Dominant negative variants in ITPR3 impair T cell Ca2+ dynamics causing combined immunodeficiency

J Exp Med. 2025 Jan 6;222(1):e20220979. doi: 10.1084/jem.20220979. Epub 2024 Nov 19.

Abstract

The importance of calcium (Ca2+) as a second messenger in T cell signaling is exemplified by genetic deficiencies of STIM1 and ORAI1, which abolish store-operated Ca2+ entry (SOCE) resulting in combined immunodeficiency (CID). We report five unrelated patients with de novo missense variants in ITPR3, encoding a subunit of the inositol 1,4,5-trisphosphate receptor (IP3R), which forms a Ca2+ channel in the endoplasmic reticulum (ER) membrane responsible for the release of ER Ca2+ required to trigger SOCE, and for Ca2+ transfer to other organelles. The patients presented with CID, abnormal T cell Ca2+ homeostasis, incompletely penetrant ectodermal dysplasia, and multisystem disease. Their predominant T cell immunodeficiency is characterized by significant T cell lymphopenia, defects in late stages of thymic T cell development, and impaired function of peripheral T cells, including inadequate NF-κB- and NFAT-mediated, proliferative, and metabolic responses to activation. Pathogenicity is not due to haploinsufficiency, rather ITPR3 protein variants interfere with IP3R channel function leading to depletion of ER Ca2+ stores and blunted SOCE in T cells.

MeSH terms

  • Calcium Signaling
  • Calcium* / metabolism
  • Child
  • Child, Preschool
  • Endoplasmic Reticulum / metabolism
  • Female
  • Humans
  • Infant
  • Inositol 1,4,5-Trisphosphate Receptors* / genetics
  • Inositol 1,4,5-Trisphosphate Receptors* / metabolism
  • Male
  • Mutation, Missense
  • Severe Combined Immunodeficiency / genetics
  • Severe Combined Immunodeficiency / immunology
  • Severe Combined Immunodeficiency / metabolism
  • Severe Combined Immunodeficiency / pathology
  • T-Lymphocytes* / immunology
  • T-Lymphocytes* / metabolism

Substances

  • Inositol 1,4,5-Trisphosphate Receptors
  • ITPR3 protein, human
  • Calcium