Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis
Developing effective strategies to prevent diarrhea and associated-gut disorders in mammals has gained great significance. Owing to the many health benefits provided by the commensal microbiota of the intestinal tract, such as against environmental perturbation, we explored the host phenotype-associ...
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| Format: | Article |
| Language: | English |
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KeAi Communications Co., Ltd.
2023-12-01
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| Series: | Animal Nutrition |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S240565452300094X |
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| author | Long Yuan Chuyang Zhu Fang Gu Miaonan Zhu Jiacheng Yao Cuipeng Zhu Shicheng Li Kun Wang Ping Hu Yunzeng Zhang Demin Cai Hao-Yu Liu |
| author_facet | Long Yuan Chuyang Zhu Fang Gu Miaonan Zhu Jiacheng Yao Cuipeng Zhu Shicheng Li Kun Wang Ping Hu Yunzeng Zhang Demin Cai Hao-Yu Liu |
| author_sort | Long Yuan |
| collection | DOAJ |
| description | Developing effective strategies to prevent diarrhea and associated-gut disorders in mammals has gained great significance. Owing to the many health benefits provided by the commensal microbiota of the intestinal tract, such as against environmental perturbation, we explored the host phenotype-associated microbes and their probiotic potential. Based on the observations that the chronic heat stress-exposed weaned piglets present as heat stress-susceptible (HS-SUS) or heat stress-resistant (HS-RES) individuals, we confirmed the phenotypic difference between the two on growth performance (P < 0.05), diarrhea index (P < 0.001), intestinal heat shock protein 70 (HSP70) regulation (P < 0.01), and inflammatory responses (P < 0.01). By comparing the gut microbiome using 16S rRNA gene sequencing and KEGG functional analysis, we found that Lactobacillus johnsonii exhibited significantly higher relative abundance in the HS-RES piglets than in the HS-SUS ones (P < 0.05). Further experiments using a mouse model for chemical-induced inflammation and intestinal injury demonstrated that oral administration of a representative L. johnsonii N5 (isolated from the HS-RES piglets) ameliorated the clinical and histological signs of colitis while suppressing intestinal pro-inflammatory cytokines TNF-α and IL-6 production (P < 0.05). We found that N5 treatment enhanced tight junction proteins ZO-1 and occludin and cytoprotective HSP70 levels under physiological condition and restored their mucosal expressions in colitis (P < 0.05). In support of the high production of the anti-inflammatory cytokine IL-10, N5 promoted the intestinal Peyer's patches MHCII+ and CD103+ dendritic cell populations (P < 0.05), increased the regulatory T (Treg) cell numbers (P < 0.05), and decreased the Th17 population and its IL-17a production under physiological condition and during colitis (P < 0.01). Our results shed light on understanding the interaction between commensal Lactobacillus and the host health, and provide L. johnsonii N5 as an alternative to antibiotics for preventing diarrhea and intestinal diseases. |
| first_indexed | 2024-03-08T21:29:42Z |
| format | Article |
| id | doaj.art-eed372b0a6bc400093510a508199e85d |
| institution | Directory Open Access Journal |
| issn | 2405-6545 |
| language | English |
| last_indexed | 2024-03-08T21:29:42Z |
| publishDate | 2023-12-01 |
| publisher | KeAi Communications Co., Ltd. |
| record_format | Article |
| series | Animal Nutrition |
| spelling | doaj.art-eed372b0a6bc400093510a508199e85d2023-12-21T07:32:59ZengKeAi Communications Co., Ltd.Animal Nutrition2405-65452023-12-0115210224Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitisLong Yuan0Chuyang Zhu1Fang Gu2Miaonan Zhu3Jiacheng Yao4Cuipeng Zhu5Shicheng Li6Kun Wang7Ping Hu8Yunzeng Zhang9Demin Cai10Hao-Yu Liu11College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China; Joint International Research Laboratory of Agricultural & Agri-Product Safety, The Ministry of Education of China, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China; Joint International Research Laboratory of Agricultural & Agri-Product Safety, The Ministry of Education of China, Yangzhou University, Yangzhou 225009, China; Corresponding authors.College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China; Joint International Research Laboratory of Agricultural & Agri-Product Safety, The Ministry of Education of China, Yangzhou University, Yangzhou 225009, China; Corresponding authors.Developing effective strategies to prevent diarrhea and associated-gut disorders in mammals has gained great significance. Owing to the many health benefits provided by the commensal microbiota of the intestinal tract, such as against environmental perturbation, we explored the host phenotype-associated microbes and their probiotic potential. Based on the observations that the chronic heat stress-exposed weaned piglets present as heat stress-susceptible (HS-SUS) or heat stress-resistant (HS-RES) individuals, we confirmed the phenotypic difference between the two on growth performance (P < 0.05), diarrhea index (P < 0.001), intestinal heat shock protein 70 (HSP70) regulation (P < 0.01), and inflammatory responses (P < 0.01). By comparing the gut microbiome using 16S rRNA gene sequencing and KEGG functional analysis, we found that Lactobacillus johnsonii exhibited significantly higher relative abundance in the HS-RES piglets than in the HS-SUS ones (P < 0.05). Further experiments using a mouse model for chemical-induced inflammation and intestinal injury demonstrated that oral administration of a representative L. johnsonii N5 (isolated from the HS-RES piglets) ameliorated the clinical and histological signs of colitis while suppressing intestinal pro-inflammatory cytokines TNF-α and IL-6 production (P < 0.05). We found that N5 treatment enhanced tight junction proteins ZO-1 and occludin and cytoprotective HSP70 levels under physiological condition and restored their mucosal expressions in colitis (P < 0.05). In support of the high production of the anti-inflammatory cytokine IL-10, N5 promoted the intestinal Peyer's patches MHCII+ and CD103+ dendritic cell populations (P < 0.05), increased the regulatory T (Treg) cell numbers (P < 0.05), and decreased the Th17 population and its IL-17a production under physiological condition and during colitis (P < 0.01). Our results shed light on understanding the interaction between commensal Lactobacillus and the host health, and provide L. johnsonii N5 as an alternative to antibiotics for preventing diarrhea and intestinal diseases.http://www.sciencedirect.com/science/article/pii/S240565452300094XLactobacillus johnsoniiProbioticHeat shock proteinDiarrheaHeat stressTreg/Th17 |
| spellingShingle | Long Yuan Chuyang Zhu Fang Gu Miaonan Zhu Jiacheng Yao Cuipeng Zhu Shicheng Li Kun Wang Ping Hu Yunzeng Zhang Demin Cai Hao-Yu Liu Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis Animal Nutrition Lactobacillus johnsonii Probiotic Heat shock protein Diarrhea Heat stress Treg/Th17 |
| title | Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis |
| title_full | Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis |
| title_fullStr | Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis |
| title_full_unstemmed | Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis |
| title_short | Lactobacillus johnsonii N5 from heat stress-resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate-induced colitis |
| title_sort | lactobacillus johnsonii n5 from heat stress resistant pigs improves gut mucosal immunity and barrier in dextran sodium sulfate induced colitis |
| topic | Lactobacillus johnsonii Probiotic Heat shock protein Diarrhea Heat stress Treg/Th17 |
| url | http://www.sciencedirect.com/science/article/pii/S240565452300094X |
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