Variant STAT4 and Response to Ruxolitinib in an Autoinflammatory Syndrome

N Engl J Med. 2023 Jun 15;388(24):2241-2252. doi: 10.1056/NEJMoa2202318. Epub 2023 May 31.

Abstract

Background: Disabling pansclerotic morphea (DPM) is a rare systemic inflammatory disorder, characterized by poor wound healing, fibrosis, cytopenias, hypogammaglobulinemia, and squamous-cell carcinoma. The cause is unknown, and mortality is high.

Methods: We evaluated four patients from three unrelated families with an autosomal dominant pattern of inheritance of DPM. Genomic sequencing independently identified three heterozygous variants in a specific region of the gene that encodes signal transducer and activator of transcription 4 (STAT4). Primary skin fibroblast and cell-line assays were used to define the functional nature of the genetic defect. We also assayed gene expression using single-cell RNA sequencing of peripheral-blood mononuclear cells to identify inflammatory pathways that may be affected in DPM and that may respond to therapy.

Results: Genome sequencing revealed three novel heterozygous missense gain-of-function variants in STAT4. In vitro, primary skin fibroblasts showed enhanced interleukin-6 secretion, with impaired wound healing, contraction of the collagen matrix, and matrix secretion. Inhibition of Janus kinase (JAK)-STAT signaling with ruxolitinib led to improvement in the hyperinflammatory fibroblast phenotype in vitro and resolution of inflammatory markers and clinical symptoms in treated patients, without adverse effects. Single-cell RNA sequencing revealed expression patterns consistent with an immunodysregulatory phenotype that were appropriately modified through JAK inhibition.

Conclusions: Gain-of-function variants in STAT4 caused DPM in the families that we studied. The JAK inhibitor ruxolitinib attenuated the dermatologic and inflammatory phenotype in vitro and in the affected family members. (Funded by the American Academy of Allergy, Asthma, and Immunology Foundation and others.).

MeSH terms

  • Anti-Inflammatory Agents / therapeutic use
  • Autoimmune Diseases* / drug therapy
  • Autoimmune Diseases* / genetics
  • Dermatologic Agents* / therapeutic use
  • Gain of Function Mutation
  • Janus Kinases* / antagonists & inhibitors
  • Mutation, Missense
  • Nitriles
  • Pyrazoles / pharmacology
  • Pyrazoles / therapeutic use
  • Pyrimidines
  • Scleroderma, Systemic* / drug therapy
  • Scleroderma, Systemic* / genetics

Substances

  • Janus Kinases
  • Nitriles
  • Pyrazoles
  • Pyrimidines
  • ruxolitinib
  • STAT4 protein, human
  • Dermatologic Agents
  • Anti-Inflammatory Agents