Redox modification of nuclear actin by MICAL-2 regulates SRF signaling

Cell. 2014 Jan 30;156(3):563-76. doi: 10.1016/j.cell.2013.12.035. Epub 2014 Jan 16.

Abstract

The serum response factor (SRF) binds to coactivators, such as myocardin-related transcription factor-A (MRTF-A), and mediates gene transcription elicited by diverse signaling pathways. SRF/MRTF-A-dependent gene transcription is activated when nuclear MRTF-A levels increase, enabling the formation of transcriptionally active SRF/MRTF-A complexes. The level of nuclear MRTF-A is regulated by nuclear G-actin, which binds to MRTF-A and promotes its nuclear export. However, pathways that regulate nuclear actin levels are poorly understood. Here, we show that MICAL-2, an atypical actin-regulatory protein, mediates SRF/MRTF-A-dependent gene transcription elicited by nerve growth factor and serum. MICAL-2 induces redox-dependent depolymerization of nuclear actin, which decreases nuclear G-actin and increases MRTF-A in the nucleus. Furthermore, we show that MICAL-2 is a target of CCG-1423, a small molecule inhibitor of SRF/MRTF-A-dependent transcription that exhibits efficacy in various preclinical disease models. These data identify redox modification of nuclear actin as a regulatory switch that mediates SRF/MRTF-A-dependent gene transcription.

Publication types

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

MeSH terms

  • Actins / metabolism
  • Amino Acid Sequence
  • Anilides / pharmacology
  • Animals
  • Benzamides / pharmacology
  • Cell Line
  • Cell Nucleus / metabolism*
  • Cells, Cultured
  • DNA-Binding Proteins / metabolism
  • Gene Knockdown Techniques
  • Humans
  • Mice
  • Microfilament Proteins / analysis
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism*
  • Mixed Function Oxygenases / analysis
  • Mixed Function Oxygenases / genetics
  • Mixed Function Oxygenases / metabolism
  • Molecular Sequence Data
  • Nerve Growth Factor / metabolism
  • Neurites / metabolism
  • Oncogene Proteins, Fusion / metabolism
  • Oxidation-Reduction
  • Oxidoreductases / analysis
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism*
  • Rats
  • Sequence Alignment
  • Serum Response Factor / metabolism*
  • Signal Transduction*
  • Trans-Activators
  • Transcription, Genetic
  • Zebrafish

Substances

  • Actins
  • Anilides
  • Benzamides
  • CCG 1423
  • DNA-Binding Proteins
  • MRTFA protein, human
  • Microfilament Proteins
  • Oncogene Proteins, Fusion
  • Serum Response Factor
  • Trans-Activators
  • Nerve Growth Factor
  • MICAL2 protein, human
  • MICAL3 protein, human
  • Mixed Function Oxygenases
  • Oxidoreductases