PKCε-CREB-Nrf2 signalling induces HO-1 in the vascular endothelium and enhances resistance to inflammation and apoptosis

Cardiovasc Res. 2015 Jun 1;106(3):509-19. doi: 10.1093/cvr/cvv131. Epub 2015 Apr 16.

Abstract

Aims: Vascular injury leading to endothelial dysfunction is a characteristic feature of chronic renal disease, diabetes mellitus, and systemic inflammatory conditions, and predisposes to apoptosis and atherogenesis. Thus, endothelial dysfunction represents a potential therapeutic target for atherosclerosis prevention. The observation that activity of either protein kinase C epsilon (PKCε) or haem oxygenase-1 (HO-1) enhances endothelial cell (EC) resistance to inflammation and apoptosis led us to test the hypothesis that HO-1 is a downstream target of PKCε.

Methods and results: Expression of constitutively active PKCε in human EC significantly increased HO-1 mRNA and protein, whereas conversely aortas or cardiac EC from PKCε-deficient mice exhibited reduced HO-1 when compared with wild-type littermates. Angiotensin II activated PKCε and induced HO-1 via a PKCε-dependent pathway. PKCε activation significantly attenuated TNFα-induced intercellular adhesion molecule-1, and increased resistance to serum starvation-induced apoptosis. These responses were reversed by the HO antagonist zinc protoporphyrin IX. Phosphokinase antibody array analysis identified CREB1((Ser133)) phosphorylation as a PKCε signalling intermediary, and cAMP response element-binding protein 1 (CREB1) siRNA abrogated PKCε-induced HO-1 up-regulation. Likewise, nuclear factor (erythroid-derived 2)-like 2 (Nrf2) was identified as a PKCε target using nuclear translocation and DNA-binding assays, and Nrf2 siRNA prevented PKCε-mediated HO-1 induction. Moreover, depletion of CREB1 inhibited PKCε-induced Nrf2 DNA binding, suggestive of transcriptional co-operation between CREB1 and Nrf2.

Conclusions: PKCε activity in the vascular endothelium regulates HO-1 via a pathway requiring CREB1 and Nrf2. Given the potent protective actions of HO-1, we propose that this mechanism is an important contributor to the emerging role of PKCε in the maintenance of endothelial homeostasis and resistance to injury.

Keywords: Apoptosis; Endothelium; Haem oxygenase-1; Inflammation; Protein kinase C epsilon.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / pharmacology
  • Animals
  • Apoptosis* / drug effects
  • Cells, Cultured
  • Cyclic AMP Response Element-Binding Protein / genetics
  • Cyclic AMP Response Element-Binding Protein / metabolism*
  • Endothelial Cells / drug effects
  • Endothelial Cells / enzymology*
  • Endothelial Cells / pathology
  • Enzyme Activation
  • Enzyme Induction
  • Enzyme Inhibitors / pharmacology
  • Gene Expression Regulation
  • Heme Oxygenase-1 / antagonists & inhibitors
  • Heme Oxygenase-1 / biosynthesis*
  • Heme Oxygenase-1 / genetics
  • Human Umbilical Vein Endothelial Cells / drug effects
  • Human Umbilical Vein Endothelial Cells / enzymology
  • Human Umbilical Vein Endothelial Cells / pathology
  • Humans
  • Inflammation / enzymology
  • Inflammation / genetics
  • Inflammation / pathology
  • Inflammation / prevention & control*
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / biosynthesis*
  • Membrane Proteins / genetics
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NF-E2-Related Factor 2 / genetics
  • NF-E2-Related Factor 2 / metabolism*
  • Phosphorylation
  • Protein Kinase C-epsilon / genetics
  • Protein Kinase C-epsilon / metabolism*
  • Protoporphyrins / pharmacology
  • RNA Interference
  • Signal Transduction* / drug effects
  • Time Factors
  • Transcription, Genetic
  • Transfection

Substances

  • CREB1 protein, human
  • Creb1 protein, mouse
  • Cyclic AMP Response Element-Binding Protein
  • Enzyme Inhibitors
  • Membrane Proteins
  • NF-E2-Related Factor 2
  • NFE2L2 protein, human
  • Nfe2l2 protein, mouse
  • Protoporphyrins
  • Angiotensin II
  • zinc protoporphyrin
  • HMOX1 protein, human
  • Heme Oxygenase-1
  • Hmox1 protein, mouse
  • Prkce protein, mouse
  • PRKCE protein, human
  • Protein Kinase C-epsilon