Nuclear factor-kappa B activation pathway in intestinal epithelial cells is a major regulator of chemokine gene expression and neutrophil migration induced by Bacteroides fragilis enterotoxin

Clin Exp Immunol. 2002 Oct;130(1):59-66. doi: 10.1046/j.1365-2249.2002.01921.x.

Abstract

Although intestinal epithelial cells are known to up-regulate the expression of several chemokine genes in response to the stimulation with B. fragilis enterotoxin (BFT), there has been little understanding on the cellular mechanisms of BFT-induced mucosal inflammation. To test whether nuclear transcriptional factor-kappa B (NF-kappaB) is involved in the process, we stimulated intestinal epithelial cells with BFT, and evaluated the signalling NF-kappaB pathways. BFT increased signals of NF-kappaB in HT-29 and T84 epithelial cell lines as well as primary human colon epithelial cells. NF-kappaB molecules activated by BFT stimulation were composed of p65 and p50 heterodimers. In contrast, BFT decreased the signals of IkappaBalpha and IkappaB epsilon, as assessed by immunoblot. Super-repressors of IkappaBalpha, IkappaB kinase (IKK)beta, and NF-kappaB inducing kinase (NIK) inhibited an up-regulated transcription of downstream target gene (CXCL8) of NF-kappaB. Moreover, blocking the activation of NF-kappaB by MG-132 or antisense p50 oligonucleotide transfection resulted in down-regulated expression of chemokines such as CXCL1, CXCL8, and CCL2 in BFT-stimulated HT-29 cells. In addition, NF-kappaB inhibition suppressed the BFT-induced neutrophil transepithelial migration in T84 cells. These results indicate that NF-kappaB can be a central regulator of chemokine gene expression in BFT-stimulated intestinal epithelial cells and may be an important regulator of neutrophil migration.

MeSH terms

  • Adult
  • Bacterial Toxins / pharmacology*
  • Bacteroides fragilis / physiology*
  • Chemokines / biosynthesis*
  • Chemokines / genetics
  • Chemotaxis, Leukocyte / drug effects*
  • Colon / cytology
  • Colonic Neoplasms / pathology
  • DNA-Binding Proteins / metabolism
  • Electrophoretic Mobility Shift Assay
  • Enzyme-Linked Immunosorbent Assay
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Gene Expression Regulation / drug effects*
  • Genes, Reporter
  • Humans
  • I-kappa B Proteins*
  • Interleukin-8 / biosynthesis
  • Interleukin-8 / genetics
  • Intestinal Mucosa / drug effects*
  • Intestinal Mucosa / metabolism
  • Luciferases / biosynthesis
  • Luciferases / genetics
  • Metalloendopeptidases / pharmacology*
  • NF-KappaB Inhibitor alpha
  • NF-kappa B / physiology*
  • NF-kappaB-Inducing Kinase
  • Neutrophils / drug effects
  • Protein Serine-Threonine Kinases / physiology
  • Proto-Oncogene Proteins / metabolism
  • Repressor Proteins / physiology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Transcription, Genetic / drug effects*
  • Tumor Cells, Cultured / drug effects
  • Tumor Cells, Cultured / metabolism

Substances

  • Bacterial Toxins
  • Chemokines
  • DNA-Binding Proteins
  • I-kappa B Proteins
  • Interleukin-8
  • NF-kappa B
  • NFKBIA protein, human
  • NFKBIE protein, human
  • Proto-Oncogene Proteins
  • Repressor Proteins
  • NF-KappaB Inhibitor alpha
  • Luciferases
  • Protein Serine-Threonine Kinases
  • Bacteroides fragilis toxin
  • Metalloendopeptidases