Ferroptosis is involved in deoxynivalenol-induced intestinal damage in pigs
Abstract Background Deoxynivalenol (DON) is a widespread issue for feed and food safety, leading to animal and human health risks. The objective of this study was to determine whether ferroptosis is involved in DON-induced intestinal injury in piglets. Three groups of 21-day-old male weanling piglet...
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| Format: | Article |
| Language: | English |
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BMC
2023-03-01
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| Series: | Journal of Animal Science and Biotechnology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40104-023-00841-4 |
| _version_ | 1797863968326287360 |
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| author | Meng Liu Lei Zhang Yixin Mo Jiahuan Li Jiacheng Yang Juan Wang Niel Alexander Karrow Hao Wu Lvhui Sun |
| author_facet | Meng Liu Lei Zhang Yixin Mo Jiahuan Li Jiacheng Yang Juan Wang Niel Alexander Karrow Hao Wu Lvhui Sun |
| author_sort | Meng Liu |
| collection | DOAJ |
| description | Abstract Background Deoxynivalenol (DON) is a widespread issue for feed and food safety, leading to animal and human health risks. The objective of this study was to determine whether ferroptosis is involved in DON-induced intestinal injury in piglets. Three groups of 21-day-old male weanling piglets (n = 7/group) were fed a control diet, or diet adding 1.0 or 3.0 mg DON/kg. At week 4, serum and small intestines were collected to assay for biochemistry, histology, redox status and ferroptosis-related genes expression. In addition, the involvement of ferroptosis and the role of FTL gene in DON-induced cell death were further verified in the IPEC-J2 cells. Results Compared to the control, dietary supplementation of DON at 1.0 and 3.0 mg/kg induced different degrees of damage in the duodenum, jejunum and ileum, and increased (P < 0.05) serum lipopolysaccharide concentration by 46.2%–51.4%. Dietary DON supplementation at 1.0 and (or) 3.0 mg/kg increased (P < 0.05) concentrations of malondialdehyde (17.4%–86.5%) and protein carbonyl by 33.1%–92.3% in the duodenum, jejunum and ileum. In addition, dietary supplemented with DON upregulated (P < 0.05) ferroptotic gene (DMT1) and anti-ferroptotic genes (FTL and FTH1), while downregulated (P < 0.05) anti-ferroptotic genes (FPN, FSP1 and CISD1) in the duodenum of the porcine. Furthermore, the in vitro study has demonstrated that deferiprone, a potent ferroptotic inhibitor, mitigated (P < 0.05) DON-induced cytotoxicity in porcine small intestinal IPEC-J2 cells. Additionally, deferiprone prevented or alleviated (P < 0.05) the dysregulation of ferroptosis-related genes (ACSL4 and FTL) by DON in IPEC-J2 cells. Moreover, specific siRNA knockdown FTL gene expression compromised the DON-induced cell death in IPEC-J2 cells. Conclusions In conclusion, this study revealed that ferroptosis is involved in DON-induced intestinal damage in porcine, and sheds a new light on the toxicity of DON to piglets. |
| first_indexed | 2024-04-09T22:44:08Z |
| format | Article |
| id | doaj.art-bfa86c817d2c49d3b3855102fa44f536 |
| institution | Directory Open Access Journal |
| issn | 2049-1891 |
| language | English |
| last_indexed | 2024-04-09T22:44:08Z |
| publishDate | 2023-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Journal of Animal Science and Biotechnology |
| spelling | doaj.art-bfa86c817d2c49d3b3855102fa44f5362023-03-22T12:00:01ZengBMCJournal of Animal Science and Biotechnology2049-18912023-03-0114111010.1186/s40104-023-00841-4Ferroptosis is involved in deoxynivalenol-induced intestinal damage in pigsMeng Liu0Lei Zhang1Yixin Mo2Jiahuan Li3Jiacheng Yang4Juan Wang5Niel Alexander Karrow6Hao Wu7Lvhui Sun8State Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Frontiers Science Center for Animal Breeding and Sustainable Production, College of Animal Sciences and Technology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Frontiers Science Center for Animal Breeding and Sustainable Production, College of Animal Sciences and Technology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Frontiers Science Center for Animal Breeding and Sustainable Production, College of Animal Sciences and Technology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Frontiers Science Center for Animal Breeding and Sustainable Production, College of Animal Sciences and Technology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Frontiers Science Center for Animal Breeding and Sustainable Production, College of Animal Sciences and Technology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Frontiers Science Center for Animal Breeding and Sustainable Production, College of Animal Sciences and Technology, Huazhong Agricultural UniversityDepartment of Animal Biosciences, University of GuelphState Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Frontiers Science Center for Animal Breeding and Sustainable Production, College of Animal Sciences and Technology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Frontiers Science Center for Animal Breeding and Sustainable Production, College of Animal Sciences and Technology, Huazhong Agricultural UniversityAbstract Background Deoxynivalenol (DON) is a widespread issue for feed and food safety, leading to animal and human health risks. The objective of this study was to determine whether ferroptosis is involved in DON-induced intestinal injury in piglets. Three groups of 21-day-old male weanling piglets (n = 7/group) were fed a control diet, or diet adding 1.0 or 3.0 mg DON/kg. At week 4, serum and small intestines were collected to assay for biochemistry, histology, redox status and ferroptosis-related genes expression. In addition, the involvement of ferroptosis and the role of FTL gene in DON-induced cell death were further verified in the IPEC-J2 cells. Results Compared to the control, dietary supplementation of DON at 1.0 and 3.0 mg/kg induced different degrees of damage in the duodenum, jejunum and ileum, and increased (P < 0.05) serum lipopolysaccharide concentration by 46.2%–51.4%. Dietary DON supplementation at 1.0 and (or) 3.0 mg/kg increased (P < 0.05) concentrations of malondialdehyde (17.4%–86.5%) and protein carbonyl by 33.1%–92.3% in the duodenum, jejunum and ileum. In addition, dietary supplemented with DON upregulated (P < 0.05) ferroptotic gene (DMT1) and anti-ferroptotic genes (FTL and FTH1), while downregulated (P < 0.05) anti-ferroptotic genes (FPN, FSP1 and CISD1) in the duodenum of the porcine. Furthermore, the in vitro study has demonstrated that deferiprone, a potent ferroptotic inhibitor, mitigated (P < 0.05) DON-induced cytotoxicity in porcine small intestinal IPEC-J2 cells. Additionally, deferiprone prevented or alleviated (P < 0.05) the dysregulation of ferroptosis-related genes (ACSL4 and FTL) by DON in IPEC-J2 cells. Moreover, specific siRNA knockdown FTL gene expression compromised the DON-induced cell death in IPEC-J2 cells. Conclusions In conclusion, this study revealed that ferroptosis is involved in DON-induced intestinal damage in porcine, and sheds a new light on the toxicity of DON to piglets.https://doi.org/10.1186/s40104-023-00841-4DeoxynivalenolFerroptosisIntestinePigletsToxicity |
| spellingShingle | Meng Liu Lei Zhang Yixin Mo Jiahuan Li Jiacheng Yang Juan Wang Niel Alexander Karrow Hao Wu Lvhui Sun Ferroptosis is involved in deoxynivalenol-induced intestinal damage in pigs Journal of Animal Science and Biotechnology Deoxynivalenol Ferroptosis Intestine Piglets Toxicity |
| title | Ferroptosis is involved in deoxynivalenol-induced intestinal damage in pigs |
| title_full | Ferroptosis is involved in deoxynivalenol-induced intestinal damage in pigs |
| title_fullStr | Ferroptosis is involved in deoxynivalenol-induced intestinal damage in pigs |
| title_full_unstemmed | Ferroptosis is involved in deoxynivalenol-induced intestinal damage in pigs |
| title_short | Ferroptosis is involved in deoxynivalenol-induced intestinal damage in pigs |
| title_sort | ferroptosis is involved in deoxynivalenol induced intestinal damage in pigs |
| topic | Deoxynivalenol Ferroptosis Intestine Piglets Toxicity |
| url | https://doi.org/10.1186/s40104-023-00841-4 |
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