Megakaryocytic leukemia 1 directs a histone H3 lysine 4 methyltransferase complex to regulate hypoxic pulmonary hypertension

Hypertension. 2015 Apr;65(4):821-33. doi: 10.1161/HYPERTENSIONAHA.114.04585. Epub 2015 Feb 2.

Abstract

Enhanced interaction between vascular endothelial cells and circulating leukocytes, as a result of transcriptional activation of cell adhesion molecules (CAM), helps establish a proinflammatory milieu contributing to the pathogenesis of chronic hypoxia-induced pulmonary hypertension. The molecular switch that dictates CAM transactivation is not clearly defined. Our goal was to determine the involvement of the transcriptional modulator megakaryocytic leukemia 1 (MKL1), also known as myocardin-related transcription factor A (MRTF-A), in CAM transactivation and the underlying mechanism. We report here that compared with wild-type littermates, MKL1/MRTF-A knockout mice were more resistant to the development of hypoxia-induced pulmonary hypertension when exposed to low oxygen pressure. Notably, CAM induction in knockout mice was significantly attenuated with a concomitant reduction of leukocyte adhesion. In cultured vascular endothelial cells, overexpression of MKL1/MRTF-A enhanced, whereas depletion of MKL1/MRTF-A dampened, hypoxia-induced CAM transactivation. In response to hypoxia, MKL1/MRTF-A formed a complex with NF-κB on the CAM promoters. Of interest, MKL1/MRTF-A was responsible for recruiting a histone H3 lysine 4 methyltransferase complex to the CAM promoters. Finally, endothelial-specific silencing of ASH2 and WDR5, 2 key components of the histone H3 lysine 4 methyltransferase complex, ameliorated hypoxia-induced pulmonary hypertension in mice. In conclusion, our data suggest that MKL1/MRTF-A, by coordinating key epigenetic alterations on CAM promoters, provides a critical link to hypoxia-induced endothelial malfunction and contributes to the pathogenesis of hypoxia-induced pulmonary hypertension.

Keywords: cell adhesion molecules; epigenetics; hypertension, pulmonary; hypoxia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Disease Models, Animal
  • Endothelium, Vascular / metabolism
  • Endothelium, Vascular / physiopathology
  • Epigenesis, Genetic
  • Gene Expression Regulation*
  • Hypertension, Pulmonary / etiology
  • Hypertension, Pulmonary / genetics*
  • Hypertension, Pulmonary / metabolism
  • Hypoxia / etiology
  • Hypoxia / genetics*
  • Hypoxia / metabolism
  • Leukemia, Megakaryoblastic, Acute / complications*
  • Leukemia, Megakaryoblastic, Acute / genetics
  • Leukemia, Megakaryoblastic, Acute / metabolism
  • Mice
  • Mice, Knockout
  • Polymerase Chain Reaction
  • Pulmonary Wedge Pressure
  • RNA / genetics*
  • Trans-Activators / biosynthesis
  • Trans-Activators / genetics*
  • Transcriptional Activation
  • Vasodilation

Substances

  • Mrtfa protein, mouse
  • Trans-Activators
  • RNA