Impact of dietary manganese on intestinal barrier and inflammatory response in broilers challenged with Salmonella Typhimurium
- Author
- Huaiyong Zhang, Shuqin Pan, Keying Zhang, Joris Michiels (UGent) , Qiufeng Zeng, Xuemei Ding, Jianping Wang, Huanwei Peng, Jie Bai, Yue Xuan, Zhuowei Su and Shiping Bai
- Organization
- Abstract
- Growing concern for public health and food safety has prompted a special interest in developing nutritional strategies for removing waterborne and foodborne pathogens, including Salmonella. Strong links between manganese (Mn) and intestinal barrier or immune function hint that dietary Mn supplementation is likely to be a promising approach to limit the loads of pathogens in broilers. Here, we provide evidence that Salmonella Typhimurium (S. Typhimurium, 4 × 108 CFUs) challenge-induced intestinal injury along with systemic Mn redistribution in broilers. Further examining of the effect of dietary Mn treatments (a basal diet plus additional 0, 40, or 100 mg Mn/kg for corresponding to Mn-deficient, control, or Mn-surfeit diet, respectively) on intestinal barrier and inflammation status of broilers infected with S. Typhimurium revealed that birds fed the control and Mn-surfeit diets exhibited improved intestinal tight junctions and microbiota composition. Even without Salmonella infection, dietary Mn deficiency alone increased intestinal permeability by impairing intestinal tight junctions. In addition, when fed the control and Mn-surfeit diets, birds showed decreased Salmonella burdens in cecal content and spleen, with a concomitant increase in inflammatory cytokine levels in spleen. Furthermore, the dietary Mn-supplementation-mediated induction of cytokine production was probably associated with the nuclear factor kappa-B (NF-κB)/hydrogen peroxide (H2O2) pathway, as judged by the enhanced manganese superoxide dismutase activity and the increased H2O2 level in mitochondria, together with the increased mRNA level of NF-κB in spleen. Ingenuity-pathway analysis indicated that acute-phase response pathways, T helper type 1 pathway, and dendritic cell maturation were significantly activated by the dietary Mn supplementation. Our data suggest that dietary Mn supplementation could enhance intestinal barrier and splenic inflammatory response to fight against Salmonella infection in broilers.
- Keywords
- Mn, intestine, Salmonella, cytokine, mitochondria, broiler, ENTERICA SEROVAR TYPHIMURIUM, NF-KAPPA-B, IMMUNE-RESPONSE, GROWTH-PERFORMANCE, GUT MICROBIOTA, MACROPHAGES, METABOLISM, CYTOKINE, ROS, SUPPLEMENTATION
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Citation
Please use this url to cite or link to this publication: http://hdl.handle.net/1854/LU-8662998
- MLA
- Zhang, Huaiyong, et al. “Impact of Dietary Manganese on Intestinal Barrier and Inflammatory Response in Broilers Challenged with Salmonella Typhimurium.” MICROORGANISMS, vol. 8, no. 5, 2020, doi:10.3390/microorganisms8050757.
- APA
- Zhang, H., Pan, S., Zhang, K., Michiels, J., Zeng, Q., Ding, X., … Bai, S. (2020). Impact of dietary manganese on intestinal barrier and inflammatory response in broilers challenged with Salmonella Typhimurium. MICROORGANISMS, 8(5). https://doi.org/10.3390/microorganisms8050757
- Chicago author-date
- Zhang, Huaiyong, Shuqin Pan, Keying Zhang, Joris Michiels, Qiufeng Zeng, Xuemei Ding, Jianping Wang, et al. 2020. “Impact of Dietary Manganese on Intestinal Barrier and Inflammatory Response in Broilers Challenged with Salmonella Typhimurium.” MICROORGANISMS 8 (5). https://doi.org/10.3390/microorganisms8050757.
- Chicago author-date (all authors)
- Zhang, Huaiyong, Shuqin Pan, Keying Zhang, Joris Michiels, Qiufeng Zeng, Xuemei Ding, Jianping Wang, Huanwei Peng, Jie Bai, Yue Xuan, Zhuowei Su, and Shiping Bai. 2020. “Impact of Dietary Manganese on Intestinal Barrier and Inflammatory Response in Broilers Challenged with Salmonella Typhimurium.” MICROORGANISMS 8 (5). doi:10.3390/microorganisms8050757.
- Vancouver
- 1.Zhang H, Pan S, Zhang K, Michiels J, Zeng Q, Ding X, et al. Impact of dietary manganese on intestinal barrier and inflammatory response in broilers challenged with Salmonella Typhimurium. MICROORGANISMS. 2020;8(5).
- IEEE
- [1]H. Zhang et al., “Impact of dietary manganese on intestinal barrier and inflammatory response in broilers challenged with Salmonella Typhimurium,” MICROORGANISMS, vol. 8, no. 5, 2020.
@article{8662998, abstract = {{Growing concern for public health and food safety has prompted a special interest in developing nutritional strategies for removing waterborne and foodborne pathogens, including Salmonella. Strong links between manganese (Mn) and intestinal barrier or immune function hint that dietary Mn supplementation is likely to be a promising approach to limit the loads of pathogens in broilers. Here, we provide evidence that Salmonella Typhimurium (S. Typhimurium, 4 × 108 CFUs) challenge-induced intestinal injury along with systemic Mn redistribution in broilers. Further examining of the effect of dietary Mn treatments (a basal diet plus additional 0, 40, or 100 mg Mn/kg for corresponding to Mn-deficient, control, or Mn-surfeit diet, respectively) on intestinal barrier and inflammation status of broilers infected with S. Typhimurium revealed that birds fed the control and Mn-surfeit diets exhibited improved intestinal tight junctions and microbiota composition. Even without Salmonella infection, dietary Mn deficiency alone increased intestinal permeability by impairing intestinal tight junctions. In addition, when fed the control and Mn-surfeit diets, birds showed decreased Salmonella burdens in cecal content and spleen, with a concomitant increase in inflammatory cytokine levels in spleen. Furthermore, the dietary Mn-supplementation-mediated induction of cytokine production was probably associated with the nuclear factor kappa-B (NF-κB)/hydrogen peroxide (H2O2) pathway, as judged by the enhanced manganese superoxide dismutase activity and the increased H2O2 level in mitochondria, together with the increased mRNA level of NF-κB in spleen. Ingenuity-pathway analysis indicated that acute-phase response pathways, T helper type 1 pathway, and dendritic cell maturation were significantly activated by the dietary Mn supplementation. Our data suggest that dietary Mn supplementation could enhance intestinal barrier and splenic inflammatory response to fight against Salmonella infection in broilers.}}, articleno = {{757}}, author = {{Zhang, Huaiyong and Pan, Shuqin and Zhang, Keying and Michiels, Joris and Zeng, Qiufeng and Ding, Xuemei and Wang, Jianping and Peng, Huanwei and Bai, Jie and Xuan, Yue and Su, Zhuowei and Bai, Shiping}}, issn = {{2076-2607}}, journal = {{MICROORGANISMS}}, keywords = {{Mn,intestine,Salmonella,cytokine,mitochondria,broiler,ENTERICA SEROVAR TYPHIMURIUM,NF-KAPPA-B,IMMUNE-RESPONSE,GROWTH-PERFORMANCE,GUT MICROBIOTA,MACROPHAGES,METABOLISM,CYTOKINE,ROS,SUPPLEMENTATION}}, language = {{eng}}, number = {{5}}, pages = {{20}}, title = {{Impact of dietary manganese on intestinal barrier and inflammatory response in broilers challenged with Salmonella Typhimurium}}, url = {{http://doi.org/10.3390/microorganisms8050757}}, volume = {{8}}, year = {{2020}}, }
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