Synergistic effect of interleukin-10-receptor variants in a case of early-onset ulcerative colitis

World J Gastroenterol. 2013 Dec 14;19(46):8659-70. doi: 10.3748/wjg.v19.i46.8659.

Abstract

Aim: To investigated the molecular cause of very early-onset ulcerative colitis (UC) in an 18-mo-old affected child.

Methods: We analysed the interleukin-10 (IL10) receptor genes at the DNA and RNA level in the proband and his relatives. Beta catenin and tumor necrosis factor-α (TNFα) receptors were analysed in the proteins extracted from peripheral blood cells of the proband, his relatives and familial adenomatous polyposis (FAP) and PTEN hamartoma tumor syndrome (PHTS) patients. Samples were also collected from the proband's inflamed colorectal mucosa and compared to healthy and tumour mucosa collected from a FAP patient and patients affected by sporadic colorectal cancer (CRC). Finally, we examined mesalazine and azathioprine effects on primary fibroblasts stabilised from UC and FAP patients.

Results: Our patient was a compound heterozygote for the IL10RB E47K polymorphism, inherited from his father, and for a novel point mutation within the IL10RA promoter (the -413G->T), inherited from his mother. Beta catenin and tumour necrosis factor α receptors-I (TNFRI) protein were both over-expressed in peripheral blood cells of the proband's relatives more than the proband. However, TNFRII was over-expressed only in the proband. Finally, both TNFα-receptors were shown to be under-expressed in the inflamed colon mucosa and colorectal cancer tissue compared to healthy colon mucosa. Consistent with this observation, mesalazine and azathioprine induced, in primary fibroblasts, IL10RB and TNFRII over-expression and TNFRI and TNFα under-expression. We suggest that β-catenin and TNFRI protein expression in peripheral blood cells could represent molecular markers of sub-clinical disease in apparently healthy relatives of patients with early-onset UC.

Conclusion: A synergistic effect of several variant alleles of the IL10 receptor genes, inherited in a Mendelian manner, is involved in UC onset in this young child.

Keywords: Beta catenin; Inflammatory bowel disease; Interleukin 10 receptors; Tumour necrosis factor α receptors; Ulcerative colitis.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenomatous Polyposis Coli / genetics
  • Adenomatous Polyposis Coli / immunology
  • Age of Onset
  • Anti-Infective Agents / pharmacology
  • Azathioprine / pharmacology
  • Biomarkers / blood
  • Cells, Cultured
  • Colitis, Ulcerative / drug therapy
  • Colitis, Ulcerative / genetics*
  • Colitis, Ulcerative / immunology
  • Colitis, Ulcerative / metabolism
  • Colon / drug effects
  • Colon / immunology
  • Colon / metabolism
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / immunology
  • Female
  • Fibroblasts / drug effects
  • Fibroblasts / immunology
  • Fibroblasts / metabolism
  • Gastrointestinal Agents / pharmacology
  • Genetic Predisposition to Disease
  • Hamartoma Syndrome, Multiple / genetics
  • Hamartoma Syndrome, Multiple / immunology
  • Heredity
  • Humans
  • Infant
  • Interleukin-10 Receptor alpha Subunit / genetics*
  • Interleukin-10 Receptor alpha Subunit / metabolism
  • Interleukin-10 Receptor beta Subunit / genetics*
  • Interleukin-10 Receptor beta Subunit / metabolism
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / metabolism
  • Male
  • Mesalamine / pharmacology
  • Pedigree
  • Phenotype
  • Point Mutation*
  • Polymorphism, Genetic*
  • Promoter Regions, Genetic
  • RNA, Messenger / metabolism
  • Receptors, Tumor Necrosis Factor, Type I / blood
  • Receptors, Tumor Necrosis Factor, Type II / blood
  • beta Catenin / blood

Substances

  • Anti-Infective Agents
  • Biomarkers
  • CTNNB1 protein, human
  • Gastrointestinal Agents
  • IL10RB protein, human
  • Interleukin-10 Receptor alpha Subunit
  • Interleukin-10 Receptor beta Subunit
  • RNA, Messenger
  • Receptors, Tumor Necrosis Factor, Type I
  • Receptors, Tumor Necrosis Factor, Type II
  • TNFRSF1A protein, human
  • TNFRSF1B protein, human
  • beta Catenin
  • Mesalamine
  • Azathioprine

Supplementary concepts

  • Pediatric ulcerative colitis