Home LiteratureArticle Details
PMID: 16011513 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Innate mechanisms for Bifidobacterium lactis to activate transient pro-inflammatory host responses in intestinal epithelial cells after the colonization of germ-free rats.

Immunology ·Vol. 115 ·No. 4 ·2005-08-00 ·Pages 441-50

Ruiz PA, Hoffmann M, Szcesny S, Blaut M, Haller D

Abstract

Bifidobacteria comprise a dominant microbial population group in the human intestinal tract with purported beneficial health effects on the host. In this study, we characterized the molecular mechanisms for the initial interaction of probiotic Bifidobacterium lactis strain BB12 with native and intestinal epithelial cell (IEC) lines. We showed that B. lactis-monoassociated Fisher F344 rats transiently induce phosphorylation/activation of the NF-kappaB transcriptionally active subunit RelA and the mitogen-activated protein kinase (MAPK) p38 in native IEC at day 5 after initial bacterial colonization. In addition, Interleukin 6 (IL-6) gene expression was significantly increased at day 5, demonstrating the physiological relevance of transient transcription factor activation in IEC. In contrast, Bacteroides vulgatus-monoassociated Fisher rats revealed RelA but not p38 MAPK phosphorylation and failed to trigger significant IL-6 gene expression in native IEC. Moreover, we demonstrated that B. lactis triggers NF-kappaB RelA and p38 MAPK phosphorylation in IEC lines. Adenoviral delivery of mutant IKK-beta (Ad5dnIKKbeta) and inhibition of the p38 MAPK pathway through the pharmacological inhibitor SB203580 significantly blocked B. lactis-induced IL-6 gene expression in IEC, suggesting that B. lactis triggers NF-kappaB and MAPK signaling to induce gene expression in the intestinal epithelium. Regarding the mechanisms of bacteria epithelial cell cross-talk, B. lactis-induced IL-6 gene expression was completely inhibited in TLR2 deficient mouse embryogenic fibroblasts (MEF TLR2-/-) as well as TLR2DeltaTIR transfected Mode-K cells. In conclusion, we demonstrated that probiotic bacteria transiently trigger innate signal transduction and pro-inflammatory gene expression in the intestinal epithelium at early stages of bacterial colonization.

MeSH Terms
Animals Bifidobacterium/immunology Cell Line Cysteine Endopeptidases Enzyme Inhibitors/immunology Epithelial Cells/immunology Gene Expression/immunology Imidazoles/immunology Inflammation/immunology Interleukin-6/genetics,immunology Intestines/immunology Intracellular Signaling Peptides and Proteins Membrane Glycoproteins/immunology NF-kappa B/immunology Nuclear Proteins Phosphorylation Probiotics Proteins/immunology Pyridines/immunology Rats Rats, Inbred F344 Receptors, Cell Surface/immunology Signal Transduction/immunology Toll-Like Receptor 2 Toll-Like Receptors Transcription Factor RelA Tumor Necrosis Factor alpha-Induced Protein 3 p38 Mitogen-Activated Protein Kinases/immunology
Chemicals
Enzyme Inhibitors Imidazoles Interleukin-6 Intracellular Signaling Peptides and Proteins Membrane Glycoproteins NF-kappa B Nuclear Proteins Proteins Pyridines Receptors, Cell Surface Tlr2 protein, rat Toll-Like Receptor 2 Toll-Like Receptors Transcription Factor RelA p38 Mitogen-Activated Protein Kinases Tumor Necrosis Factor alpha-Induced Protein 3 Cysteine Endopeptidases Tnfaip3 protein, mouse SB 203580
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Ruiz Pedro A
Centre for Nutrition and Food Research, Immunobiology of Nutrition, Technical University of Munich, Freising-Weihenstephan, Germany.
Hoffmann Micha
Szcesny Silke
Blaut Michael
Haller Dirk
References (47)
47 references, click to expand
  1. Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019.
    Am J Clin Nutr. 2001 Dec;74(6):833-9 PMID: 11722966
  2. IL-10 gene-deficient mice lack TGF-beta/Smad signaling and fail to inhibit proinflammatory gene expression in intestinal epithelial cells after the colonization with colitogenic Enterococcus faecalis.
    J Immunol. 2005 Mar 1;174(5):2990-9 PMID: 15728512
  3. Intestinal flora during the first months of life: new perspectives.
    Br J Nutr. 2002 Sep;88 Suppl 1:S11-8 PMID: 12215177
  4. IKK beta and phosphatidylinositol 3-kinase/Akt participate in non-pathogenic Gram-negative enteric bacteria-induced RelA phosphorylation and NF-kappa B activation in both primary and intestinal epithelial cell lines.
    J Biol Chem. 2002 Oct 11;277(41):38168-78 PMID: 12140289
  5. A new mathematical model for relative quantification in real-time RT-PCR.
    Nucleic Acids Res. 2001 May 1;29(9):e45 PMID: 11328886
  6. Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells.
    J Biol Chem. 2002 Dec 27;277(52):50959-65 PMID: 12393915
  7. The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense.
    Sci STKE. 2003 Feb 25;2003(171):re3 PMID: 12606705
  8. Toll-like receptors.
    Annu Rev Immunol. 2003;21:335-76 PMID: 12524386
  9. The two faces of IKK and NF-kappaB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion.
    Nat Med. 2003 May;9(5):575-81 PMID: 12692538
  10. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial.
    Gastroenterology. 2003 May;124(5):1202-9 PMID: 12730861
  11. Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance.
    Gut. 2003 Jul;52(7):975-80 PMID: 12801954
  12. Transforming growth factor-beta 1 inhibits non-pathogenic Gram negative bacteria-induced NF-kappa B recruitment to the interleukin-6 gene promoter in intestinal epithelial cells through modulation of histone acetylation.
    J Biol Chem. 2003 Jun 27;278(26):23851-60 PMID: 12672795
  13. Toll-like receptor 4-mediated signaling by epithelial surfaces: necessity or threat?
    Microbes Infect. 2003 Sep;5(11):951-9 PMID: 12941387
  14. Effect of probiotic bacteria on induction and maintenance of oral tolerance to beta-lactoglobulin in gnotobiotic mice.
    Clin Diagn Lab Immunol. 2003 Sep;10(5):787-92 PMID: 12965905
  15. Death receptor activation complexes: it takes two to activate TNF receptor 1.
    Cell Cycle. 2003 Nov-Dec;2(6):550-2 PMID: 14504472
  16. Potential uses of probiotics in clinical practice.
    Clin Microbiol Rev. 2003 Oct;16(4):658-72 PMID: 14557292
  17. Interaction between resident luminal bacteria and the host: can a healthy relationship turn sour?
    J Pediatr Gastroenterol Nutr. 2004 Feb;38(2):123-36 PMID: 14734871
  18. Modulation of the effect of dextran sulfate sodium-induced acute colitis by the administration of different probiotic strains of Lactobacillus and Bifidobacterium.
    Dig Dis Sci. 2004 Feb;49(2):320-7 PMID: 15104378
  19. Effect of Bifidobacterium longum ingestion on experimental salmonellosis in mice.
    J Appl Microbiol. 2004;97(1):29-37 PMID: 15186439
  20. Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C.
    Gastroenterology. 2004 Jul;127(1):224-38 PMID: 15236188
  21. Genetic heterogeneity and functional properties of intestinal bifidobacteria.
    J Appl Microbiol. 2004;97(3):459-70 PMID: 15281925
  22. 15-deoxy-delta12,14-prostaglandin J2-mediated ERK signaling inhibits gram-negative bacteria-induced RelA phosphorylation and interleukin-6 gene expression in intestinal epithelial cells through modulation of protein phosphatase 2A activity.
    J Biol Chem. 2004 Aug 20;279(34):36103-11 PMID: 15199053
  23. Effects of ingesting Lactobacillus- and Bifidobacterium-containing yogurt in subjects with colonized Helicobacter pylori.
    Am J Clin Nutr. 2004 Sep;80(3):737-41 PMID: 15321816
  24. The gastrointestinal epithelium and its autochthonous bacterial flora.
    J Exp Med. 1968 Jan 1;127(1):67-76 PMID: 4169441
  25. Human fecal flora: the normal flora of 20 Japanese-Hawaiians.
    Appl Microbiol. 1974 May;27(5):961-79 PMID: 4598229
  26. Expression of a nonpolymorphic MHC class I-like molecule, CD1D, by human intestinal epithelial cells.
    J Immunol. 1991 Oct 15;147(8):2518-24 PMID: 1717564
  27. Intestinal flora and aging.
    Nutr Rev. 1992 Dec;50(12):438-46 PMID: 1488186
  28. Immortalization of mouse intestinal epithelial cells by the SV40-large T gene. Phenotypic and immune characterization of the MODE-K cell line.
    J Immunol Methods. 1993 Nov 5;166(1):63-73 PMID: 7693823
  29. Commensal enteric bacteria engender a self-limiting humoral mucosal immune response while permanently colonizing the gut.
    Infect Immun. 1995 Oct;63(10):3904-13 PMID: 7558298
  30. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats.
    J Clin Invest. 1996 Aug 15;98(4):945-53 PMID: 8770866
  31. The indigenous gastrointestinal microflora.
    Trends Microbiol. 1996 Nov;4(11):430-5 PMID: 8950812
  32. Epithelial cells as sensors for microbial infection.
    J Clin Invest. 1997 Jul 1;100(1):6-10 PMID: 9202050
  33. Intestinal epithelial cells use two distinct pathways for HLA class II antigen processing.
    J Clin Invest. 1997 Jul 1;100(1):204-15 PMID: 9202073
  34. Epithelial cell growth and differentiation. III. Promoting diversity in the intestine: conversations between the microflora, epithelium, and diffuse GALT.
    Am J Physiol. 1997 Sep;273(3 Pt 1):G565-70 PMID: 9316460
  35. Lipopolysaccharide induces the antiapoptotic molecules, A1 and A20, in microvascular endothelial cells.
    Blood. 1998 Oct 15;92(8):2759-65 PMID: 9763560
  36. Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1157-70 PMID: 9841668
  37. Influences of microbiota on intestinal immune system development.
    Am J Clin Nutr. 1999 May;69(5):1046S-1051S PMID: 10232647
  38. Activators and target genes of Rel/NF-kappaB transcription factors.
    Oncogene. 1999 Nov 22;18(49):6853-66 PMID: 10602461
  39. The I kappa B/NF-kappa B system: a key determinant of mucosalinflammation and protection.
    Am J Physiol Cell Physiol. 2000 Mar;278(3):C451-62 PMID: 10712233
  40. Lactobacilli and Streptococci activate NF-kappa B and STAT signaling pathways in human macrophages.
    J Immunol. 2000 Apr 1;164(7):3733-40 PMID: 10725732
  41. Recruitment of the IKK signalosome to the p55 TNF receptor: RIP and A20 bind to NEMO (IKKgamma) upon receptor stimulation.
    Immunity. 2000 Mar;12(3):301-11 PMID: 10755617
  42. Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trial.
    Gastroenterology. 2000 Aug;119(2):305-9 PMID: 10930365
  43. A20 and A20-binding proteins as cellular inhibitors of nuclear factor-kappa B-dependent gene expression and apoptosis.
    Biochem Pharmacol. 2000 Oct 15;60(8):1143-51 PMID: 11007952
  44. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice.
    Science. 2000 Sep 29;289(5488):2350-4 PMID: 11009421
  45. Toll-like receptor-mediated NF-kappaB activation: a phylogenetically conserved paradigm in innate immunity.
    J Clin Invest. 2001 Jan;107(1):13-9 PMID: 11134172
  46. Probiotic bacteria enhance murine and human intestinal epithelial barrier function.
    Gastroenterology. 2001 Sep;121(3):580-91 PMID: 11522742
  47. Intestinal microflora of human infants and current trends for its nutritional modulation.
    Br J Nutr. 2002 May;87(5):405-20 PMID: 12010580
Article Info
Journal
Immunology
Abbr.
Immunology
ISSN
0019-2805
Published
2005-08-00
Pages
441-50
Language
English
Region
England
NLM ID
0374672
PMCID
PMC1782184
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]