Inflammation and autoimmunity caused by a SHP1 mutation depend on IL-1, MyD88, and a microbial trigger

Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15028-33. doi: 10.1073/pnas.0806619105. Epub 2008 Sep 19.

Abstract

A recessive phenotype called spin (spontaneous inflammation) was induced by N-ethyl-N-nitrosourea (ENU) mutagenesis in C57BL/6J mice. Homozygotes display chronic inflammatory lesions affecting the feet, salivary glands and lungs, and antichromatin antibodies. They are immunocompetent and show enhanced resistance to infection by Listeria monocytogenes. TLR-induced TNF and IL-1 production are normal in macrophages derived from spin mice. The autoinflammatory phenotype of spin mice is fully suppressed by compound homozygosity for Myd88(poc), Irak4(otiose), and Il1r1-null mutations, but not Ticam1(Lps2), Stat1(m1Btlr), or Tnf-null mutations. Both autoimmune and autoinflammatory phenotypes are suppressed when spin homozygotes are derived into a germ-free environment. The spin phenotype was ascribed to a viable hypomorphic allele of Ptpn6, which encodes the tyrosine phosphatase SHP1, mutated in mice with the classical motheaten alleles me and me-v. Inflammation and autoimmunity caused by SHP1 deficiency are thus conditional. The SHP1-deficient phenotype is driven by microbes, which activate TLR signaling pathways to elicit IL-1 production. IL-1 signaling via MyD88 elicits inflammatory disease.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Alleles
  • Animals
  • Autoimmune Diseases / genetics*
  • Autoimmune Diseases / immunology
  • Autoimmune Diseases / microbiology
  • Autoimmunity / genetics
  • Ethylnitrosourea / pharmacology
  • Homozygote
  • Inflammation / genetics*
  • Inflammation / immunology
  • Inflammation / microbiology
  • Interleukin-1 / genetics
  • Interleukin-1 / immunology*
  • Interleukin-1 Receptor-Associated Kinases / genetics
  • Interleukin-1 Receptor-Associated Kinases / immunology
  • Listeriosis / immunology*
  • Mice
  • Mice, Mutant Strains
  • Mutagenesis
  • Mutation
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / immunology*
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6 / genetics*
  • Receptors, Interleukin-1 / immunology
  • Toll-Like Receptors / immunology

Substances

  • Interleukin-1
  • Myeloid Differentiation Factor 88
  • Receptors, Interleukin-1
  • Toll-Like Receptors
  • Interleukin-1 Receptor-Associated Kinases
  • Irak4 protein, mouse
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6
  • Ptpn6 protein, mouse
  • Ethylnitrosourea