Nuclear RhoA signaling regulates MRTF-dependent SMC-specific transcription

Am J Physiol Heart Circ Physiol. 2014 Aug 1;307(3):H379-90. doi: 10.1152/ajpheart.01002.2013. Epub 2014 Jun 6.

Abstract

We have previously shown that RhoA-mediated actin polymerization stimulates smooth muscle cell (SMC)-specific transcription by regulating the nuclear localization of the myocardin-related transcription factors (MRTFs). On the basis of the recent demonstration that nuclear G-actin regulates MRTF nuclear export and observations from our laboratory and others that the RhoA effector, mDia2, shuttles between the nucleus and cytoplasm, we investigated whether nuclear RhoA signaling plays a role in regulating MRTF activity. We identified sequences that control mDia2 nuclear-cytoplasmic shuttling and used mDia2 variants to demonstrate that the ability of mDia2 to fully stimulate MRTF nuclear accumulation and SMC-specific gene transcription was dependent on its localization to the nucleus. To test whether RhoA signaling promotes nuclear actin polymerization, we established a fluorescence recovery after photobleaching (FRAP)-based assay to measure green fluorescent protein-actin diffusion in the nuclear compartment. Nuclear actin FRAP was delayed in cells expressing nuclear-targeted constitutively active mDia1 and mDia2 variants and in cells treated with the polymerization inducer, jasplakinolide. In contrast, FRAP was enhanced in cells expressing a nuclear-targeted variant of mDia that inhibits both mDia1 and mDia2. Treatment of 10T1/2 cells with sphingosine 1-phosphate induced RhoA activity in the nucleus and forced nuclear localization of RhoA or the Rho-specific guanine nucleotide exchange factor (GEF), leukemia-associated RhoGEF, enhanced the ability of these proteins to stimulate MRTF activity. Taken together, these data support the emerging idea that RhoA-dependent nuclear actin polymerization has important effects on transcription and nuclear structure.

Keywords: RhoA; diaphanous formins; myocardin-related factors; serum response factor; smooth muscle.

Publication types

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

MeSH terms

  • Actins / genetics
  • Actins / metabolism
  • Active Transport, Cell Nucleus
  • Animals
  • Aorta, Thoracic / enzymology
  • COS Cells
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Differentiation
  • Cell Nucleus / enzymology*
  • Chlorocebus aethiops
  • Fluorescence Recovery After Photobleaching
  • Formins
  • Gene Expression Regulation
  • Green Fluorescent Proteins / biosynthesis
  • Green Fluorescent Proteins / genetics
  • Mice
  • Microtubule-Associated Proteins / genetics
  • Microtubule-Associated Proteins / metabolism
  • Muscle, Smooth, Vascular / enzymology*
  • Myocytes, Smooth Muscle / enzymology*
  • NADPH Dehydrogenase / genetics
  • NADPH Dehydrogenase / metabolism
  • RNA Interference
  • Rho Guanine Nucleotide Exchange Factors / genetics
  • Rho Guanine Nucleotide Exchange Factors / metabolism
  • Signal Transduction*
  • Time Factors
  • Trans-Activators / genetics
  • Trans-Activators / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transcription, Genetic*
  • Transfection
  • rho GTP-Binding Proteins / metabolism*
  • rhoA GTP-Binding Protein

Substances

  • Actins
  • Arhgef12 protein, mouse
  • Carrier Proteins
  • Diap1 protein, mouse
  • Formins
  • Microtubule-Associated Proteins
  • Mrtfa protein, mouse
  • Rho Guanine Nucleotide Exchange Factors
  • Trans-Activators
  • Transcription Factors
  • myocardin-related transcription factor B, mouse
  • Green Fluorescent Proteins
  • Dia2 protein, mouse
  • NADPH Dehydrogenase
  • RhoA protein, mouse
  • rho GTP-Binding Proteins
  • rhoA GTP-Binding Protein