C-C Motif Chemokine Receptor 9 Exacerbates Pressure Overload-Induced Cardiac Hypertrophy and Dysfunction

J Am Heart Assoc. 2016 May 4;5(5):e003342. doi: 10.1161/JAHA.116.003342.

Abstract

Background: Maladaptive cardiac hypertrophy is a major risk factor for heart failure, which is the leading cause of death worldwide. C-C motif chemokine receptor 9 (CCR9), a subfamily of the G protein-coupled receptor supergene family, has been highlighted as an immunologic regulator in the development and homing of immune cells and in immune-related diseases. Recently, CCR9 was found to be involved in the pathogenesis of other diseases such as cardiovascular diseases; however, the effects that CCR9 exerts in cardiac hypertrophy remain elusive.

Methods and results: We observed significantly increased CCR9 protein levels in failing human hearts and in a mouse or cardiomyocyte hypertrophy model. In loss- and gain-of-function experiments, we found that pressure overload-induced hypertrophy was greatly attenuated by CCR9 deficiency in cardiac-specific CCR9 knockout mice, whereas CCR9 overexpression in cardiac-specific transgenic mice strikingly enhanced cardiac hypertrophy. The prohypertrophic effects of CCR9 were also tested in vitro, and a similar phenomenon was observed. Consequently, we identified a causal role for CCR9 in pathological cardiac hypertrophy. Mechanistically, we revealed a lack of difference in the expression levels of mitogen-activated protein kinases between groups, whereas the phosphorylation of AKT/protein kinase B and downstream effectors significantly decreased in CCR9 knockout mice and increased in CCR9 transgenic mice after aortic binding surgery.

Conclusions: The prohypertrophic effects of CCR9 were not attributable to the mitogen-activated protein kinase signaling pathway but rather to the AKT-mammalian target of rapamycin-glycogen synthase kinase 3β signaling cascade.

Keywords: AKT; C‐C motif chemokine receptor 9; cardiac dysfunction; cardiac hypertrophy; cardiovascular disease; cardiovascular research; heart failure; hypertrophy.

MeSH terms

  • Animals
  • Cardiomegaly / metabolism*
  • Cardiomyopathy, Dilated / diagnostic imaging
  • Cardiomyopathy, Dilated / metabolism*
  • Cardiomyopathy, Hypertrophic / diagnostic imaging
  • Cardiomyopathy, Hypertrophic / metabolism*
  • Glycogen Synthase Kinase 3 beta / metabolism
  • Humans
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / pathology
  • Phosphorylation
  • Proto-Oncogene Proteins c-akt / metabolism
  • Rats
  • Real-Time Polymerase Chain Reaction
  • Receptors, CCR / genetics
  • Receptors, CCR / metabolism*
  • Signal Transduction
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • CC chemokine receptor 9
  • Receptors, CCR
  • Glycogen Synthase Kinase 3 beta
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases