Beclin 1 gene transfer activates autophagy and ameliorates the neurodegenerative pathology in alpha-synuclein models of Parkinson's and Lewy body diseases

J Neurosci. 2009 Oct 28;29(43):13578-88. doi: 10.1523/JNEUROSCI.4390-09.2009.

Abstract

Accumulation of the synaptic protein alpha-synuclein (alpha-syn) is a hallmark of Parkinson's disease (PD) and Lewy body disease (LBD), a heterogeneous group of disorders with dementia and parkinsonism, where Alzheimer's disease and PD interact. Accumulation of alpha-syn in these patients might be associated with alterations in the autophagy pathway. Therefore, we postulate that delivery of beclin 1, a regulator of the autophagy pathway, might constitute a strategy toward developing a therapy for LBD/PD. Overexpression of alpha-syn from lentivirus transduction in a neuronal cell line resulted in lysosomal accumulation and alterations in autophagy. Coexpression of beclin 1 activated autophagy, reduced accumulation of alpha-syn, and ameliorated associated neuritic alterations. The effects of beclin 1 overexpression on LC3 and alpha-syn accumulation were partially blocked by 3-MA and completely blocked by bafilomycin A1. In contrast, rapamycin enhanced the effects of beclin 1. To evaluate the potential effects of activating autophagy in vivo, a lentivirus expressing beclin 1 was delivered to the brain of a alpha-syn transgenic mouse. Neuropathological analysis demonstrated that beclin 1 injections ameliorated the synaptic and dendritic pathology in the tg mice and reduced the accumulation of alpha-syn in the limbic system without any significant deleterious effects. This was accompanied by enhanced lysosomal activation and reduced alterations in the autophagy pathway. Thus, beclin 1 plays an important role in the intracellular degradation of alpha-syn either directly or indirectly through the autophagy pathway and may present a novel therapeutic target for LBD/PD.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins / genetics*
  • Apoptosis Regulatory Proteins / metabolism*
  • Autophagy / physiology*
  • Beclin-1
  • Brain / cytology
  • Brain / pathology
  • Brain / physiopathology
  • Cell Line, Tumor
  • Disease Models, Animal
  • Gene Transfer Techniques
  • Humans
  • Lewy Body Disease / pathology
  • Lewy Body Disease / physiopathology*
  • Mice
  • Mice, Transgenic
  • Nerve Degeneration / pathology
  • Nerve Degeneration / physiopathology*
  • Neurons / cytology
  • Neurons / pathology
  • Neurons / physiology
  • Parkinson Disease / pathology
  • Parkinson Disease / physiopathology*
  • Rats
  • Signal Transduction
  • alpha-Synuclein / genetics
  • alpha-Synuclein / metabolism*

Substances

  • Apoptosis Regulatory Proteins
  • Beclin-1
  • Becn1 protein, mouse
  • alpha-Synuclein