CXCR4 induces podocyte injury and proteinuria by activating β-catenin signaling

Theranostics. 2022 Jan 1;12(2):767-781. doi: 10.7150/thno.65948. eCollection 2022.

Abstract

Background: C-X-C chemokine receptor type 4 (CXCR4) plays a crucial role in mediating podocyte dysfunction, proteinuria and glomerulosclerosis. However, the underlying mechanism remains poorly understood. Here we studied the role of β-catenin in mediating CXCR4-triggered podocyte injury. Methods: Mouse models of proteinuric kidney diseases were used to assess CXCR4 and β-catenin expression. We utilized cultured podocytes and glomeruli to delineate the signal pathways involved. Conditional knockout mice with podocyte-specific deletion of CXCR4 were generated and used to corroborate a role of CXCR4/β-catenin in podocyte injury and proteinuria. Results: Both CXCR4 and β-catenin were induced and colocalized in the glomerular podocytes in several models of proteinuric kidney diseases. Activation of CXCR4 by its ligand SDF-1α stimulated β-catenin activation but did not affect the expression of Wnt ligands in vitro. Blockade of β-catenin signaling by ICG-001 preserved podocyte signature proteins and inhibited Snail1 and MMP-7 expression in vitro and ex vivo. Mechanistically, activation of CXCR4 by SDF-1α caused the formation of CXCR4/β-arrestin-1/Src signalosome in podocytes, which led to sequential phosphorylation of Src, EGFR, ERK1/2 and GSK-3β and ultimately β-catenin stabilization and activation. Silencing β-arrestin-1 abolished this cascade of events and inhibited β-catenin in response to CXCR4 stimulation. Podocyte-specific knockout of CXCR4 in mice abolished β-catenin activation, preserved podocyte integrity, reduced proteinuria and ameliorated glomerulosclerosis after Adriamycin injury. Conclusion: These results suggest that CXCR4 promotes podocyte dysfunction and proteinuria by assembling CXCR4/β-arrestin-1/Src signalosome, which triggers a cascade of signal events leading to β-catenin activation.

Keywords: CXCR4; Podocyte; glomerulosclerosis; proteinuria; β-arrestin-1; β-catenin.

Publication types

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

MeSH terms

  • Animals
  • Cell Line
  • Drug Delivery Systems
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Podocytes / metabolism*
  • Proteinuria / etiology*
  • Proteinuria / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, CXCR4 / antagonists & inhibitors
  • Receptors, CXCR4 / metabolism*
  • Renal Insufficiency, Chronic / drug therapy
  • Renal Insufficiency, Chronic / etiology*
  • Renal Insufficiency, Chronic / metabolism
  • Signal Transduction*
  • beta Catenin / metabolism*

Substances

  • CXCR4 protein, mouse
  • Receptors, CXCR4
  • beta Catenin