Exploiting functional domains of GRK2/3 to alter the competitive balance of pro- and anticontractile signaling in airway smooth muscle

FASEB J. 2014 Feb;28(2):956-65. doi: 10.1096/fj.13-240226. Epub 2013 Oct 16.

Abstract

To clarify the potential utility of targeting GRK2/3-mediated desensitization as a means of manipulating airway smooth muscle (ASM) contractile state, we assessed the specificity of GRK2/3 regulation of procontractile and relaxant G-protein-coupled receptors in ASM. Functional domains of GRK2/3 were stably expressed, or siRNA-mediated GRK2/3 knockdown was performed, in human ASM cultures, and agonist-induced signaling was assessed. Regulation of contraction of murine tracheal rings expressing GRK2 C terminus was also assessed. GRK2/3 knockdown or expression of the GRK2 C terminus caused a significant (∼ 30-90%) increase in maximal β-agonist and histamine [phosphoinositide (PI) hydrolysis] signaling, without affecting the calculated EC50. GRK2 C-terminal expression did not affect signaling by methacholine, thrombin, or LTD4. Expression of the GRK2 N terminus or kinase-dead holo-GRK2 diminished (∼ 30-70%) both PI hydrolysis and Ca(2+) mobilization by every Gq-coupled receptor examined. Under conditions of GRK2 C-terminal expression, β-agonist inhibition of methacholine-stimulated PI hydrolysis was greater. Finally, transgenic expression of the GRK2 C terminus in murine ASM enabled ∼ 30-50% greater β-agonist-mediated relaxation of methacholine-induced contraction. Collectively these data demonstrate the relative selectivity of GRKs for the β2AR in ASM and the ability to exploit GRK2/3 functional domains to render ASM hyporesponsive to contractile agents while increasing responsiveness to bronchodilating β-agonist.

Keywords: G-protein-coupled receptor; asthma; bronchodilation; desensitization; β-agonist.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Calcium / metabolism
  • Cyclic AMP / metabolism
  • G-Protein-Coupled Receptor Kinase 2 / chemistry
  • G-Protein-Coupled Receptor Kinase 2 / metabolism*
  • G-Protein-Coupled Receptor Kinase 3 / chemistry
  • G-Protein-Coupled Receptor Kinase 3 / metabolism*
  • Humans
  • Muscle, Smooth / metabolism*
  • RNA, Small Interfering
  • Receptors, G-Protein-Coupled / metabolism
  • Respiratory System / cytology
  • Signal Transduction / physiology

Substances

  • RNA, Small Interfering
  • Receptors, G-Protein-Coupled
  • Cyclic AMP
  • G-Protein-Coupled Receptor Kinase 3
  • GRK2 protein, human
  • GRK3 protein, human
  • G-Protein-Coupled Receptor Kinase 2
  • Calcium