Ruxolitinib reverses dysregulated T helper cell responses and controls autoimmunity caused by a novel signal transducer and activator of transcription 1 (STAT1) gain-of-function mutation

J Allergy Clin Immunol. 2017 May;139(5):1629-1640.e2. doi: 10.1016/j.jaci.2016.11.022. Epub 2017 Jan 27.

Abstract

Background: Gain-of-function (GOF) mutations in the human signal transducer and activator of transcription 1 (STAT1) manifest in immunodeficiency and autoimmunity with impaired TH17 cell differentiation and exaggerated responsiveness to type I and II interferons. Allogeneic bone marrow transplantation has been attempted in severely affected patients, but outcomes have been poor.

Objective: We sought to define the effect of increased STAT1 activity on T helper cell polarization and to investigate the therapeutic potential of ruxolitinib in treating autoimmunity secondary to STAT1 GOF mutations.

Methods: We used in vitro polarization assays, as well as phenotypic and functional analysis of STAT1-mutated patient cells.

Results: We report a child with a novel mutation in the linker domain of STAT1 who had life-threatening autoimmune cytopenias and chronic mucocutaneous candidiasis. Naive lymphocytes from the affected patient displayed increased TH1 and follicular T helper cell and suppressed TH17 cell responses. The mutation augmented cytokine-induced STAT1 phosphorylation without affecting dephosphorylation kinetics. Treatment with the Janus kinase 1/2 inhibitor ruxolitinib reduced hyperresponsiveness to type I and II interferons, normalized TH1 and follicular T helper cell responses, improved TH17 differentiation, cured mucocutaneous candidiasis, and maintained remission of immune-mediated cytopenias.

Conclusions: Autoimmunity and infection caused by STAT1 GOF mutations are the result of dysregulated T helper cell responses. Janus kinase inhibitor therapy could represent an effective targeted treatment for long-term disease control in severely affected patients for whom hematopoietic stem cell transplantation is not available.

Keywords: IFN-γ; STAT1 gain of function; T helper cell polarization; T(H)1 cell; T(H)17 cell; autoimmunity; follicular T helper cell; ruxolitinib.

Publication types

  • Case Reports

MeSH terms

  • Anemia, Hemolytic, Autoimmune / genetics*
  • Anemia, Hemolytic, Autoimmune / immunology
  • Autoimmunity / drug effects
  • Candidiasis, Chronic Mucocutaneous / genetics
  • Candidiasis, Chronic Mucocutaneous / immunology
  • Child
  • Cytokines / immunology
  • Female
  • Humans
  • Janus Kinases / antagonists & inhibitors
  • Mutation
  • Nitriles
  • Protein Kinase Inhibitors / pharmacology*
  • Purpura, Thrombocytopenic, Idiopathic / genetics*
  • Purpura, Thrombocytopenic, Idiopathic / immunology
  • Pyrazoles / pharmacology*
  • Pyrimidines
  • STAT1 Transcription Factor / genetics*
  • STAT1 Transcription Factor / immunology
  • Th1 Cells / drug effects*
  • Th1 Cells / immunology
  • Th17 Cells / drug effects*
  • Th17 Cells / immunology

Substances

  • Cytokines
  • Nitriles
  • Protein Kinase Inhibitors
  • Pyrazoles
  • Pyrimidines
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • ruxolitinib
  • Janus Kinases