Anti-inflammatory Effect of Probiotic Limosilactobacillus reuteri KUB-AC5 Against Salmonella Infection in a Mouse Colitis Model
Acute non-typhoidal salmonellosis (NTS) caused by Salmonella enterica Typhimurium (STM) is among the most prevalent of foodborne diseases. A global rising of antibiotic resistance strains of STM raises an urgent need for alternative methods to control this important pathogen. Major human food animal...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-08-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.716761/full |
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| author | Songphon Buddhasiri Chutikarn Sukjoi Thattawan Kaewsakhorn Kowit Nambunmee Kowit Nambunmee Massalin Nakphaichit Sunee Nitisinprasert Parameth Thiennimitr Parameth Thiennimitr Parameth Thiennimitr |
| author_facet | Songphon Buddhasiri Chutikarn Sukjoi Thattawan Kaewsakhorn Kowit Nambunmee Kowit Nambunmee Massalin Nakphaichit Sunee Nitisinprasert Parameth Thiennimitr Parameth Thiennimitr Parameth Thiennimitr |
| author_sort | Songphon Buddhasiri |
| collection | DOAJ |
| description | Acute non-typhoidal salmonellosis (NTS) caused by Salmonella enterica Typhimurium (STM) is among the most prevalent of foodborne diseases. A global rising of antibiotic resistance strains of STM raises an urgent need for alternative methods to control this important pathogen. Major human food animals which harbor STM in their gut are cattle, swine, and poultry. Previous studies showed that the probiotic Limosilactobacillus (Lactobacillus) reuteri KUB-AC5 (AC5) exhibited anti-Salmonella activities in chicken by modulating gut microbiota and the immune response. However, the immunobiotic effect of AC5 in a mammalian host is still not known. Here, we investigated the anti-Salmonella and anti-inflammatory effects of AC5 on STM infection using a mouse colitis model. Three groups of C57BL/6 mice (prophylactic, therapeutic, and combined) were fed with 109 colony-forming units (cfu) AC5 daily for 7, 4, and 11 days, respectively. Then, the mice were challenged with STM compared to the untreated group. By using a specific primer pair, we found that AC5 can transiently colonize mouse gut (colon, cecum, and ileum). Interestingly, AC5 reduced STM gut proliferation and invasion together with attenuated gut inflammation and systemic dissemination in mice. The decreased STM numbers in mouse gut lumen, gut tissues, and spleen possibly came from longer AC5 feeding duration and/or the combinatorial (direct and indirect inhibitory) effect of AC5 on STM. However, AC5 attenuated inflammation (both in the gut and in the spleen) with no difference between these three approaches. This study demonstrated that AC5 confers both direct and indirect inhibitory effects on STM in the inflamed gut. |
| first_indexed | 2024-12-17T00:23:47Z |
| format | Article |
| id | doaj.art-5cbb458be39c4d51958ac317b68bd144 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-17T00:23:47Z |
| publishDate | 2021-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-5cbb458be39c4d51958ac317b68bd1442022-12-21T22:10:31ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-08-011210.3389/fmicb.2021.716761716761Anti-inflammatory Effect of Probiotic Limosilactobacillus reuteri KUB-AC5 Against Salmonella Infection in a Mouse Colitis ModelSongphon Buddhasiri0Chutikarn Sukjoi1Thattawan Kaewsakhorn2Kowit Nambunmee3Kowit Nambunmee4Massalin Nakphaichit5Sunee Nitisinprasert6Parameth Thiennimitr7Parameth Thiennimitr8Parameth Thiennimitr9Department of Microbiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, ThailandDepartment of Microbiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, ThailandDepartment of Veterinary Biosciences and Veterinary Public Health, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, ThailandMajor of Occupational Health and Safety, School of Health Science, Mae Fah Luang University, Chiang Rai, ThailandUrban Safety Innovation Research Group, Mae Fah Luang University, Chiang Rai, ThailandDepartment of Biotechnology, Faculty of Agro-Industry, Kasetsart University, Bangkok, ThailandDepartment of Biotechnology, Faculty of Agro-Industry, Kasetsart University, Bangkok, ThailandDepartment of Microbiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, ThailandResearch Center of Microbial Diversity and Sustainable Utilization, Chiang Mai University, Chiang Mai, ThailandFaculty of Medicine, Center of Multidisciplinary Technology for Advanced Medicine, Chiang Mai University, Chiang Mai, ThailandAcute non-typhoidal salmonellosis (NTS) caused by Salmonella enterica Typhimurium (STM) is among the most prevalent of foodborne diseases. A global rising of antibiotic resistance strains of STM raises an urgent need for alternative methods to control this important pathogen. Major human food animals which harbor STM in their gut are cattle, swine, and poultry. Previous studies showed that the probiotic Limosilactobacillus (Lactobacillus) reuteri KUB-AC5 (AC5) exhibited anti-Salmonella activities in chicken by modulating gut microbiota and the immune response. However, the immunobiotic effect of AC5 in a mammalian host is still not known. Here, we investigated the anti-Salmonella and anti-inflammatory effects of AC5 on STM infection using a mouse colitis model. Three groups of C57BL/6 mice (prophylactic, therapeutic, and combined) were fed with 109 colony-forming units (cfu) AC5 daily for 7, 4, and 11 days, respectively. Then, the mice were challenged with STM compared to the untreated group. By using a specific primer pair, we found that AC5 can transiently colonize mouse gut (colon, cecum, and ileum). Interestingly, AC5 reduced STM gut proliferation and invasion together with attenuated gut inflammation and systemic dissemination in mice. The decreased STM numbers in mouse gut lumen, gut tissues, and spleen possibly came from longer AC5 feeding duration and/or the combinatorial (direct and indirect inhibitory) effect of AC5 on STM. However, AC5 attenuated inflammation (both in the gut and in the spleen) with no difference between these three approaches. This study demonstrated that AC5 confers both direct and indirect inhibitory effects on STM in the inflamed gut.https://www.frontiersin.org/articles/10.3389/fmicb.2021.716761/fullacute non-typhoidal salmonellosisSalmonella enterica Typhimuriumprobiotic Limosilactobacillus (Lactobacillus)mouse colitis modelanti-inflammatory effectimmunomodulation |
| spellingShingle | Songphon Buddhasiri Chutikarn Sukjoi Thattawan Kaewsakhorn Kowit Nambunmee Kowit Nambunmee Massalin Nakphaichit Sunee Nitisinprasert Parameth Thiennimitr Parameth Thiennimitr Parameth Thiennimitr Anti-inflammatory Effect of Probiotic Limosilactobacillus reuteri KUB-AC5 Against Salmonella Infection in a Mouse Colitis Model Frontiers in Microbiology acute non-typhoidal salmonellosis Salmonella enterica Typhimurium probiotic Limosilactobacillus (Lactobacillus) mouse colitis model anti-inflammatory effect immunomodulation |
| title | Anti-inflammatory Effect of Probiotic Limosilactobacillus reuteri KUB-AC5 Against Salmonella Infection in a Mouse Colitis Model |
| title_full | Anti-inflammatory Effect of Probiotic Limosilactobacillus reuteri KUB-AC5 Against Salmonella Infection in a Mouse Colitis Model |
| title_fullStr | Anti-inflammatory Effect of Probiotic Limosilactobacillus reuteri KUB-AC5 Against Salmonella Infection in a Mouse Colitis Model |
| title_full_unstemmed | Anti-inflammatory Effect of Probiotic Limosilactobacillus reuteri KUB-AC5 Against Salmonella Infection in a Mouse Colitis Model |
| title_short | Anti-inflammatory Effect of Probiotic Limosilactobacillus reuteri KUB-AC5 Against Salmonella Infection in a Mouse Colitis Model |
| title_sort | anti inflammatory effect of probiotic limosilactobacillus reuteri kub ac5 against salmonella infection in a mouse colitis model |
| topic | acute non-typhoidal salmonellosis Salmonella enterica Typhimurium probiotic Limosilactobacillus (Lactobacillus) mouse colitis model anti-inflammatory effect immunomodulation |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.716761/full |
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