Complex Autoinflammatory Syndrome Unveils Fundamental Principles of JAK1 Kinase Transcriptional and Biochemical Function

Immunity. 2020 Sep 15;53(3):672-684.e11. doi: 10.1016/j.immuni.2020.07.006. Epub 2020 Aug 3.

Abstract

Autoinflammatory disease can result from monogenic errors of immunity. We describe a patient with early-onset multi-organ immune dysregulation resulting from a mosaic, gain-of-function mutation (S703I) in JAK1, encoding a kinase essential for signaling downstream of >25 cytokines. By custom single-cell RNA sequencing, we examine mosaicism with single-cell resolution. We find that JAK1 transcription was predominantly restricted to a single allele across different cells, introducing the concept of a mutational "transcriptotype" that differs from the genotype. Functionally, the mutation increases JAK1 activity and transactivates partnering JAKs, independent of its catalytic domain. S703I JAK1 is not only hypermorphic for cytokine signaling but also neomorphic, as it enables signaling cascades not canonically mediated by JAK1. Given these results, the patient was treated with tofacitinib, a JAK inhibitor, leading to the rapid resolution of clinical disease. These findings offer a platform for personalized medicine with the concurrent discovery of fundamental biological principles.

Keywords: JAK inhibitors; JAK-STAT signaling; JAK1; cytokine signaling; inborn errors of immunity; monoallelic expression; mosaicis; precision medicine.

Publication types

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

MeSH terms

  • Adolescent
  • COVID-19 / mortality
  • Catalytic Domain / genetics
  • Cell Line
  • Cytokines / metabolism
  • Female
  • Gain of Function Mutation / genetics
  • Genotype
  • HEK293 Cells
  • Hereditary Autoinflammatory Diseases / drug therapy
  • Hereditary Autoinflammatory Diseases / genetics*
  • Hereditary Autoinflammatory Diseases / pathology*
  • Humans
  • Janus Kinase 1 / antagonists & inhibitors
  • Janus Kinase 1 / genetics*
  • Mosaicism
  • Piperidines / therapeutic use
  • Precision Medicine / methods
  • Pyrimidines / therapeutic use
  • Signal Transduction / immunology
  • Systemic Inflammatory Response Syndrome / drug therapy
  • Systemic Inflammatory Response Syndrome / genetics*
  • Systemic Inflammatory Response Syndrome / pathology*

Substances

  • Cytokines
  • Piperidines
  • Pyrimidines
  • tofacitinib
  • JAK1 protein, human
  • Janus Kinase 1