Immunomodulatory Effects of Lactiplantibacillus plantarum Strain RW1 During Salmonella Infection in Murine Intestinal Epithelial Cells and Dextran Sulfate Sodium-Induced Murine Colitis

Probiotics Antimicrob Proteins. 2024 Dec 3. doi: 10.1007/s12602-024-10411-3. Online ahead of print.

Abstract

Inflammatory diseases resulting from bacterial infections or inflammatory bowel disease pose significant threats to the health of both animals and humans. Although probiotics have emerged as a crucial preventive and adjunctive therapy for these conditions, the precise mechanisms through which probiotics regulate inflammatory diseases remain incompletely understood. In our previous study, animal-derived Lactiplantibacillus plantarum strain RW1 (L. plantarum RW1) with probiotic potential was isolated and characterized. In this study, the signaling pathway of L. plantarum RW1 inhibiting the inflammatory response of mouse intestinal epithelial cells caused by Salmonella infection was studied. Our results revealed that infection of Salmonella enterica subsp. enterica serovar Typhimurium strain ATCC14028 (S. Typhimurium ATCC14028) and Salmonella enterica subsp. enterica serovar Typhimurium strain SL1344 (S. Typhimurium SL1344) significantly increased NF-κB/p65 and TLR4 mRNA levels while decreasing IκB and TLR2 mRNA levels. Whereas L. plantarum RW1 treatment significantly reversed these changes. Western blotting confirmed these findings. Additionally, we explored the protective effects of L. plantarum RW1 in a murine colitis model induced by dextran sulfate sodium (DSS). Treatment with L. plantarum RW1 significantly increased both intestinal length and body weight compared to DSS-treated mice. 16S rRNA sequencing analysis demonstrated that L. plantarum RW1 restored the dysbiosis caused by DSS. Flow cytometry analyses further revealed that L. plantarum RW1 specifically increased regulatory T-cell proportions in Peyer's patches while reducing macrophage and neutrophil proportions, indicating the modulatory effects of L. plantarum RW1 on immune responses in gut-associated lymphatic tissue in the context of colitis. This study sheds light on the intricate interaction between probiotics and hosts, offering valuable insights into their potential application for treating inflammatory diseases in animals and humans.

Keywords: L. plantarum strain RW1; Salmonella; Cytokines; Immune regulation; Macrophages; Microbiota; T cells.

Grants and funding