Lactobacillus reuteri DSM 17938 differentially modulates effector memory T cells and Foxp3+ regulatory T cells in a mouse model of necrotizing enterocolitis

Am J Physiol Gastrointest Liver Physiol. 2014 Jul 15;307(2):G177-86. doi: 10.1152/ajpgi.00038.2014. Epub 2014 May 22.

Abstract

Necrotizing enterocolitis (NEC) is an inflammatory disease with evidence of increased production of proinflammatory cytokines in the intestinal mucosa. Lactobacillus reuteri DSM 17938 (LR17938) has been shown to have anti-inflammatory activities in an experimental model of NEC. Activated effector lymphocyte recruitment to sites of inflammation requires the sequential engagement of adhesion molecules such as CD44. The phenotype of CD44(+)CD45RB(lo) separates T effector/memory (Tem) cells from naive (CD44(-)CD45RB(hi)) cells. It is unknown whether these Tem cells participate in the inflammation associated with NEC and can be altered by LR17938. NEC was induced in 8- to 10-day-old C57BL/6J mice by gavage feeding with formula and exposure to hypoxia and cold stress for 4 days. Survival curves and histological scores were analyzed. Lymphocytes isolated from mesenteric lymph nodes and ileum were labeled for CD4, CD44, CD45RB, intracellular Foxp3, and Helios and subsequently analyzed by flow cytometry. LR17938 decreased mortality and the incidence and severity of NEC. The percentage of Tem cells in the ileum and mesenteric lymph nodes was increased in NEC but decreased by LR17938. Conversely, the percentage of CD4(+)Foxp3(+) regulatory T (Treg) cells in the intestine decreased during NEC and was restored to normal by LR17938. The majority of the Treg cells preserved by LR17938 were Helios+ subsets, possibly of thymic origin. In conclusion, LR17938 may represent a useful treatment to prevent NEC. The mechanism of protection by LR17938 involves modulation of the balance between Tem and Treg cells. These T cell subsets might be potential biomarkers and therapeutic targets during intestinal inflammation.

Keywords: inflammation; intestine; necrotizing enterocolitis; probiotics; regulatory T cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Cytokines / metabolism
  • Disease Models, Animal
  • Enterocolitis, Necrotizing / immunology
  • Enterocolitis, Necrotizing / metabolism
  • Enterocolitis, Necrotizing / microbiology
  • Enterocolitis, Necrotizing / pathology
  • Enterocolitis, Necrotizing / prevention & control*
  • Forkhead Transcription Factors / metabolism*
  • Ileum / immunology
  • Ileum / metabolism
  • Ileum / microbiology*
  • Ileum / pathology
  • Immunity, Mucosal
  • Immunologic Memory*
  • Inflammation Mediators / metabolism
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / microbiology
  • Limosilactobacillus reuteri / physiology*
  • Lymph Nodes / immunology
  • Lymph Nodes / metabolism
  • Lymph Nodes / microbiology*
  • Mice
  • Mice, Inbred C57BL
  • Probiotics*
  • Severity of Illness Index
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism
  • T-Lymphocytes, Regulatory / microbiology*
  • Time Factors

Substances

  • Cytokines
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Inflammation Mediators