Genetic activation of Nrf2 reduces cutaneous symptoms in a murine model of Netherton syndrome

Dis Model Mech. 2020 Jun 1;13(5):dmm042648. doi: 10.1242/dmm.042648.

Abstract

Netherton syndrome is a monogenic autosomal recessive disorder primarily characterized by the detachment of the uppermost layer of the epidermis, the stratum corneum It results from mutations in the SPINK5 gene, which codes for a kallikrein inhibitor. Uncontrolled kallikrein activity leads to premature desquamation, resulting in a severe epidermal barrier defect and subsequent life-threatening systemic infections and chronic cutaneous inflammation. Here, we show that genetic activation of the transcription factor nuclear factor (erythroid-derived 2)-like 2 (Nfe2l2/Nrf2) in keratinocytes of Spink5 knockout mice, a model for Netherton syndrome, significantly alleviates their cutaneous phenotype. Nrf2 activation promoted attachment of the stratum corneum and concomitant epidermal barrier function, and reduced the expression of pro-inflammatory cytokines such as tumor necrosis factor α and thymic stromal lymphopoietin. Mechanistically, we show that Nrf2 activation induces overexpression of secretory leukocyte protease inhibitor (Slpi), a known inhibitor of kallikrein 7 and elastase 2, in mouse and human keratinocytes in vivo and in vitro, respectively. In the Spink5-deficient epidermis, the upregulation of Slpi is likely to promote stabilization of corneodesmosomes, thereby preventing premature desquamation. Our results suggest pharmacological NRF2 activation as a promising treatment modality for Netherton syndrome patients.This article has an associated First Person interview with the first author of the paper.

Keywords: Epidermal barrier; Inflammation; Netherton syndrome; Nrf2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Adhesion
  • Cell Differentiation
  • Chemokines / metabolism
  • Disease Models, Animal
  • Epidermis / pathology
  • Humans
  • Inflammation / pathology
  • Inflammation Mediators / metabolism
  • Integrases / metabolism
  • Keratinocytes / pathology
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NAD(P)H Dehydrogenase (Quinone) / metabolism
  • NF-E2-Related Factor 2 / genetics*
  • NF-E2-Related Factor 2 / metabolism
  • Netherton Syndrome / genetics*
  • Netherton Syndrome / pathology*
  • Secretory Leukocyte Peptidase Inhibitor / metabolism
  • Serine Peptidase Inhibitor Kazal-Type 5 / deficiency
  • Serine Peptidase Inhibitor Kazal-Type 5 / genetics
  • Skin / pathology*

Substances

  • Chemokines
  • Inflammation Mediators
  • NF-E2-Related Factor 2
  • SLPI protein, human
  • Secretory Leukocyte Peptidase Inhibitor
  • Serine Peptidase Inhibitor Kazal-Type 5
  • Spink5 protein, mouse
  • NAD(P)H Dehydrogenase (Quinone)
  • NQO1 protein, human
  • Cre recombinase
  • Integrases