Protein kinase A, Ca2+/calmodulin-dependent kinase II, and calcineurin regulate the intracellular trafficking of myopodin between the Z-disc and the nucleus of cardiac myocytes

Mol Cell Biol. 2007 Dec;27(23):8215-27. doi: 10.1128/MCB.00950-07. Epub 2007 Oct 8.

Abstract

Spatial and temporal resolution of intracellular signaling can be achieved by compartmentalizing transduction units. Myopodin is a dual-compartment, actin-bundling protein that shuttles between the nucleus and the Z-disc of myocytes in a differentiation- and stress-dependent fashion. Importin alpha binding and nuclear import of myopodin are regulated by serine/threonine phosphorylation-dependent binding of myopodin to 14-3-3. Here we show that in the heart myopodin forms a Z-disc signaling complex with alpha-actinin, calcineurin, Ca2+/calmodulin-dependent kinase II (CaMKII), muscle-specific A-kinase anchoring protein, and myomegalin. Phosphorylation of myopodin by protein kinase A (PKA) or CaMKII mediates 14-3-3 binding and nuclear import in myoblasts. Dephosphorylation of myopodin by calcineurin abrogates 14-3-3beta binding. Activation of PKA or inhibition of calcineurin in adult cardiac myocytes releases myopodin from the Z-disc and induces its nuclear import. The identification of myopodin as a direct target of PKA, CaMKII, and calcineurin defines a novel intracellular signaling pathway whereby changes in Z-disc dynamics may translate into compartmentalized signal transduction in the heart.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • 14-3-3 Proteins / metabolism
  • A Kinase Anchor Proteins / metabolism
  • Actinin / metabolism
  • Active Transport, Cell Nucleus
  • Adaptor Proteins, Signal Transducing
  • Animals
  • Binding, Competitive
  • Calcineurin / metabolism*
  • Calcineurin Inhibitors
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism*
  • Cell Line
  • Cell Nucleus / metabolism*
  • Cyclic AMP-Dependent Protein Kinases / metabolism*
  • Cytoskeletal Proteins
  • Enzyme Activation
  • Humans
  • Mice
  • Microfilament Proteins / metabolism*
  • Muscle Proteins / metabolism
  • Myoblasts / cytology
  • Myoblasts / enzymology
  • Myocytes, Cardiac / cytology*
  • Myocytes, Cardiac / enzymology*
  • Nuclear Proteins / metabolism
  • Phosphoserine / metabolism
  • Phosphothreonine / metabolism
  • Protein Binding
  • Protein Transport
  • Rats
  • Signal Transduction

Substances

  • 14-3-3 Proteins
  • A Kinase Anchor Proteins
  • AKAP6 protein, human
  • Adaptor Proteins, Signal Transducing
  • Calcineurin Inhibitors
  • Cytoskeletal Proteins
  • Microfilament Proteins
  • Muscle Proteins
  • Nuclear Proteins
  • PDE4DIP protein, human
  • Synpo2 protein, mouse
  • Actinin
  • Phosphothreonine
  • Phosphoserine
  • Cyclic AMP-Dependent Protein Kinases
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcineurin