Abstract
BackgroundThere is limited knowledge on the extent and dynamics of the mucosal response to commensal and probiotic species in the human intestinal lumen. This study aimed to identify the acute, time-dependent responses of intestinal mucosa to commensal Lactobacillus plantarum WCFS1 in vivo in two placebo-controlled human intervention studies in healthy volunteers. Transcriptional changes in duodenal mucosa upon continuous intraduodenal infusion of L. plantarum WCFS1 for one- and six h, respectively, were studied using oro- and nasogastric intubations with dedicated orogastric catheters and tissue sampling by standard flexible gastroduodenoscopy.ResultsOne- and six-h exposure of small intestinal mucosa to L. plantarum WCFS1 induced differential expression of 669 and 424 gene reporters, respectively. While short-term exposure to L. plantarum WCFS1 inhibited fatty acid metabolism and cell cycle progression, cells switched to a more proliferative phase after prolonged exposure with an overall expression profile characterized by upregulation of genes involved in lipid metabolism, cellular growth and development. Cell death and immune responses were triggered, but cell death-executing genes or inflammatory signals were not expressed. Proteome analysis showed differential expression of several proteins. Only the microsomal protein 'microsomal triglyceride transfer protein' was regulated on both the transcriptional and the protein level in all subjects.ConclusionOverall, this study showed that intestinal exposure to L. plantarum WCFS1 induced consistent, time-dependent transcriptional responses in healthy intestinal mucosa. This extensive exploration of the human response to L. plantarum WCFS1 could eventually provide molecular support for specific or probiotic activity of this strain or species, and exemplifies the strength of the applied technology to identify the potential bio-activity of microbes in the human intestine.
Highlights
There is limited knowledge on the extent and dynamics of the mucosal response to commensal and probiotic species in the human intestinal lumen
Lactobacillus plantarum on symptoms in patients suffering from irritable bowel syndrome (IBS) [4], in inflammatory bowel disease (IBD) patients [5], and on the intestinal barrier function in stressed conditions [6]
DiCaro et al investigated the effects of L. rhamnosus GG on transcriptional responses of small intestinal mucosa in oesophagitis patients [7], delivering a myriad of information about the impact of a probiotic supplementation regimen on the human mucosal response to probiotics in a limited number (n = 3) of subjects suffering from an underlying medical condition
Summary
There is limited knowledge on the extent and dynamics of the mucosal response to commensal and probiotic species in the human intestinal lumen. This study aimed to identify the acute, time-dependent responses of intestinal mucosa to commensal Lactobacillus plantarum. Many lactic acid bacteria (LAB) have a long history of use in the preservation of food ingredients [1]. Various LAB species, given as food supplements, exert beneficial bioactivity in the intestine [2,3]. DiCaro et al investigated the effects of L. rhamnosus GG on transcriptional responses of small intestinal mucosa in oesophagitis patients [7], delivering a myriad of information about the impact of a probiotic supplementation regimen on the human mucosal response to probiotics in a limited number (n = 3) of subjects suffering from an underlying medical condition
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