Febuxostat ameliorates secondary progressive experimental autoimmune encephalomyelitis by restoring mitochondrial energy production in a GOT2-dependent manner

PLoS One. 2017 Nov 6;12(11):e0187215. doi: 10.1371/journal.pone.0187215. eCollection 2017.

Abstract

Oxidative stress and mitochondrial dysfunction are important determinants of neurodegeneration in secondary progressive multiple sclerosis (SPMS). We previously showed that febuxostat, a xanthine oxidase inhibitor, ameliorated both relapsing-remitting and secondary progressive experimental autoimmune encephalomyelitis (EAE) by preventing neurodegeneration in mice. In this study, we investigated how febuxostat protects neuron in secondary progressive EAE. A DNA microarray analysis revealed that febuxostat treatment increased the CNS expression of several mitochondria-related genes in EAE mice, most notably including GOT2, which encodes glutamate oxaloacetate transaminase 2 (GOT2). GOT2 is a mitochondrial enzyme that oxidizes glutamate to produce α-ketoglutarate for the Krebs cycle, eventually leading to the production of adenosine triphosphate (ATP). Whereas GOT2 expression was decreased in the spinal cord during the chronic progressive phase of EAE, febuxostat-treated EAE mice showed increased GOT2 expression. Moreover, febuxostat treatment of Neuro2a cells in vitro ameliorated ATP exhaustion induced by rotenone application. The ability of febuxostat to preserve ATP production in the presence of rotenone was significantly reduced by GOT2 siRNA. GOT2-mediated ATP synthesis may be a pivotal mechanism underlying the protective effect of febuxostat against neurodegeneration in EAE. Accordingly, febuxostat may also have clinical utility as a disease-modifying drug in SPMS.

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Aspartate Aminotransferase, Mitochondrial / genetics
  • Aspartate Aminotransferase, Mitochondrial / metabolism*
  • Cell Line
  • Encephalomyelitis, Autoimmune, Experimental / enzymology
  • Encephalomyelitis, Autoimmune, Experimental / prevention & control*
  • Energy Metabolism
  • Febuxostat / pharmacology
  • Febuxostat / therapeutic use*
  • Humans
  • Mice
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Neurons / drug effects
  • Neurons / metabolism
  • Oligonucleotide Array Sequence Analysis
  • Rotenone / pharmacology
  • Xanthine Oxidase / antagonists & inhibitors

Substances

  • Rotenone
  • Febuxostat
  • Adenosine Triphosphate
  • Xanthine Oxidase
  • Aspartate Aminotransferase, Mitochondrial

Grants and funding

This study is supported in part by the Practical Research Project for Rare/Intractable Diseases of the Japan Agency for Medical Research and Development (AMED), JSPS KAKENHI (grant numbers JP26461293 and JP15K09339), and a Health and Labor Sciences Research Grant for Rare and Intractable Diseases from the Ministry of Health, Labor and Welfare of Japan. Teijin Pharma Ltd. provided support in the form of salaries for authors T.S. and M.T., but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the 'author contributions' section.