Ethanol triggers neural crest apoptosis through the selective activation of a pertussis toxin-sensitive G protein and a phospholipase Cbeta-dependent Ca2+ transient

Alcohol Clin Exp Res. 2005 Jul;29(7):1237-46. doi: 10.1097/01.alc.0000172460.05756.d9.

Abstract

Background: Alcohol is a potent neurotoxin that triggers the selective apoptosis of neuronal populations in the developing fetus. For neural crest cells, clinically relevant ethanol levels (0.3%) rapidly elicit a phospholipase C (PLC)-dependent intracellular Ca2+ transient that is sufficient to activate apoptosis. We investigated the biochemical origins of this Ca2+ transient.

Methods: Three somite chick embryos (stage 8-) were pretreated with agonists and antagonists of PLC signaling pathways before ethanol challenge. The resulting intracellular Ca2+ release was quantified using Fluo-3; apoptosis was assessed using vital dyes.

Results: Pretreatment of embryos with PLC antagonists U73122 or ET-18-OCH3 confirmed that a phosphoinositide-specific PLC was required for both the ethanol-dependent Ca2+ transient and subsequent cell death. Ethanol rapidly elevated intracellular inositol-1,4,5-trisphosphate [Ins(1,4,5)P3] levels in the rostral portion of the embryo that contains neural crest progenitors. The Ins(1,4,5)P3 receptor antagonist xestospongin C blocked the appearance of the ethanol-dependent Ca2+ transient. Pretreatment with the pan-Galpha protein antagonist GDPbetaS, but not with the tyrosine kinase antagonist genistein, suppressed ethanol's ability to elicit the Ca2+ transient, suggesting that a rise in PLC activity and Ins(1,4,5)P3 concentration originates from stimulation of heterotrimeric G proteins. To probe the identity of this G protein, embryos were treated with G protein antagonists. Pertussis toxin and NF023 suppressed the ethanol-induced Ca2+ transient and subsequent neural crest apoptosis, whereas suramin was weakly inhibitory. C3 exoenzyme was embryolethal over a wide concentration range, consistent with suggestions that Rho family GTPases participate in neural crest development. Galphai2 was identified by immunostaining in the neural crest cells.

Conclusion: We propose a role for Galphai/o protein activation and subsequent interaction of Gbetagamma with PLCbeta in mediating the proapoptotic effects of ethanol upon the developing neural crest.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / drug effects*
  • Calcium / metabolism*
  • Chick Embryo
  • Disease Models, Animal
  • Enzyme Activation / drug effects
  • Estrenes / pharmacology
  • Ethanol / toxicity*
  • Female
  • Fetal Alcohol Spectrum Disorders / physiopathology*
  • GTP-Binding Proteins / metabolism*
  • Humans
  • Isoenzymes / physiology*
  • Neural Crest / drug effects*
  • Neural Crest / pathology
  • Pertussis Toxin / pharmacology*
  • Phospholipase C beta
  • Phospholipid Ethers / pharmacology
  • Pregnancy
  • Pyrrolidinones / pharmacology
  • Type C Phospholipases / physiology*

Substances

  • Estrenes
  • Isoenzymes
  • Phospholipid Ethers
  • Pyrrolidinones
  • 1-(6-((3-methoxyestra-1,3,5(10)-trien-17-yl)amino)hexyl)-1H-pyrrole-2,5-dione
  • edelfosine
  • Ethanol
  • Pertussis Toxin
  • Type C Phospholipases
  • Phospholipase C beta
  • GTP-Binding Proteins
  • Calcium