Tenascin-C promotes acute kidney injury to chronic kidney disease progression by impairing tubular integrity via αvβ6 integrin signaling

Kidney Int. 2020 May;97(5):1017-1031. doi: 10.1016/j.kint.2020.01.026. Epub 2020 Feb 17.

Abstract

Tenascin-C is an extracellular matrix glycoprotein that plays a critical role in kidney fibrosis by orchestrating a fibrogenic niche. Here, we demonstrate that tenascin-C is a biomarker and a mediator of kidney fibrogenesis by impairing tubular integrity. Tenascin-C was found to be increased in kidney biopsies from patients with chronic kidney disease (CKD). In a cohort of 225 patients with CKD, the urinary tenascin-C level was markedly elevated, compared to 39 healthy individuals. Moreover, the level of urinary tenascin-C in CKD was correlated with the severity of kidney dysfunction and fibrosis. In mouse model of acute kidney injury-to-CKD induced by ischemia/reperfusion, depletion of tenascin-C preserved tubular integrity and ameliorated renal fibrotic lesions. In vitro, tenascin-C impaired tubular cell integrity by inducing partial epithelial-mesenchymal transition. Using decellularized kidney tissue scaffolds, we found that tenascin-C-enriched scaffolds facilitated tubular epithelial-mesenchymal transition ex vivo. Mechanistically, tenascin-C specifically induced integrins αvβ6 in tubular cells and activated focal adhesion kinase (FAK). Blocking αvβ6 integrins or inhibition of FAK restored tubular integrity by repressing epithelial-mesenchymal transition and alleviated kidney fibrosis. Thus, our studies underscore that tenascin-C is a noninvasive biomarker of kidney fibrogenesis and a pathogenic mediator that impairs tubular integrity. Hence, blockade of the tenascin-C/αvβ6 integrin/FAK signal cascade may be a novel strategy for therapeutic intervention of kidney fibrosis.

Keywords: chronic kidney disease; epithelial-mesenchymal transition; integrin; microenvironment; renal fibrosis; tenascin-C.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Kidney Injury*
  • Animals
  • Antigens, Neoplasm
  • Epithelial-Mesenchymal Transition
  • Extracellular Matrix
  • Fibrosis
  • Humans
  • Integrins
  • Mice
  • Renal Insufficiency, Chronic*
  • Tenascin

Substances

  • Antigens, Neoplasm
  • Integrins
  • Tenascin
  • integrin alphavbeta6