Deregulation of XBP1 expression contributes to myocardial vascular endothelial growth factor-A expression and angiogenesis during cardiac hypertrophy in vivo

Aging Cell. 2016 Aug;15(4):625-33. doi: 10.1111/acel.12460. Epub 2016 May 1.

Abstract

Endoplasmic reticulum (ER) stress has been reported to be involved in many cardiovascular diseases such as atherosclerosis, diabetes, myocardial ischemia, and hypertension that ultimately result in heart failure. XBP1 is a key ER stress signal transducer and an important pro-survival factor of the unfolded protein response (UPR) in mammalian cells. The aim of this study was to establish a role for XBP1 in the deregulation of pro-angiogenic factor VEGF expression and potential regulatory mechanisms in hypertrophic and failing heart. Western blots showed that myocardial XBP1s protein was significantly increased in both isoproterenol (ISO)-induced and pressure-overload-induced hypertrophic and failing heart compared to normal control. Furthermore, XBP1 silencing exacerbates ISO-induced cardiac dysfunction along with a reduction of myocardial capillary density and cardiac expression of pro-angiogenic factor VEGF-A in vivo. Consistently, experiments in cultured cardiomyocytes H9c2 (2-1) cells showed that UPR-induced VEGF-A upregulation was determined by XBP1 expression level. Importantly, VEGF-A expression was increased in failing human heart tissue and blood samples and was correlated with the levels of XBP1. These results suggest that XBP1 regulates VEGF-mediated cardiac angiogenesis, which contributes to the progression of adaptive hypertrophy, and might provide novel targets for prevention and treatment of heart failure.

Keywords: XBP1; angiogenesis; cardiac hypertrophy; unfolded protein response; vascular endothelial growth factor-A.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Animals
  • Capillaries / drug effects
  • Capillaries / pathology
  • Cardiomegaly / complications
  • Cardiomegaly / genetics*
  • Cardiomegaly / metabolism
  • Cardiomegaly / physiopathology
  • Cell Line
  • Dependovirus / metabolism
  • Endoplasmic Reticulum Stress / genetics
  • Female
  • Gene Silencing
  • Heart Failure / complications
  • Heart Failure / genetics
  • Heart Failure / metabolism
  • Heart Failure / physiopathology
  • Humans
  • Isoproterenol
  • Male
  • Mice, Inbred C57BL
  • Middle Aged
  • Models, Biological
  • Myocardium / metabolism*
  • Myocardium / pathology
  • Neovascularization, Physiologic / genetics*
  • RNA, Small Interfering / metabolism
  • Rats
  • Unfolded Protein Response / genetics
  • Up-Regulation
  • Vascular Endothelial Growth Factor A / metabolism*
  • X-Box Binding Protein 1 / genetics*
  • X-Box Binding Protein 1 / metabolism

Substances

  • RNA, Small Interfering
  • Vascular Endothelial Growth Factor A
  • X-Box Binding Protein 1
  • XBP1 protein, human
  • Xbp1 protein, mouse
  • Xbp1 protein, rat
  • Isoproterenol