β1-adrenergic receptor and sphingosine-1-phosphate receptor 1 (S1PR1) reciprocal downregulation influences cardiac hypertrophic response and progression to heart failure: protective role of S1PR1 cardiac gene therapy

Circulation. 2013 Oct 8;128(15):1612-22. doi: 10.1161/CIRCULATIONAHA.113.002659. Epub 2013 Aug 22.

Abstract

Background: The sphingosine-1-phosphate receptor 1 (S1PR1) and β1-adrenergic receptor (β1AR) are G-protein-coupled receptors expressed in the heart. These 2 receptors have opposing actions on adenylyl cyclase because of differential G-protein coupling. Importantly, both of these receptors can be regulated by the actions of G-protein-coupled receptor kinase-2, which triggers desensitization and downregulation processes. Although classic signaling paradigms suggest that simultaneous activation of β1ARs and S1PR1s in a myocyte would simply result in opposing action on cAMP production, in this report we have uncovered a direct interaction between these 2 receptors, with regulatory involvement of G-protein-coupled receptor kinase-2.

Methods and results: In HEK (human embryonic kidney) 293 cells overexpressing both β1AR and S1PR1, we demonstrated that β1AR downregulation can occur after stimulation with sphingosine-1-phosphate (an S1PR1 agonist), whereas S1PR1 downregulation can be triggered by isoproterenol (a β-adrenergic receptor agonist) treatment. This cross talk between these 2 distinct G-protein-coupled receptors appears to have physiological significance, because they interact and show reciprocal regulation in mouse hearts undergoing chronic β-adrenergic receptor stimulation and in a rat model of postischemic heart failure.

Conclusions: We demonstrate that restoration of cardiac plasma membrane levels of S1PR1 produces beneficial effects that counterbalance the deleterious β1AR overstimulation in heart failure.

Keywords: genetic therapy; heart failure; hypertrophy; receptors, adrenergic, beta; signal transduction.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cardiomegaly / physiopathology
  • Cardiomegaly / therapy
  • Disease Models, Animal
  • Disease Progression
  • Down-Regulation / physiology
  • Genetic Therapy / methods*
  • Green Fluorescent Proteins / genetics
  • HEK293 Cells
  • Heart Failure / physiopathology*
  • Heart Failure / therapy*
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Myoblasts, Cardiac / cytology
  • Myocardial Infarction / physiopathology
  • Myocardial Infarction / therapy
  • Rats
  • Rats, Inbred WKY
  • Receptor Cross-Talk / physiology
  • Receptors, Adrenergic, beta-1 / genetics*
  • Receptors, Adrenergic, beta-1 / metabolism
  • Receptors, Lysosphingolipid / genetics*
  • Receptors, Lysosphingolipid / metabolism
  • Sphingosine-1-Phosphate Receptors

Substances

  • Receptors, Adrenergic, beta-1
  • Receptors, Lysosphingolipid
  • S1pr1 protein, mouse
  • Sphingosine-1-Phosphate Receptors
  • Green Fluorescent Proteins