Probiotics can generate FoxP3 T-cell responses in the small intestine and simultaneously inducing CD4 and CD8 T cell activation in the large intestine

Maaike J Smelt, Bart J de Haan, Peter A Bron, Iris van Swam, Marjolein Meijerink, Jerry M Wells, Marijke M Faas, Paul de Vos

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Most studies on probiotics aim to restore intestinal homeostasis to reduce immune-pathology in disease. Of equal importance are studies on how probiotics might prevent or delay disease in healthy individuals. However, knowledge on mechanisms of probiotic actions in healthy individuals is scarce. To gain more insight in how different bacterial strains may modulate the healthy intestinal immune system, we investigated the effect of the food derived bacterial strains L. plantarum WCFS1, L. salivarius UCC118, and L. lactis MG1363, on the intestinal regulatory immune phenotype in healthy mice. All three bacterial strains induced an upregulation of activity and numbers of CD11c+ MHCII+ DCs in the immune-sampling Peyer's Patches. Only L. salivarius UCC118 skewed towards an immune regulatory phenotype in the small intestinal lamina propria (SILP). The effects were different in the large intestine lamina propria. L. salivarius UCC118 induced activation in both CD4 and CD8 positive T-cells while L. plantarum WCFS1 induced a more regulatory phenotype. Moreover, L. plantarum WCFS1 decreased the Th1/Th2 ratio in the SILP. Also L. lactis MG1363 had immunomodulatory effects. L. lactis MG1363 decreased the expression of the GATA-3 and T-bet in the SILP. As our data show that contradictory effects may occur in different parts of the gut, it is recommended to study effects of probiotic in different sites in the intestine. Our strain-specific results suggest that unspecified application of probiotics may not be very effective. Our data also indicate that selection of specific probiotic strain activities on the basis of responses in healthy mice may be a promising strategy to specifically stimulate or suppress immunity in specific parts of the intestine. © 2013 Smelt et al.
Original languageEnglish
Pages (from-to)e68952
JournalPLOS one
Volume8
Issue number7
DOIs
Publication statusPublished - 4 Jul 2013
Externally publishedYes

Fingerprint

T-cells
Large Intestine
Probiotics
large intestine
probiotics
Small Intestine
small intestine
T-lymphocytes
Chemical activation
laminae (animals)
T-Lymphocytes
Mucous Membrane
Phenotype
phenotype
Intestines
intestines
Peyer's Patches
Peyer's patches
Immune system
mice

Keywords

  • Animals
  • CD11c Antigen/genetics
  • CD4-Positive T-Lymphocytes/cytology
  • CD8-Positive T-Lymphocytes/cytology
  • Cell Count
  • Dendritic Cells/cytology
  • Forkhead Transcription Factors/genetics
  • GATA3 Transcription Factor/genetics
  • Gene Expression Regulation/drug effects
  • Humans
  • Intestinal Mucosa/drug effects
  • Intestine, Large/drug effects
  • Intestine, Small/drug effects
  • Lactobacillus/physiology
  • Lymphocyte Activation
  • Male
  • Mice
  • Peyer's Patches/drug effects
  • Probiotics/pharmacology
  • Species Specificity
  • T-Box Domain Proteins/genetics
  • Th1-Th2 Balance/drug effects

Cite this

Smelt, Maaike J ; de Haan, Bart J ; Bron, Peter A ; van Swam, Iris ; Meijerink, Marjolein ; Wells, Jerry M ; Faas, Marijke M ; de Vos, Paul. / Probiotics can generate FoxP3 T-cell responses in the small intestine and simultaneously inducing CD4 and CD8 T cell activation in the large intestine. In: PLOS one. 2013 ; Vol. 8, No. 7. pp. e68952.
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abstract = "Most studies on probiotics aim to restore intestinal homeostasis to reduce immune-pathology in disease. Of equal importance are studies on how probiotics might prevent or delay disease in healthy individuals. However, knowledge on mechanisms of probiotic actions in healthy individuals is scarce. To gain more insight in how different bacterial strains may modulate the healthy intestinal immune system, we investigated the effect of the food derived bacterial strains L. plantarum WCFS1, L. salivarius UCC118, and L. lactis MG1363, on the intestinal regulatory immune phenotype in healthy mice. All three bacterial strains induced an upregulation of activity and numbers of CD11c+ MHCII+ DCs in the immune-sampling Peyer's Patches. Only L. salivarius UCC118 skewed towards an immune regulatory phenotype in the small intestinal lamina propria (SILP). The effects were different in the large intestine lamina propria. L. salivarius UCC118 induced activation in both CD4 and CD8 positive T-cells while L. plantarum WCFS1 induced a more regulatory phenotype. Moreover, L. plantarum WCFS1 decreased the Th1/Th2 ratio in the SILP. Also L. lactis MG1363 had immunomodulatory effects. L. lactis MG1363 decreased the expression of the GATA-3 and T-bet in the SILP. As our data show that contradictory effects may occur in different parts of the gut, it is recommended to study effects of probiotic in different sites in the intestine. Our strain-specific results suggest that unspecified application of probiotics may not be very effective. Our data also indicate that selection of specific probiotic strain activities on the basis of responses in healthy mice may be a promising strategy to specifically stimulate or suppress immunity in specific parts of the intestine. {\circledC} 2013 Smelt et al.",
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Probiotics can generate FoxP3 T-cell responses in the small intestine and simultaneously inducing CD4 and CD8 T cell activation in the large intestine. / Smelt, Maaike J; de Haan, Bart J; Bron, Peter A; van Swam, Iris; Meijerink, Marjolein; Wells, Jerry M; Faas, Marijke M; de Vos, Paul.

In: PLOS one, Vol. 8, No. 7, 04.07.2013, p. e68952.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - de Haan, Bart J

AU - Bron, Peter A

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AU - Meijerink, Marjolein

AU - Wells, Jerry M

AU - Faas, Marijke M

AU - de Vos, Paul

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KW - Mice

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KW - Probiotics/pharmacology

KW - Species Specificity

KW - T-Box Domain Proteins/genetics

KW - Th1-Th2 Balance/drug effects

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