Aldehyde dehydrogenase inhibition as a pathogenic mechanism in Parkinson disease

Proc Natl Acad Sci U S A. 2013 Jan 8;110(2):636-41. doi: 10.1073/pnas.1220399110. Epub 2012 Dec 24.

Abstract

Parkinson disease (PD) is a neurodegenerative disorder particularly characterized by the loss of dopaminergic neurons in the substantia nigra. Pesticide exposure has been associated with PD occurrence, and we previously reported that the fungicide benomyl interferes with several cellular processes potentially relevant to PD pathogenesis. Here we propose that benomyl, via its bioactivated thiocarbamate sulfoxide metabolite, inhibits aldehyde dehydrogenase (ALDH), leading to accumulation of the reactive dopamine metabolite 3,4-dihydroxyphenylacetaldehyde (DOPAL), preferential degeneration of dopaminergic neurons, and development of PD. This hypothesis is supported by multiple lines of evidence. (i) We previously showed in mice the metabolism of benomyl to S-methyl N-butylthiocarbamate sulfoxide, which inhibits ALDH at nanomolar levels. We report here that benomyl exposure in primary mesencephalic neurons (ii) inhibits ALDH and (iii) alters dopamine homeostasis. It induces selective dopaminergic neuronal damage (iv) in vitro in primary mesencephalic cultures and (v) in vivo in a zebrafish system. (vi) In vitro cell loss was attenuated by reducing DOPAL formation. (vii) In our epidemiology study, higher exposure to benomyl was associated with increased PD risk. This ALDH model for PD etiology may help explain the selective vulnerability of dopaminergic neurons in PD and provide a potential mechanism through which environmental toxicants contribute to PD pathogenesis.

Publication types

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

MeSH terms

  • 3,4-Dihydroxyphenylacetic Acid / analogs & derivatives
  • 3,4-Dihydroxyphenylacetic Acid / metabolism
  • Aldehyde Dehydrogenase / antagonists & inhibitors*
  • Animals
  • Benomyl / toxicity*
  • Dopaminergic Neurons / drug effects
  • Dopaminergic Neurons / pathology
  • Flow Cytometry
  • Fungicides, Industrial / toxicity*
  • Humans
  • Logistic Models
  • Mesencephalon / cytology
  • Mitochondria / metabolism
  • Nerve Degeneration / chemically induced
  • Odds Ratio
  • Parkinson Disease / enzymology
  • Parkinson Disease / epidemiology*
  • Parkinson Disease / etiology*
  • Parkinson Disease / physiopathology*
  • Rats
  • Zebrafish

Substances

  • Fungicides, Industrial
  • 3,4-Dihydroxyphenylacetic Acid
  • 3,4-dihydroxyphenylacetaldehyde
  • Aldehyde Dehydrogenase
  • Benomyl