAJ |
| description | Summary: As highly organized consortia of bacteria, biofilms have long been implicated in aggravating inflammation. However, our understanding regarding in vivo host-biofilm interactions in the complex tissue environments remains limited. Here, we show a unique pattern of crypt occupation by mucus-associated biofilms during the early stage of colitis, which is genetically dependent on bacterial biofilm-forming capacity and restricted by host epithelial α1,2-fucosylation. α1,2-Fucosylation deficiency leads to markedly augmented crypt occupation by biofilms originated from pathogenic Salmonella Typhimurium or indigenous Escherichia coli, resulting in exacerbated intestinal inflammation. Mechanistically, α1,2-fucosylation-mediated restriction of biofilms relies on interactions between bacteria and liberated fucose from biofilm-occupied mucus. Fucose represses biofilm formation and biofilm-related genes in vitro and in vivo. Finally, fucose administration ameliorates experimental colitis, suggesting therapeutic potential of fucose for biofilm-related disorders. This work illustrates host-biofilm interactions during gut inflammation and identifies fucosylation as a physiological strategy for restraining biofilm formation. |
| first_indexed | 2024-03-13T01:19:54Z |
| format | Article |
| id | doaj.art-e131c9fad5244b2fab25899892ebdf55 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-03-13T01:19:54Z |
| publishDate | 2023-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-e131c9fad5244b2fab25899892ebdf552023-07-05T05:15:55ZengElsevierCell Reports2211-12472023-07-01427112754Interactions between host and intestinal crypt-resided biofilms are controlled by epithelial fucosylationXue-Kun Guo0Jiali Wang1Vincent P. van Hensbergen2Jintao Liu3Huji Xu4Xiaoyu Hu5Institute for Immunology and School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua-Peking Center for Life Sciences, Tsinghua University, Beijing 100084, China; Beijing Key Laboratory for Immunological Research on Chronic Diseases, Tsinghua University, Beijing 100084, China; Corresponding authorInstitute for Immunology and School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua-Peking Center for Life Sciences, Tsinghua University, Beijing 100084, China; Beijing Key Laboratory for Immunological Research on Chronic Diseases, Tsinghua University, Beijing 100084, ChinaInstitute for Immunology and School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua-Peking Center for Life Sciences, Tsinghua University, Beijing 100084, China; Beijing Key Laboratory for Immunological Research on Chronic Diseases, Tsinghua University, Beijing 100084, ChinaTsinghua-Peking Center for Life Sciences, Tsinghua University, Beijing 100084, China; Center for Infectious Disease Research, School of Medicine, Tsinghua University, Beijing 10084, ChinaTsinghua-Peking Center for Life Sciences, Tsinghua University, Beijing 100084, China; School of Clinical Medicine and School of Medicine, Tsinghua University, Beijing 100084, China; Department of Rheumatology and Immunology, Changzheng Hospital, Second Military Medical University, Shanghai 200003, China; Corresponding authorInstitute for Immunology and School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua-Peking Center for Life Sciences, Tsinghua University, Beijing 100084, China; Beijing Key Laboratory for Immunological Research on Chronic Diseases, Tsinghua University, Beijing 100084, China; Corresponding authorSummary: As highly organized consortia of bacteria, biofilms have long been implicated in aggravating inflammation. However, our understanding regarding in vivo host-biofilm interactions in the complex tissue environments remains limited. Here, we show a unique pattern of crypt occupation by mucus-associated biofilms during the early stage of colitis, which is genetically dependent on bacterial biofilm-forming capacity and restricted by host epithelial α1,2-fucosylation. α1,2-Fucosylation deficiency leads to markedly augmented crypt occupation by biofilms originated from pathogenic Salmonella Typhimurium or indigenous Escherichia coli, resulting in exacerbated intestinal inflammation. Mechanistically, α1,2-fucosylation-mediated restriction of biofilms relies on interactions between bacteria and liberated fucose from biofilm-occupied mucus. Fucose represses biofilm formation and biofilm-related genes in vitro and in vivo. Finally, fucose administration ameliorates experimental colitis, suggesting therapeutic potential of fucose for biofilm-related disorders. This work illustrates host-biofilm interactions during gut inflammation and identifies fucosylation as a physiological strategy for restraining biofilm formation.http://www.sciencedirect.com/science/article/pii/S2211124723007659CP: Microbiology |
| spellingShingle | Xue-Kun Guo Jiali Wang Vincent P. van Hensbergen Jintao Liu Huji Xu Xiaoyu Hu Interactions between host and intestinal crypt-resided biofilms are controlled by epithelial fucosylation Cell Reports CP: Microbiology |
| title | Interactions between host and intestinal crypt-resided biofilms are controlled by epithelial fucosylation |
| title_full | Interactions between host and intestinal crypt-resided biofilms are controlled by epithelial fucosylation |
| title_fullStr | Interactions between host and intestinal crypt-resided biofilms are controlled by epithelial fucosylation |
| title_full_unstemmed | Interactions between host and intestinal crypt-resided biofilms are controlled by epithelial fucosylation |
| title_short | Interactions between host and intestinal crypt-resided biofilms are controlled by epithelial fucosylation |
| title_sort | interactions between host and intestinal crypt resided biofilms are controlled by epithelial fucosylation |
| topic | CP: Microbiology |
| url | http://www.sciencedirect.com/science/article/pii/S2211124723007659 |
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