Probiotic Lactobacillus plantarum Promotes Intestinal Barrier Function by Strengthening the Epithelium and Modulating Gut Microbiota

Abstract

Weaning disturbs the intestinal barrier function and increases the risk of infection in piglets. Probiotics exert beneficial health effects, mainly by reinforcing the intestinal epithelium and modulating the gut microbiota. However, the mechanisms of action, and especially, the specific regulatory effects of modulated microbiota by probiotics on the intestinal epithelium have not yet been elucidated. The present study aimed to decipher the protective effects of the probiotic Lactobacillus plantarum strain ZLP001 on the intestinal epithelium and microbiota as well as the effects of modulated microbiota on epithelial function. Paracellular permeability was measured with fluorescein isothiocyanate-dextran (FD-4). Gene and protein expression levels of tight junction (TJ) proteins, proinflammatory cytokines, and host defense peptides were determined by RT-qPCR, ELISA, and western blot analysis. Short-chain fatty acid (SCFA) concentrations were measured by ion chromatography. Fecal microbiota composition was assessed by high-throughput sequencing. The results showed that pretreatment with 108 colony forming units (CFU) mL−1 of L. plantarum ZLP001 significantly counteracted the increase in gut permeability to FD-4 induced by 106 CFU mL−1 enterotoxigenic Escherichia coli (ETEC). In addition, L. plantarum ZLP001 pretreatment alleviated the reduction in TJ proteins (claudin-1, occludin, and ZO-1) and downregulated proinflammatory cytokines IL-6 and IL-8, and TNFα expression and secretion caused by ETEC. L. plantarum ZLP001 also significantly increased the expression of the host defense peptides pBD2 and PG1-5 and pBD2 secretion relative to the control. Furthermore, L. plantarum ZLP001 treatment affected piglet fecal microbiota. The abundance of butyrate-producing bacteria Anaerotruncus and Faecalibacterium was significantly increased in L. plantarum ZLP001-treated piglets, and showed a positive correlation with fecal butyric and acetic acid concentrations. In addition, the cell density of Clostridium sensu stricto 1, which may cause epithelial inflammation, was decreased after L. plantarum ZLP001 administration, while the beneficial Lactobacillus was significantly increased. Our findings suggest that L. plantarum ZLP001 fortifies the intestinal barrier by strengthening epithelial defense functions and modulating gut microbiota.

Dietary Postbiotic Lactobacillus plantarum Improves Serum and Ruminal Antioxidant Activity and Upregulates Hepatic Antioxidant Enzymes and Ruminal Barrier Function in Post-Weaning Lambs

“…Studies on L. plantarum as feed additives in another species showed improvement of gut barrier function accompanied by a better gut environment. Post-weaning piglets received L. plantarum in the diet had improvement in the regulation of tight junction proteins (claudin-1, occludin and zona-occluden-1 (ZO-1)) concurrently with the strengthening of epithelium and modulating gut microbiota [55]. In suckling piglets, L. plantarum administration in the diet upregulated the jejunal OCLD, ileal ZO-1 and jejunal and the ileum of porcine B-defensin with an improvement of intestinal morphology and increment of relative abundance of phyla Firmicutes and Actinobacteria and genus Lactobacillus [56].…”

Intestinal Flora and Disease Mutually Shape the Regional Immune System in the Intestinal Tract

“…Perhaps these changes in miRNA levels also play a role in the alleviation of diseases (112). As another example, Lactobacillus plantarum ZLP001 impacts the composition of the intestinal microflora, and increases the abundance of butyrate-producing bacteria such as Anaerotruncus and Faecalibacterium in the 30-day trial (113). Meanwhile, in terms of immune regulation, the strain downregulates production of proinflammatory cytokines, including IL-6, IL-8, and TNF-α, and increases levels of host defense peptides pBD2 and PG1-5.…”

“…Meanwhile, in terms of immune regulation, the strain downregulates production of proinflammatory cytokines, including IL-6, IL-8, and TNF-α, and increases levels of host defense peptides pBD2 and PG1-5. Ultimately, L. plantarum ZLP001 strengthens the intestinal barrier by improving the epithelial defense function and regulating the intestinal microbiota, which reduces the risk of infection (113).…”

Effects of Lactobacillus plantarum on the intestinal morphology, intestinal barrier function and microbiota composition of suckling piglets

“…Lactobacillus plantarum is considered an excellent probiotic in the gastrointestinal tracts of humans and animals and performs important probiotic actions, such as inhibiting Escherichia coli ‐induced intestinal permeability, reducing the incidence of Clostridium difficile , alleviating oxidative damage to the liver, improving growth performance and increasing intestinal immunity and anti‐inflammatory properties (de Vries, Vaughan, Kleerebezem, & de Vos, ; Dudzicz, Kujawa‐Szewieczek, Kwiecien, Wiecek, & Adamczak, ; Fak, Ahrne, Molin, Jeppsson, & Westrom, ; Herías et al, ; Khanian, Karimi‐Torshizi, & Allameh, ; Malik et al, ; Wullt, Johansson Hagslatt, Odenholt, & Berggren, ). Researches have shown that oral administration of L. plantarum can improve the immune responses and enhance the intestinal barrier function of weaning piglets (Wang, Ji, et al, ; Yang, Jiang, Zheng, Wang, & Yang, ). Diet with L. plantarum ‐fermented wheat also can improve the apparent total tract digestibility of nutrients and energy, nitrogen retention, and energy content of weaned piglets (Koo, Bustamante‐García, & Nyachoti, ).…”