Vascular smooth muscle cell contractile protein expression is increased through protein kinase G-dependent and -independent pathways by glucose-6-phosphate dehydrogenase inhibition and deficiency

Am J Physiol Heart Circ Physiol. 2016 Oct 1;311(4):H904-H912. doi: 10.1152/ajpheart.00335.2016. Epub 2016 Aug 12.

Abstract

Homeostatic control of vascular smooth muscle cell (VSMC) differentiation is critical for contractile activity and regulation of blood flow. Recently, we reported that precontracted blood vessels are relaxed and the phenotype of VSMC is regulated from a synthetic to contractile state by glucose-6-phosphate dehydrogenase (G6PD) inhibition. In the current study, we investigated whether the increase in the expression of VSMC contractile proteins by inhibition and knockdown of G6PD is mediated through a protein kinase G (PKG)-dependent pathway and whether it regulates blood pressure. We found that the expression of VSMC-restricted contractile proteins, myocardin (MYOCD), and miR-1 and miR-143 are increased by G6PD inhibition or knockdown. Importantly, RNA-sequence analysis of aortic tissue from G6PD-deficient mice revealed uniform increases in VSMC-restricted genes, particularly those regulated by the MYOCD-serum response factor (SRF) switch. Conversely, expression of Krüppel-like factor 4 (KLF4) is decreased by G6PD inhibition. Interestingly, the G6PD inhibition-induced expression of miR-1 and contractile proteins was blocked by Rp-β-phenyl-1,N2-etheno-8-bromo-guanosine-3',5'-cyclic monophosphorothioate, a PKG inhibitor. On the other hand, MYOCD and miR-143 levels are increased by G6PD inhibition through a PKG-independent manner. Furthermore, blood pressure was lower in the G6PD-deficient compared with wild-type mice. Therefore, our results suggest that the expression of VSMC contractile proteins induced by G6PD inhibition occurs via PKG1α-dependent and -independent pathways.

Keywords: NADPH redox; RNA-seq; epigenetics; metabolism; pentose phosphate pathway; protein kinase G; vascular smooth muscle phenotype.

MeSH terms

  • Animals
  • Aorta / drug effects
  • Aorta / metabolism*
  • Blotting, Western
  • Cattle
  • Chromatography, Liquid
  • Contractile Proteins / drug effects
  • Contractile Proteins / genetics*
  • Contractile Proteins / metabolism
  • Cyclic GMP-Dependent Protein Kinase Type I / antagonists & inhibitors
  • Cyclic GMP-Dependent Protein Kinase Type I / metabolism*
  • Cyclic GMP-Dependent Protein Kinases / antagonists & inhibitors
  • Cyclic GMP-Dependent Protein Kinases / metabolism
  • Gene Knockdown Techniques
  • Glucosephosphate Dehydrogenase / antagonists & inhibitors*
  • Glucosephosphate Dehydrogenase / genetics
  • Immunoprecipitation
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors / drug effects
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism
  • Mice
  • MicroRNAs / drug effects
  • MicroRNAs / genetics
  • Muscle, Smooth, Vascular / cytology
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / metabolism*
  • Myocytes, Smooth Muscle / drug effects
  • Myocytes, Smooth Muscle / metabolism*
  • Nuclear Proteins / drug effects
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Polymerase Chain Reaction
  • Rats
  • Serum Response Factor / drug effects
  • Serum Response Factor / genetics
  • Serum Response Factor / metabolism
  • Tandem Mass Spectrometry
  • Trans-Activators / drug effects
  • Trans-Activators / genetics
  • Trans-Activators / metabolism

Substances

  • Contractile Proteins
  • Klf4 protein, mouse
  • Klf4 protein, rat
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors
  • MicroRNAs
  • Mirn1 microRNA, mouse
  • MIRN143 microRNA, mouse
  • Nuclear Proteins
  • Serum Response Factor
  • Trans-Activators
  • myocardin
  • Glucosephosphate Dehydrogenase
  • Cyclic GMP-Dependent Protein Kinase Type I
  • Cyclic GMP-Dependent Protein Kinases