Gain-of-function human UNC93B1 variants cause systemic lupus erythematosus and chilblain lupus

J Exp Med. 2024 Aug 5;221(8):e20232066. doi: 10.1084/jem.20232066. Epub 2024 Jun 13.

Abstract

UNC93B1 is a transmembrane domain protein mediating the signaling of endosomal Toll-like receptors (TLRs). We report five families harboring rare missense substitutions (I317M, G325C, L330R, R466S, and R525P) in UNC93B1 causing systemic lupus erythematosus (SLE) or chilblain lupus (CBL) as either autosomal dominant or autosomal recessive traits. As for a D34A mutation causing murine lupus, we recorded a gain of TLR7 and, to a lesser extent, TLR8 activity with the I317M (in vitro) and G325C (in vitro and ex vivo) variants in the context of SLE. Contrastingly, in three families segregating CBL, the L330R, R466S, and R525P variants were isomorphic with respect to TLR7 activity in vitro and, for R525P, ex vivo. Rather, these variants demonstrated a gain of TLR8 activity. We observed enhanced interaction of the G325C, L330R, and R466S variants with TLR8, but not the R525P substitution, indicating different disease mechanisms. Overall, these observations suggest that UNC93B1 mutations cause monogenic SLE or CBL due to differentially enhanced TLR7 and TLR8 signaling.

MeSH terms

  • Adult
  • Chilblains* / genetics
  • Child
  • Child, Preschool
  • Female
  • Gain of Function Mutation
  • HEK293 Cells
  • Humans
  • Lupus Erythematosus, Cutaneous / genetics
  • Lupus Erythematosus, Cutaneous / pathology
  • Lupus Erythematosus, Systemic* / genetics
  • Male
  • Membrane Transport Proteins / genetics
  • Membrane Transport Proteins / metabolism
  • Mutation, Missense
  • Pedigree
  • Toll-Like Receptor 7* / genetics
  • Toll-Like Receptor 7* / metabolism
  • Toll-Like Receptor 8 / genetics
  • Toll-Like Receptor 8 / metabolism
  • Young Adult

Substances

  • Membrane Transport Proteins
  • TLR7 protein, human
  • Toll-Like Receptor 7
  • Toll-Like Receptor 8
  • UNC93B1 protein, human

Supplementary concepts

  • Chilblain lupus 1