Arsenic inhibits neurite outgrowth by inhibiting the LKB1-AMPK signaling pathway

Environ Health Perspect. 2010 May;118(5):627-34. doi: 10.1289/ehp.0901510.

Abstract

Background: Arsenic (As) is an environmental pollutant that induces numerous pathological effects, including neurodevelopmental disorders.

Objectives and methods: We evaluated the role of the LKB1-AMPK pathway in As-induced developmental neurotoxicity using Neuro-2a (N2a) neuroblastoma cells as a model of developing neurons.

Results: The addition of low concentrations of As (<or= 5 microM) during differentiation caused an inhibitory effect on the neurite outgrowth in N2a cells in the absence of cell death. Activation of adenosine monophosphate-activated kinase (AMPK) induced by retinoic acid in differentiating cells was blocked by As. Pretreatment with the AMPK-specific activator 5-aminoimidazole-4-carboxamide riboside or overexpression of a constitutively active AMPK-alpha1 plasmid reversed As-induced inhibition of neurite outgrowth. The activation of LKB1 (serine/threonine kinase 11), a major AMPK kinase, was also suppressed by As by inhibiting both the phosphorylation and the translocation of LKB1 from nucleus to cytoplasm. Antioxidants, such as N-acetyl cysteine and superoxide dismutase, but not catalase, protected against As-induced inactivation of the LKB1-AMPK pathway and reversed the inhibitory effect of As on neurite outgrowth.

Conclusions: Reduced neurite outgrowth induced by As results from deficient activation of AMPK as a consequence of a lack of activation of LKB1. Oxidative stress induced by As, especially excessive superoxide, plays a critical role in blocking the LKB1-AMPK pathway. Our studies provide insight into the mechanisms underlying As-induced developmental neurotoxicity, which is important for designing a new strategy for protecting children against this neurotoxic substance.

Publication types

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

MeSH terms

  • AMP-Activated Protein Kinase Kinases
  • AMP-Activated Protein Kinases / antagonists & inhibitors*
  • Arsenic / toxicity*
  • Cell Differentiation / drug effects
  • Cell Line
  • Environmental Health
  • Enzyme Inhibitors / toxicity
  • Humans
  • Neurites / drug effects*
  • Neurites / enzymology*
  • Neurites / ultrastructure
  • Neurons / cytology
  • Neurons / drug effects
  • Neurons / metabolism
  • Oxidative Stress / drug effects
  • Protein Serine-Threonine Kinases / antagonists & inhibitors*
  • Reactive Oxygen Species / metabolism
  • Signal Transduction / drug effects
  • Water Pollutants, Chemical / toxicity*

Substances

  • Enzyme Inhibitors
  • Reactive Oxygen Species
  • Water Pollutants, Chemical
  • Protein Serine-Threonine Kinases
  • STK11 protein, human
  • AMP-Activated Protein Kinase Kinases
  • AMP-Activated Protein Kinases
  • Arsenic