Axon guidance of sympathetic neurons to cardiomyocytes by glial cell line-derived neurotrophic factor (GDNF)

PLoS One. 2013 Jul 3;8(7):e65202. doi: 10.1371/journal.pone.0065202. Print 2013.

Abstract

Molecular signaling of cardiac autonomic innervation is an unresolved issue. Here, we show that glial cell line-derived neurotrophic factor (GDNF) promotes cardiac sympathetic innervation in vitro and in vivo. In vitro, ventricular myocytes (VMs) and sympathetic neurons (SNs) isolated from neonatal rat ventricles and superior cervical ganglia were cultured at a close distance. Then, morphological and functional coupling between SNs and VMs was assessed in response to GDNF (10 ng/ml) or nerve growth factor (50 ng/ml). As a result, fractions of neurofilament-M-positive axons and synapsin-I-positive area over the surface of VMs were markedly increased with GDNF by 9-fold and 25-fold, respectively, compared to control without neurotrophic factors. Pre- and post-synaptic stimulation of β1-adrenergic receptors (BAR) with nicotine and noradrenaline, respectively, resulted in an increase of the spontaneous beating rate of VMs co-cultured with SNs in the presence of GDNF. GDNF overexpressing VMs by adenovirus vector (AdGDNF-VMs) attracted more axons from SNs compared with mock-transfected VMs. In vivo, axon outgrowth toward the denervated myocardium in adult rat hearts after cryoinjury was also enhanced significantly by adenovirus-mediated GDNF overexpression. GDNF acts as a potent chemoattractant for sympathetic innervation of ventricular myocytes, and is a promising molecular target for regulation of cardiac function in diseased hearts.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autonomic Denervation
  • Axons / drug effects*
  • Axons / metabolism
  • Coculture Techniques
  • Excitation Contraction Coupling / physiology
  • Ganglia, Sympathetic / drug effects*
  • Ganglia, Sympathetic / metabolism
  • Glial Cell Line-Derived Neurotrophic Factor / metabolism
  • Glial Cell Line-Derived Neurotrophic Factor / pharmacology*
  • Male
  • Myocytes, Cardiac / metabolism*
  • Nerve Growth Factor / pharmacology
  • Neuromuscular Junction / metabolism
  • Neuromuscular Junction / ultrastructure
  • Neurons / drug effects*
  • Neurons / metabolism
  • Rats
  • Receptors, Adrenergic, beta-1 / metabolism
  • Sympathetic Fibers, Postganglionic / drug effects*
  • Sympathetic Fibers, Postganglionic / growth & development*

Substances

  • Glial Cell Line-Derived Neurotrophic Factor
  • Receptors, Adrenergic, beta-1
  • Nerve Growth Factor

Grants and funding

This work was supported in part by: 1. Japan Society for the Promotion of Science (1) (http://www.jsps.go.jp/english/e-grants/index.html) 2. The Ministry of Education, Culture, Sports, Science and Technology, Japan (1) (http://www.mext.go.jp/english/) 3. The Suzuken Memorial Foundation (1) (http://www.suzukenzaidan.or.jp/index.html) 4. The TERUMO Research Fellowship (1) (https://www.terumozaidan.or.jp/english/) The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. No additional external funding received for this study.