A distinct metabolomic pattern revealed intestinal microenvironment factor-mediated food allergy in a BALB/c mouse model
Intestinal immune homeostasis plays a critical role in the pathogenesis of food allergy. However, the association between intestinal microenvironment factors and food allergy severity is not well studied. In this study, we established a gluten allergy (GA) BALB/c mouse model and revealed the intesti...
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| Format: | Article |
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Tsinghua University Press
2024-11-01
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| Series: | Food Science and Human Wellness |
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| Online Access: | https://www.sciopen.com/article/10.26599/FSHW.2023.9250049 |
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| author | Qiang Xie Chenglong Liu Wenhui Fu Chen Chen Dan Luo Shimin Gu Wentong Xue |
| author_facet | Qiang Xie Chenglong Liu Wenhui Fu Chen Chen Dan Luo Shimin Gu Wentong Xue |
| author_sort | Qiang Xie |
| collection | DOAJ |
| description | Intestinal immune homeostasis plays a critical role in the pathogenesis of food allergy. However, the association between intestinal microenvironment factors and food allergy severity is not well studied. In this study, we established a gluten allergy (GA) BALB/c mouse model and revealed the intestinal luminal factor-mediated alterations in phenotypes and endotypes of GA, combined with untargeted metabolomic profiling of the colonic contents. Our results showed that gluten sensitization induced severe allergic responses in BALB/c mice, characterized by exacerbated clinical allergic and diarrheal symptoms, increased histamine, elevated gluten-specific immunoglobulin (Ig)E and IgG2a levels, and increased mast cell degranulation. In response to GA, T-cell balance was disrupted, with aberrant production of interleukin (IL)-4, interferon (IFN)-γ, IL-10, and IL-2 in the spleen. GA led to a disrupted intestinal microenvironment homeostasis, including increased pH and water content, impaired intestinal antioxidant capacity and epithelial barrier function, decreased short-chain fatty acid production, and microbial dysbiosis, which was strongly correlated with GA severity. By metabolomic profiling, we found 29 differential expressed metabolites (DEMs) associated with GA, with 9 down-regulated and 20 up-regulated. A total of 11 out of all DEMs were classified into dipeptides, and 10 of them were up-regulated in the GA mice. Pathway enrichment analysis showed that most of the DEMs were enriched into the bile secretion metabolic route. |
| format | Article |
| id | doaj-art-b094295ebbb8430cbdef47ad0b496d01 |
| institution | Kabale University |
| issn | 2097-0765 2213-4530 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Tsinghua University Press |
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| series | Food Science and Human Wellness |
| spelling | doaj-art-b094295ebbb8430cbdef47ad0b496d012025-01-10T06:57:02ZengTsinghua University PressFood Science and Human Wellness2097-07652213-45302024-11-011363680369610.26599/FSHW.2023.9250049A distinct metabolomic pattern revealed intestinal microenvironment factor-mediated food allergy in a BALB/c mouse modelQiang Xie0Chenglong Liu1Wenhui Fu2Chen Chen3Dan Luo4Shimin Gu5Wentong Xue6College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100089, ChinaCollege of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100089, ChinaSchool of Medicine, Nankai University, Tianjin 300071, ChinaCollege of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100089, ChinaCollege of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100089, ChinaCollege of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100089, ChinaCollege of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100089, ChinaIntestinal immune homeostasis plays a critical role in the pathogenesis of food allergy. However, the association between intestinal microenvironment factors and food allergy severity is not well studied. In this study, we established a gluten allergy (GA) BALB/c mouse model and revealed the intestinal luminal factor-mediated alterations in phenotypes and endotypes of GA, combined with untargeted metabolomic profiling of the colonic contents. Our results showed that gluten sensitization induced severe allergic responses in BALB/c mice, characterized by exacerbated clinical allergic and diarrheal symptoms, increased histamine, elevated gluten-specific immunoglobulin (Ig)E and IgG2a levels, and increased mast cell degranulation. In response to GA, T-cell balance was disrupted, with aberrant production of interleukin (IL)-4, interferon (IFN)-γ, IL-10, and IL-2 in the spleen. GA led to a disrupted intestinal microenvironment homeostasis, including increased pH and water content, impaired intestinal antioxidant capacity and epithelial barrier function, decreased short-chain fatty acid production, and microbial dysbiosis, which was strongly correlated with GA severity. By metabolomic profiling, we found 29 differential expressed metabolites (DEMs) associated with GA, with 9 down-regulated and 20 up-regulated. A total of 11 out of all DEMs were classified into dipeptides, and 10 of them were up-regulated in the GA mice. Pathway enrichment analysis showed that most of the DEMs were enriched into the bile secretion metabolic route.https://www.sciopen.com/article/10.26599/FSHW.2023.9250049gluten allergyintestinal microenvironment homeostasisgut microbiotashort-chain fatty acidsbile secretion |
| spellingShingle | Qiang Xie Chenglong Liu Wenhui Fu Chen Chen Dan Luo Shimin Gu Wentong Xue A distinct metabolomic pattern revealed intestinal microenvironment factor-mediated food allergy in a BALB/c mouse model Food Science and Human Wellness gluten allergy intestinal microenvironment homeostasis gut microbiota short-chain fatty acids bile secretion |
| title | A distinct metabolomic pattern revealed intestinal microenvironment factor-mediated food allergy in a BALB/c mouse model |
| title_full | A distinct metabolomic pattern revealed intestinal microenvironment factor-mediated food allergy in a BALB/c mouse model |
| title_fullStr | A distinct metabolomic pattern revealed intestinal microenvironment factor-mediated food allergy in a BALB/c mouse model |
| title_full_unstemmed | A distinct metabolomic pattern revealed intestinal microenvironment factor-mediated food allergy in a BALB/c mouse model |
| title_short | A distinct metabolomic pattern revealed intestinal microenvironment factor-mediated food allergy in a BALB/c mouse model |
| title_sort | distinct metabolomic pattern revealed intestinal microenvironment factor mediated food allergy in a balb c mouse model |
| topic | gluten allergy intestinal microenvironment homeostasis gut microbiota short-chain fatty acids bile secretion |
| url | https://www.sciopen.com/article/10.26599/FSHW.2023.9250049 |
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