Involvement of caspase activation in azaspiracid-induced neurotoxicity in neocortical neurons

Toxicol Sci. 2010 Apr;114(2):323-34. doi: 10.1093/toxsci/kfp312. Epub 2010 Jan 4.

Abstract

Azaspiracids (AZAs) are a novel group of marine phycotoxins that have been associated with severe human intoxication. We found that AZA-1 exposure increased lactate dehydrogense (LDH) efflux in murine neocortical neurons. AZA-1 also produced nuclear condensation and stimulated caspase-3 activity with an half maximal effective concentration (EC(50)) value of 25.8 nM. These data indicate that AZA-1 triggers neuronal death in neocortical neurons by both necrotic and apoptotic mechanisms. An evaluation of the structure-activity relationships of AZA analogs on LDH efflux and caspase-3 activation demonstrated that the full structure of AZAs was required to produce necrotic or apoptotic cell death. The similar potencies of AZA-1 to stimulate LDH efflux and caspase-3 activation and the parallel structure-activity relationships of azaspiracid analogs in the two assays are consistent with a common molecular target for both responses. To explore the molecular mechanism for AZA-1-induced neurotoxicity, we assessed the influence of AZA-1 on Ca(2+) homeostasis. AZA-1 suppressed spontaneous Ca(2+) oscillations (EC(50) = 445 nM) in neocortical neurons. A distinct structure-activity profile was found for inhibition of Ca(2+) oscillations where both the full structure as well as analogs containing only the FGHI domain attached to a phenyl glycine methyl ester moiety were potent inhibitors. The molecular targets for inhibition of spontaneous Ca(2+) oscillations and neurotoxicity may therefore differ. The caspase protease inhibitor Z-VAD-FMK produced a complete elimination of AZA-1-induced LDH efflux and nuclear condensation in neocortical neurons. Although the molecular target for AZA-induced neurotoxicity remains to be established, these results demonstrate that the observed neurotoxicity is dependent on a caspase signaling pathway.

Publication types

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

MeSH terms

  • Amino Acid Chloromethyl Ketones / pharmacology
  • Animals
  • Apoptosis / drug effects
  • Calcium / metabolism
  • Caspase 3 / biosynthesis*
  • Caspase 3 / drug effects*
  • Caspase Inhibitors
  • Cells, Cultured
  • Cysteine Proteinase Inhibitors / pharmacology
  • Embryo, Mammalian / cytology
  • Embryo, Mammalian / embryology
  • Homeostasis / drug effects
  • Homeostasis / physiology
  • Humans
  • L-Lactate Dehydrogenase / drug effects
  • L-Lactate Dehydrogenase / metabolism
  • Marine Toxins / chemistry
  • Marine Toxins / toxicity*
  • Mice
  • Necrosis / chemically induced
  • Neocortex / cytology
  • Neocortex / embryology
  • Neurons / drug effects*
  • Neurons / metabolism
  • Neurons / pathology
  • Shellfish Poisoning*
  • Signal Transduction / drug effects
  • Spiro Compounds / chemistry
  • Spiro Compounds / toxicity*
  • Structure-Activity Relationship

Substances

  • Amino Acid Chloromethyl Ketones
  • Caspase Inhibitors
  • Cysteine Proteinase Inhibitors
  • Marine Toxins
  • Spiro Compounds
  • azaspiracid
  • benzyloxycarbonylvalyl-alanyl-aspartyl fluoromethyl ketone
  • L-Lactate Dehydrogenase
  • Caspase 3
  • Calcium