Lactiplantibacillus plantarum 299v supplementation modulates β-cell ER stress and antioxidative defense pathways and prevents type 1 diabetes in gluten-free BioBreeding rats
The increasing incidence of Type 1 diabetes has coincided with the emergence of the low-fiber, high-gluten Western diet and other environmental factors linked to dysbiosis. Since Lactiplantibacillus plantarum 299 v (Lp299v) supplementation improves gut barrier function and reduces systemic inflammat...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2022-12-01
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| Series: | Gut Microbes |
| Subjects: | |
| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2022.2136467 |
| _version_ | 1798027968929333248 |
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| author | Pinar Sargin Mark F. Roethle Shuang Jia Tarun Pant Ashley E. Ciecko Samantha N. Atkinson Nita H. Salzman Ru-Jeng Teng Yi-Guang Chen Susanne M. Cabrera Martin J. Hessner |
| author_facet | Pinar Sargin Mark F. Roethle Shuang Jia Tarun Pant Ashley E. Ciecko Samantha N. Atkinson Nita H. Salzman Ru-Jeng Teng Yi-Guang Chen Susanne M. Cabrera Martin J. Hessner |
| author_sort | Pinar Sargin |
| collection | DOAJ |
| description | The increasing incidence of Type 1 diabetes has coincided with the emergence of the low-fiber, high-gluten Western diet and other environmental factors linked to dysbiosis. Since Lactiplantibacillus plantarum 299 v (Lp299v) supplementation improves gut barrier function and reduces systemic inflammation, we studied its effects in spontaneously diabetic DRlyp/lyp rats provided a normal cereal diet (ND) or a gluten-free hydrolyzed casein diet (HCD). All rats provided ND developed diabetes (62.5±7.7 days); combining ND with Lp299v did not improve survival. Diabetes was delayed by HCD (72.2±9.4 days, p = .01) and further delayed by HCD+Lp299v (84.9±14.3 days, p < .001). HCD+Lp299v pups exhibited increased plasma propionate and butyrate levels, which correlated with enriched fecal Bifidobacteriaceae and Clostridiales taxa. Islet transcriptomic and histologic analyses at 40-days of age revealed that rats fed HCD expressed an autophagy profile, while those provided HCD+Lp299v expressed ER-associated protein degradation (ERAD) and antioxidative defense pathways, including Nrf2. Exposing insulinoma cells to propionate and butyrate promoted the antioxidative defense response but did not recapitulate the HCD+Lp299v islet ERAD transcriptomic profile. Here, both diet and microbiota influenced diabetes susceptibility. Moreover, Lp299v supplement modulated antioxidative defense and ER stress responses in β-cells, potentially offering a new therapeutic direction to thwart diabetes progression and preserve insulin secretion. |
| first_indexed | 2024-04-11T19:00:18Z |
| format | Article |
| id | doaj.art-04e49acff871446096d9b0058aa801e5 |
| institution | Directory Open Access Journal |
| issn | 1949-0976 1949-0984 |
| language | English |
| last_indexed | 2024-04-11T19:00:18Z |
| publishDate | 2022-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj.art-04e49acff871446096d9b0058aa801e52022-12-22T04:08:03ZengTaylor & Francis GroupGut Microbes1949-09761949-09842022-12-0114110.1080/19490976.2022.2136467Lactiplantibacillus plantarum 299v supplementation modulates β-cell ER stress and antioxidative defense pathways and prevents type 1 diabetes in gluten-free BioBreeding ratsPinar Sargin0Mark F. Roethle1Shuang Jia2Tarun Pant3Ashley E. Ciecko4Samantha N. Atkinson5Nita H. Salzman6Ru-Jeng Teng7Yi-Guang Chen8Susanne M. Cabrera9Martin J. Hessner10The Max McGee Research Center for Juvenile Diabetes, Children’s Research Institute of Children’s Hospital of Wisconsin, Milwaukee, WI, USAThe Max McGee Research Center for Juvenile Diabetes, Children’s Research Institute of Children’s Hospital of Wisconsin, Milwaukee, WI, USAThe Max McGee Research Center for Juvenile Diabetes, Children’s Research Institute of Children’s Hospital of Wisconsin, Milwaukee, WI, USAThe Max McGee Research Center for Juvenile Diabetes, Children’s Research Institute of Children’s Hospital of Wisconsin, Milwaukee, WI, USAThe Max McGee Research Center for Juvenile Diabetes, Children’s Research Institute of Children’s Hospital of Wisconsin, Milwaukee, WI, USACenter for Microbiome Research, Medical College of Wisconsin, Milwaukee, WI, USACenter for Microbiome Research, Medical College of Wisconsin, Milwaukee, WI, USADepartment of Pediatrics, Division of Neonatology, the Medical College of Wisconsin, Milwaukee, WI, USAThe Max McGee Research Center for Juvenile Diabetes, Children’s Research Institute of Children’s Hospital of Wisconsin, Milwaukee, WI, USAThe Max McGee Research Center for Juvenile Diabetes, Children’s Research Institute of Children’s Hospital of Wisconsin, Milwaukee, WI, USAThe Max McGee Research Center for Juvenile Diabetes, Children’s Research Institute of Children’s Hospital of Wisconsin, Milwaukee, WI, USAThe increasing incidence of Type 1 diabetes has coincided with the emergence of the low-fiber, high-gluten Western diet and other environmental factors linked to dysbiosis. Since Lactiplantibacillus plantarum 299 v (Lp299v) supplementation improves gut barrier function and reduces systemic inflammation, we studied its effects in spontaneously diabetic DRlyp/lyp rats provided a normal cereal diet (ND) or a gluten-free hydrolyzed casein diet (HCD). All rats provided ND developed diabetes (62.5±7.7 days); combining ND with Lp299v did not improve survival. Diabetes was delayed by HCD (72.2±9.4 days, p = .01) and further delayed by HCD+Lp299v (84.9±14.3 days, p < .001). HCD+Lp299v pups exhibited increased plasma propionate and butyrate levels, which correlated with enriched fecal Bifidobacteriaceae and Clostridiales taxa. Islet transcriptomic and histologic analyses at 40-days of age revealed that rats fed HCD expressed an autophagy profile, while those provided HCD+Lp299v expressed ER-associated protein degradation (ERAD) and antioxidative defense pathways, including Nrf2. Exposing insulinoma cells to propionate and butyrate promoted the antioxidative defense response but did not recapitulate the HCD+Lp299v islet ERAD transcriptomic profile. Here, both diet and microbiota influenced diabetes susceptibility. Moreover, Lp299v supplement modulated antioxidative defense and ER stress responses in β-cells, potentially offering a new therapeutic direction to thwart diabetes progression and preserve insulin secretion.https://www.tandfonline.com/doi/10.1080/19490976.2022.2136467Type 1 diabetesprobiotic supplementendoplasmic reticulum stressLactiplantibacillus plantarumbeta cellNrf2 |
| spellingShingle | Pinar Sargin Mark F. Roethle Shuang Jia Tarun Pant Ashley E. Ciecko Samantha N. Atkinson Nita H. Salzman Ru-Jeng Teng Yi-Guang Chen Susanne M. Cabrera Martin J. Hessner Lactiplantibacillus plantarum 299v supplementation modulates β-cell ER stress and antioxidative defense pathways and prevents type 1 diabetes in gluten-free BioBreeding rats Gut Microbes Type 1 diabetes probiotic supplement endoplasmic reticulum stress Lactiplantibacillus plantarum beta cell Nrf2 |
| title | Lactiplantibacillus plantarum 299v supplementation modulates β-cell ER stress and antioxidative defense pathways and prevents type 1 diabetes in gluten-free BioBreeding rats |
| title_full | Lactiplantibacillus plantarum 299v supplementation modulates β-cell ER stress and antioxidative defense pathways and prevents type 1 diabetes in gluten-free BioBreeding rats |
| title_fullStr | Lactiplantibacillus plantarum 299v supplementation modulates β-cell ER stress and antioxidative defense pathways and prevents type 1 diabetes in gluten-free BioBreeding rats |
| title_full_unstemmed | Lactiplantibacillus plantarum 299v supplementation modulates β-cell ER stress and antioxidative defense pathways and prevents type 1 diabetes in gluten-free BioBreeding rats |
| title_short | Lactiplantibacillus plantarum 299v supplementation modulates β-cell ER stress and antioxidative defense pathways and prevents type 1 diabetes in gluten-free BioBreeding rats |
| title_sort | lactiplantibacillus plantarum 299v supplementation modulates β cell er stress and antioxidative defense pathways and prevents type 1 diabetes in gluten free biobreeding rats |
| topic | Type 1 diabetes probiotic supplement endoplasmic reticulum stress Lactiplantibacillus plantarum beta cell Nrf2 |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2022.2136467 |
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