Innate Immune Signaling Contributes to Tubular Cell Senescence in the Glis2 Knockout Mouse Model of Nephronophthisis

Am J Pathol. 2020 Jan;190(1):176-189. doi: 10.1016/j.ajpath.2019.09.013. Epub 2019 Oct 30.

Abstract

Nephronophthisis (NPHP), the leading genetic cause of end-stage renal failure in children and young adults, is a group of autosomal recessive diseases characterized by kidney-cyst degeneration and fibrosis for which no therapy is currently available. To date, mutations in >25 genes have been identified as causes of this disease that, in several cases, result in chronic DNA damage in kidney tubular cells. Among such mutations, those in the transcription factor-encoding GLIS2 cause NPHP type 7. Loss of function of mouse Glis2 causes senescence of kidney tubular cells. Senescent cells secrete proinflammatory molecules that induce progressive organ damage through several pathways, among which NF-κB signaling is prevalent. Herein, we show that the NF-κB signaling is active in Glis2 knockout kidney epithelial cells and that genetic inactivation of the toll-like receptor (TLR)/IL-1 receptor or pharmacologic elimination of senescent cells (senolytic therapy) reduces tubule damage, fibrosis, and apoptosis in the Glis2 mouse model of NPHP. Notably, in Glis2, Tlr2 double knockouts, senescence was also reduced and proliferation was increased, suggesting that loss of TLR2 activity improves the regenerative potential of tubular cells in Glis2 knockout kidneys. Our results further suggest that a combination of TLR/IL-1 receptor inhibition and senolytic therapy may delay the progression of kidney disease in NPHP type 7 and other forms of this disease.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis
  • Cellular Senescence / immunology*
  • Disease Models, Animal*
  • Immunity, Innate / immunology*
  • Kidney Diseases, Cystic / immunology
  • Kidney Diseases, Cystic / metabolism
  • Kidney Diseases, Cystic / pathology*
  • Kidney Tubules / immunology
  • Kidney Tubules / metabolism
  • Kidney Tubules / pathology*
  • Kruppel-Like Transcription Factors / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myeloid Differentiation Factor 88 / physiology
  • Nerve Tissue Proteins / physiology*
  • Toll-Like Receptor 2 / physiology

Substances

  • Gli5 protein, mouse
  • Kruppel-Like Transcription Factors
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Nerve Tissue Proteins
  • Tlr2 protein, mouse
  • Toll-Like Receptor 2