N6-methyladenosine demethylase FTO regulates neuronal oxidative stress via YTHDC1-ATF3 axis in arsenic-induced cognitive dysfunction

J Hazard Mater. 2024 Dec 5:480:135736. doi: 10.1016/j.jhazmat.2024.135736. Epub 2024 Sep 4.

Abstract

Excessive exposure to metals in daily life has been proposed as an environmental risk factor for neurological disorders. Oxidative stress is an inevitable stage involved in the neurotoxic effects induced by metals, nevertheless, the underlying mechanisms are still unclear. In this study, we used arsenic as a representative environmental heavy metal to induce neuronal oxidative stress and demonstrated that both in vitro and in vivo exposure to arsenic significantly increased the level of N6-methyladenosine (m6A) by down-regulating its demethylase FTO. Importantly, the results obtained from FTO transgenic mice and FTO overexpressed/knockout cells indicated that FTO likely regulated neuronal oxidative stress by modulating activating transcription factor 3 (ATF3) in a m6A-dependent manner. We also identified the specific m6A reader protein, YTHDC1, which interacted with ATF3 and thereby affecting its regulatory effects on oxidative stress. To further explore potential intervention strategies, cerebral metabolomics was conducted and we newly identified myo-inositol as a metabolite that exhibited potential in protecting against arsenic-induced oxidative stress and cognitive dysfunction. Overall, these findings provide new insights into the importance of the FTO-ATF3 signaling axis in neuronal oxidative stress from an m6A perspective, and highlight a beneficial metabolite that can counteract the oxidative stress induced by arsenic.

Keywords: Cognitive dysfunction; FTO; M(6)A modification; Neuronal oxidative stress.

MeSH terms

  • Activating Transcription Factor 3* / genetics
  • Activating Transcription Factor 3* / metabolism
  • Adenosine* / analogs & derivatives
  • Adenosine* / metabolism
  • Alpha-Ketoglutarate-Dependent Dioxygenase FTO* / genetics
  • Alpha-Ketoglutarate-Dependent Dioxygenase FTO* / metabolism
  • Animals
  • Arsenic* / toxicity
  • Cognitive Dysfunction* / chemically induced
  • Cognitive Dysfunction* / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neurons* / drug effects
  • Neurons* / metabolism
  • Oxidative Stress* / drug effects
  • Signal Transduction / drug effects

Substances

  • Alpha-Ketoglutarate-Dependent Dioxygenase FTO
  • Activating Transcription Factor 3
  • N-methyladenosine
  • Adenosine
  • FTO protein, mouse
  • Arsenic
  • Atf3 protein, mouse