Inhibition of Microglia-Derived Oxidative Stress by Ciliary Neurotrophic Factor Protects Dopamine Neurons In Vivo from MPP⁺ Neurotoxicity

Int J Mol Sci. 2018 Nov 10;19(11):3543. doi: 10.3390/ijms19113543.

Abstract

We demonstrated that capsaicin (CAP), an agonist of transient receptor potential vanilloid subtype 1 (TRPV1), inhibits microglia activation and microglia-derived oxidative stress in the substantia nigra (SN) of MPP⁺-lesioned rat. However, the detailed mechanisms how microglia-derived oxidative stress is regulated by CAP remain to be determined. Here we report that ciliary neurotrophic factor (CNTF) endogenously produced by CAP-activated astrocytes through TRPV1, but not microglia, inhibits microglial activation and microglia-derived oxidative stress, as assessed by OX-6 and OX-42 immunostaining and hydroethidine staining, respectively, resulting in neuroprotection. The significant increase in levels of CNTF receptor alpha (CNTFRα) expression was evident on microglia in the MPP⁺-lesioned rat SN and the observed beneficial effects of CNTF was abolished by treatment with CNTF receptor neutralizing antibody. It is therefore likely that CNTF can exert its effect via CNTFRα on microglia, which rescues dopamine neurons in the SN of MPP⁺-lesioned rats and ameliorates amphetamine-induced rotations. Immunohistochemical analysis revealed also a significantly increased expression of CNTFRα on microglia in the SN from human Parkinson's disease patients compared with age-matched controls, indicating that these findings may have relevance to the disease. These data suggest that CNTF originated from TRPV1 activated astrocytes may be beneficial to treat neurodegenerative disease associated with neuro-inflammation such as Parkinson's disease.

Keywords: Ciliary neurotrophic factor; Ciliary neurotrophic factor receptor; Microglia; Parkinson’s disease; oxidative stress.

MeSH terms

  • 1-Methyl-4-phenylpyridinium / toxicity*
  • Aged
  • Animals
  • Astrocytes / drug effects
  • Astrocytes / metabolism
  • Astrocytes / pathology
  • Capsaicin / pharmacology
  • Cell Survival / drug effects
  • Ciliary Neurotrophic Factor / pharmacology*
  • Dopaminergic Neurons / drug effects
  • Dopaminergic Neurons / metabolism
  • Dopaminergic Neurons / pathology*
  • Female
  • Gene Knockdown Techniques
  • Humans
  • Male
  • Microglia / drug effects
  • Microglia / metabolism
  • Microglia / pathology*
  • Models, Biological
  • Nerve Degeneration / pathology
  • Neuroprotection / drug effects*
  • Neurotoxicity Syndromes / pathology*
  • Oxidative Stress* / drug effects
  • RNA, Small Interfering / metabolism
  • Rats, Sprague-Dawley
  • Reactive Oxygen Species / metabolism
  • Receptor, Ciliary Neurotrophic Factor / metabolism
  • Substantia Nigra / drug effects
  • Substantia Nigra / metabolism
  • Substantia Nigra / pathology
  • TRPV Cation Channels / metabolism

Substances

  • Ciliary Neurotrophic Factor
  • RNA, Small Interfering
  • Reactive Oxygen Species
  • Receptor, Ciliary Neurotrophic Factor
  • TRPV Cation Channels
  • TRPV1 receptor
  • 1-Methyl-4-phenylpyridinium
  • Capsaicin