Inherited human IRAK-1 deficiency selectively impairs TLR signaling in fibroblasts

Proc Natl Acad Sci U S A. 2017 Jan 24;114(4):E514-E523. doi: 10.1073/pnas.1620139114. Epub 2017 Jan 9.

Abstract

Most members of the Toll-like receptor (TLR) and interleukin-1 receptor (IL-1R) families transduce signals via a canonical pathway involving the MyD88 adapter and the interleukin-1 receptor-associated kinase (IRAK) complex. This complex contains four molecules, including at least two (IRAK-1 and IRAK-4) active kinases. In mice and humans, deficiencies of IRAK-4 or MyD88 abolish most TLR (except for TLR3 and some TLR4) and IL-1R signaling in both leukocytes and fibroblasts. TLR and IL-1R responses are weak but not abolished in mice lacking IRAK-1, whereas the role of IRAK-1 in humans remains unclear. We describe here a boy with X-linked MECP2 deficiency-related syndrome due to a large de novo Xq28 chromosomal deletion encompassing both MECP2 and IRAK1 Like many boys with MECP2 null mutations, this child died very early, at the age of 7 mo. Unlike most IRAK-4- or MyD88-deficient patients, he did not suffer from invasive bacterial diseases during his short life. The IRAK-1 protein was completely absent from the patient's fibroblasts, which responded very poorly to all TLR2/6 (PAM2CSK4, LTA, FSL-1), TLR1/2 (PAM3CSK4), and TLR4 (LPS, MPLA) agonists tested but had almost unimpaired responses to IL-1β. By contrast, the patient's peripheral blood mononuclear cells responded normally to all TLR1/2, TLR2/6, TLR4, TLR7, and TLR8 (R848) agonists tested, and to IL-1β. The death of this child precluded long-term evaluations of the clinical consequences of inherited IRAK-1 deficiency. However, these findings suggest that human IRAK-1 is essential downstream from TLRs but not IL-1Rs in fibroblasts, whereas it plays a redundant role downstream from both TLRs and IL-1Rs in leukocytes.

Keywords: IRAK-1; IRAK-4; Toll-like receptor; interleukin-1 receptor; primary immunodeficiency.

Publication types

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

MeSH terms

  • Chromosome Deletion
  • Chromosomes, Human, X / genetics
  • Fibroblasts / metabolism*
  • Humans
  • Infant
  • Interleukin-1 Receptor-Associated Kinases / deficiency*
  • Interleukin-1 Receptor-Associated Kinases / genetics
  • Leukocytes / metabolism
  • Male
  • Methyl-CpG-Binding Protein 2 / genetics
  • Receptors, Interleukin-1 / metabolism
  • Signal Transduction
  • Toll-Like Receptors / genetics
  • Toll-Like Receptors / metabolism*

Substances

  • MECP2 protein, human
  • Methyl-CpG-Binding Protein 2
  • Receptors, Interleukin-1
  • Toll-Like Receptors
  • IRAK1 protein, human
  • Interleukin-1 Receptor-Associated Kinases