Antibiotic-induced dysbiosis alters host-bacterial interactions and leads to colonic sensory and motor changes in mice

Gut Microbes. 2015;6(1):10-23. doi: 10.4161/19490976.2014.990790. Epub 2015 Jan 20.

Abstract

Alterations in the composition of the commensal microbiota (dysbiosis) seem to be a pathogenic component of functional gastrointestinal disorders, mainly irritable bowel syndrome (IBS), and might participate in the secretomotor and sensory alterations observed in these patients.We determined if a state antibiotics-induced intestinal dysbiosis is able to modify colonic pain-related and motor responses and characterized the neuro-immune mechanisms implicated in mice. A 2-week antibiotics treatment induced a colonic dysbiosis (increments in Bacteroides spp, Clostridium coccoides and Lactobacillus spp and reduction in Bifidobacterium spp). Bacterial adherence was not affected. Dysbiosis was associated with increased levels of secretory-IgA, up-regulation of the antimicrobial lectin RegIIIγ, and toll-like receptors (TLR) 4 and 7 and down-regulation of the antimicrobial-peptide Resistin-Like Molecule-β and TLR5. Dysbiotic mice showed less goblet cells, without changes in the thickness of the mucus layer. Neither macroscopical nor microscopical signs of inflammation were observed. In dysbiotic mice, expression of the cannabinoid receptor 2 was up-regulated, while the cannabinoid 1 and the mu-opioid receptors were down-regulated. In antibiotic-treated mice, visceral pain-related responses elicited by intraperitoneal acetic acid or intracolonic capsaicin were significantly attenuated. Colonic contractility was enhanced during dysbiosis. Intestinal dysbiosis induce changes in the innate intestinal immune system and modulate the expression of pain-related sensory systems, an effect associated with a reduction in visceral pain-related responses. Commensal microbiota modulates gut neuro-immune sensory systems, leading to functional changes, at least as it relates to viscerosensitivity. Similar mechanisms might explain the beneficial effects of antibiotics or certain probiotics in the treatment of IBS.

Keywords: AMP, antimicrobial peptide; CB1/2, cannabinoid receptor type 1 or 2; FGD, functional gastrointestinal disorder; FISH, fluorescent in situ hybridization; GCM, gut commensal microbiota; GI, gastrointestinal; IBS, irritable bowel syndrome; MOR, mu-opioid receptor; NGF, nerve growth factor; PPR, pattern recognition receptor; RELMβ, resistin-like molecule-β; RT-qPCR, reverse transcription quantitative polymerase chain reaction; Reg3γ, regenerating islet-derived protein 3 gamma; SFB, segmented filamentous bacteria; TLR, toll-like receptor; TPH 1/2, tryptophan hydroxylase isoforms 1 or 2; TRPV1/3, transient receptor potential vanilloid types 1 or 3; cannabinoid receptors; colonic motility; gut commensal microbiota; iNOS, inducible nitric oxide synthase; innate immune system; intestinal dysbiosis; opioid receptors; sIgA, secretory IgA; visceral sensitivity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / administration & dosage
  • Anti-Bacterial Agents / adverse effects*
  • Colon / drug effects
  • Colon / microbiology*
  • Colon / pathology
  • Colon / physiology*
  • Dysbiosis / chemically induced*
  • Female
  • Gastrointestinal Microbiome / drug effects*
  • Mice

Substances

  • Anti-Bacterial Agents