Immunomodulating role of the JAKs inhibitor tofacitinib in a mouse model of bleomycin-induced scleroderma

J Dermatol Sci. 2021 Mar;101(3):174-184. doi: 10.1016/j.jdermsci.2020.12.007. Epub 2020 Dec 30.

Abstract

Background: Janus kinase (JAK)-signal transducer and activator of transcription (STAT) was hyperactivated in biopsies from patients with systemic sclerosis (SSc) and in several autoimmune disease models. Tofacitinib, a pan-JAK inhibitor, blocks the downstream signaling of multiple cytokines and has exhibited therapeutic efficacy in various autoimmune diseases, although its immunomodulating property in scleroderma is unclear.

Objective: To evaluate the effect of tofacitinib on the modulation of cytokine-producing T and B cells, and proinflammatory cells in a mouse model of SSc.

Methods: Bleomycin (BLM)-induced SSc was generated by intradermal injection of BLM or PBS for control. Mice received intraperitoneal tofacitinib (20 mg/kg) or vehicle 3 times per week from day 0-28. Mice were sacrificed at day 28 after the last BLM/PBS injection.

Results: Tofacitinib administration significantly alleviated fibrosis of the skin and lungs in scleroderma mouse model. Furthermore, tofacitinib suppressed adaptive and innate immune responses by reducing splenocytes, total lymphocytes, CD4+ T helper cells (especially Th2 and Th17 subtypes), IL-6-producing effector B cells, PDCA-1+ dendritic cells in the spleen, and infiltration of F4/80+, CD206+ and CD163+ macrophages in the skin and lungs. Conversely, tofacitinib increased the proportions of splenic regulatory T and B cells. The mRNA expression of extracellular matrix proteins and fibrogenic cytokines was downregulated by tofacitinib in both the skin and lungs.

Conclusion: These observations suggest JAK inhibition as a therapeutic approach for the treatment of inflammatory and fibrotic diseases, and highlight the potential of tofacitinib as a promising candidate for treating patients with scleroderma.

Keywords: Cytokines; Fibrosis; Immunomodulation; Systemic sclerosis; Tofacitinib.

MeSH terms

  • Adaptive Immunity / drug effects
  • Animals
  • B-Lymphocytes, Regulatory / immunology
  • B-Lymphocytes, Regulatory / metabolism
  • Bleomycin / administration & dosage
  • Bleomycin / toxicity
  • Cell Differentiation / drug effects
  • Cell Differentiation / immunology
  • Cytokines / metabolism
  • Disease Models, Animal
  • Female
  • Humans
  • Injections, Intraperitoneal
  • Janus Kinase Inhibitors / pharmacology*
  • Janus Kinase Inhibitors / therapeutic use
  • Lung / drug effects
  • Lung / immunology
  • Lung / pathology
  • Macrophages / drug effects
  • Macrophages / immunology
  • Mice
  • Piperidines / pharmacology*
  • Piperidines / therapeutic use
  • Pyrimidines / pharmacology*
  • Pyrimidines / therapeutic use
  • Scleroderma, Systemic / chemically induced
  • Scleroderma, Systemic / drug therapy*
  • Scleroderma, Systemic / immunology
  • Scleroderma, Systemic / pathology
  • Signal Transduction / drug effects
  • Signal Transduction / immunology
  • Skin / drug effects
  • Skin / immunology
  • Skin / pathology
  • T-Lymphocytes, Helper-Inducer / immunology
  • T-Lymphocytes, Helper-Inducer / metabolism
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism

Substances

  • Cytokines
  • Janus Kinase Inhibitors
  • Piperidines
  • Pyrimidines
  • Bleomycin
  • tofacitinib