NADPH oxidase activation and 4-hydroxy-2-nonenal/aquaporin-4 adducts as possible new players in oxidative neuronal damage presents in drug-resistant epilepsy

Biochim Biophys Acta. 2015 Mar;1852(3):507-19. doi: 10.1016/j.bbadis.2014.11.016. Epub 2014 Nov 22.

Abstract

A correlation between epilepsy and cellular redox imbalance has been suggested, although the mechanism by which oxidative stress (OS) can be implicated in this disorder is not clear. In the present study several oxidative stress markers and enzymes involved in OS have been determined. In particular, we examined the levels of 4-hydroxy-2-nonenal protein adducts (HNE-PA), a by-product of lipid peroxidation, and the activation of NADPH oxidase 2 (NOX2), as cellular source of superoxide (O(2)(-)), in surgically resected epileptic tissue from drug-resistant patients (N=50). In addition, we investigated whether oxidative-mediated protein damage can affect aquaporin-4 (AQP4), a water channel implicated in brain excitability and epilepsy. Results showed high levels of HNE-PA in epileptic hippocampus, in both neurons and glial cells and cytoplasmic positivity for p47(phox) and p67(phox) suggesting NOX2 activation. Interestingly, in epileptic tissue immunohistochemical localization of AQP4 was identified not only in perivascular astrocytic endfeet, but also in neurons. Nevertheless, negativity for AQP4 was observed in neurons in degeneration. Of note, HNE-mediated post-translational modifications of AQP4 were increased in epileptic tissues and double immunofluorescence clearly demonstrated co-localization of AQP4 and HNE-PA in epileptic hippocampal structures. The idea is that sudden, disorderly, and excessive neuronal discharges activates NOX2 with O(2)(-) production, leading to lipid peroxidation. The resulting generation of HNE targets AQP4, affecting water and ion balance. Therefore, we suggest that seizure induces oxidative damage as well as neuronal loss, thereby promoting neuronal hyperexcitability, also affecting water and ion balance by AQP4 modulation, and thus generating a vicious cycle.

Keywords: 4-Hydroxy-2-nonenal; Aquaporin-4; Drug-resistant epilepsy; Matrix metalloproteinase; NADPH oxidase.

MeSH terms

  • Adolescent
  • Adult
  • Aldehydes / metabolism*
  • Aquaporin 4 / metabolism*
  • Astrocytes / metabolism
  • Astrocytes / pathology
  • Child, Preschool
  • Drug Resistance*
  • Enzyme Activation
  • Epilepsy / mortality*
  • Epilepsy / pathology
  • Female
  • Hippocampus / metabolism
  • Hippocampus / pathology
  • Humans
  • Lipid Peroxidation
  • Male
  • Membrane Glycoproteins / metabolism*
  • NADPH Oxidase 2
  • NADPH Oxidases / metabolism*
  • Neurodegenerative Diseases / metabolism*
  • Neurodegenerative Diseases / pathology
  • Neurons / metabolism
  • Neurons / pathology
  • Superoxides / metabolism
  • Water-Electrolyte Balance

Substances

  • AQP4 protein, human
  • Aldehydes
  • Aquaporin 4
  • Membrane Glycoproteins
  • Superoxides
  • CYBB protein, human
  • NADPH Oxidase 2
  • NADPH Oxidases
  • 4-hydroxy-2-nonenal