Inflammatory bowel disease and mutations affecting the interleukin-10 receptor

N Engl J Med. 2009 Nov 19;361(21):2033-45. doi: 10.1056/NEJMoa0907206. Epub 2009 Nov 4.

Abstract

Background: The molecular cause of inflammatory bowel disease is largely unknown.

Methods: We performed genetic-linkage analysis and candidate-gene sequencing on samples from two unrelated consanguineous families with children who were affected by early-onset inflammatory bowel disease. We screened six additional patients with early-onset colitis for mutations in two candidate genes and carried out functional assays in patients' peripheral-blood mononuclear cells. We performed an allogeneic hematopoietic stem-cell transplantation in one patient.

Results: In four of nine patients with early-onset colitis, we identified three distinct homozygous mutations in genes IL10RA and IL10RB, encoding the IL10R1 and IL10R2 proteins, respectively, which form a heterotetramer to make up the interleukin-10 receptor. The mutations abrogate interleukin-10-induced signaling, as shown by deficient STAT3 (signal transducer and activator of transcription 3) phosphorylation on stimulation with interleukin-10. Consistent with this observation was the increased secretion of tumor necrosis factor alpha and other proinflammatory cytokines from peripheral-blood mononuclear cells from patients who were deficient in IL10R subunit proteins, suggesting that interleukin-10-dependent "negative feedback" regulation is disrupted in these cells. The allogeneic stem-cell transplantation performed in one patient was successful.

Conclusions: Mutations in genes encoding the IL10R subunit proteins were found in patients with early-onset enterocolitis, involving hyperinflammatory immune responses in the intestine. Allogeneic stem-cell transplantation resulted in disease remission in one patient.

Publication types

  • Case Reports
  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Age of Onset
  • Chromosomes, Human, Pair 11
  • Chromosomes, Human, Pair 21
  • Female
  • Genetic Linkage
  • Humans
  • Infant
  • Inflammatory Bowel Diseases / genetics*
  • Inflammatory Bowel Diseases / therapy
  • Interleukin-10 / metabolism
  • Interleukin-10 Receptor alpha Subunit / chemistry
  • Interleukin-10 Receptor alpha Subunit / genetics*
  • Interleukin-10 Receptor beta Subunit / chemistry
  • Interleukin-10 Receptor beta Subunit / genetics*
  • Male
  • Mutation, Missense*
  • Pedigree
  • Polymorphism, Single Nucleotide
  • Remission Induction
  • Sequence Analysis, DNA
  • Stem Cell Transplantation
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Interleukin-10 Receptor alpha Subunit
  • Interleukin-10 Receptor beta Subunit
  • Tumor Necrosis Factor-alpha
  • Interleukin-10