Synaptopodin Is a Coincidence Detector of Tyrosine versus Serine/Threonine Phosphorylation for the Modulation of Rho Protein Crosstalk in Podocytes

J Am Soc Nephrol. 2017 Mar;28(3):837-851. doi: 10.1681/ASN.2016040414. Epub 2016 Sep 14.

Abstract

Tyrosine and serine/threonine signal-transduction pathways influence many aspects of cell behavior, including the spatial and temporal regulation of the actin cytoskeleton. However, little is known about how input from diverse tyrosine and serine/threonine kinases is integrated to control Rho protein crosstalk and actin remodeling, which are critically important in podocyte health and disease. Here we unveil the proteolytically-regulated, actin organizing protein synaptopodin as a coincidence detector of tyrosine versus serine/threonine phosphorylation. We show that serine/threonine and tyrosine kinases duel for synaptopodin stability versus degradation. EGFR/Src-mediated tyrosine phosphorylation of synaptopodin in podocytes promotes binding to the serine/threonine phosphatase calcineurin. This leads to the loss of 14-3-3 binding, resulting in synaptopodin degradation, Vav2 activation, enhanced Rac1 signaling, and ultimate loss of stress fibers. Our studies reveal how synaptopodin, a single proteolytically-controlled protein, integrates antagonistic tyrosine versus serine/threonine phosphorylation events for the dynamic control of the actin cytoskeleton in podocytes.

Keywords: EGFR; FSGS; Rac1; TRPC5; cytoskeleton; glomerular disease.

MeSH terms

  • Animals
  • Calcineurin / metabolism
  • Cells, Cultured
  • Mice
  • Microfilament Proteins / physiology*
  • Phosphorylation
  • Podocytes / physiology*
  • Receptor Cross-Talk
  • Serine / metabolism*
  • Signal Transduction
  • Threonine / metabolism*
  • Tyrosine / metabolism*
  • rhoA GTP-Binding Protein / physiology*

Substances

  • Microfilament Proteins
  • Synpo protein, mouse
  • Threonine
  • Tyrosine
  • Serine
  • Calcineurin
  • rhoA GTP-Binding Protein