Neurodegeneration in a transgenic mouse model of multiple system atrophy is associated with altered expression of oligodendroglial-derived neurotrophic factors

J Neurosci. 2010 May 5;30(18):6236-46. doi: 10.1523/JNEUROSCI.0567-10.2010.

Abstract

Multiple system atrophy (MSA) is a neurodegenerative disorder characterized by striatonigral degeneration and olivo-pontocerebellar atrophy. Neuronal degeneration is accompanied by primarily oligodendrocytic accumulation of alpha-synuclein (alphasyn) as opposed to the neuronal inclusions more commonly found in other alpha-synucleinopathies such as Parkinson's disease. It is unclear how alphasyn accumulation in oligodendrocytes may lead to the extensive neurodegeneration observed in MSA; we hypothesize that the altered expression of oligodendrocyte-derived neurotrophic factors by alphasyn may be involved. In this context, the expression of a number neurotrophic factors reportedly expressed by oligodendrocytes [glial-derived neurotrophic factor (GDNF), brain-derived neurotrophic factor (BDNF), and insulin-like growth factor 1 (IGF-1), as well as basic fibroblast growth factor 2 (bFGF2), reportedly astrocyte derived] were examined in transgenic mouse models expressing human alphasyn (halphasyn) under the control of either neuronal (PDGFbeta or mThy1) or oligodendrocytic (MBP) promoters. Although protein levels of BDNF and IGF-1 were altered in all the alphasyn transgenic mice regardless of promoter type, a specific decrease in GDNF protein expression was observed in the MBP-halphasyn transgenic mice. Intracerebroventricular infusion of GDNF improved behavioral deficits and ameliorated neurodegenerative pathology in the MBP-halphasyn transgenic mice. Consistent with the studies in the MBP-halphasyn transgenic mice, analysis of GDNF expression levels in human MSA samples demonstrated a decrease in the white frontal cortex and to a lesser degree in the cerebellum compared with controls. These results suggest a mechanism in which alphasyn expression in oligodendrocytes impacts on the trophic support provided by these cells for neurons, perhaps contributing to neurodegeneration.

Publication types

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

MeSH terms

  • Aged
  • Animals
  • Behavior, Animal / drug effects
  • Brain / metabolism
  • Brain / pathology
  • Disease Models, Animal*
  • Female
  • Glial Cell Line-Derived Neurotrophic Factor / administration & dosage
  • Humans
  • Injections, Intraventricular
  • Male
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • Multiple System Atrophy* / drug therapy
  • Multiple System Atrophy* / genetics
  • Multiple System Atrophy* / metabolism
  • Multiple System Atrophy* / pathology
  • Nerve Degeneration / drug therapy*
  • Nerve Degeneration / pathology
  • Nerve Fibers, Myelinated / metabolism
  • Nerve Growth Factors / metabolism*
  • Neurons / drug effects
  • Neurons / metabolism
  • Neurons / pathology
  • Oligodendroglia / drug effects
  • Oligodendroglia / metabolism*
  • Promoter Regions, Genetic
  • alpha-Synuclein / genetics

Substances

  • Glial Cell Line-Derived Neurotrophic Factor
  • Nerve Growth Factors
  • alpha-Synuclein