Selective α-Synuclein Knockdown in Monoamine Neurons by Intranasal Oligonucleotide Delivery: Potential Therapy for Parkinson's Disease

Mol Ther. 2018 Feb 7;26(2):550-567. doi: 10.1016/j.ymthe.2017.11.015. Epub 2017 Nov 29.

Abstract

Progressive neuronal death in brainstem nuclei and widespread accumulation of α-synuclein are neuropathological hallmarks of Parkinson's disease (PD). Reduction of α-synuclein levels is therefore a potential therapy for PD. However, because α-synuclein is essential for neuronal development and function, α-synuclein elimination would dramatically impact brain function. We previously developed conjugated small interfering RNA (siRNA) sequences that selectively target serotonin (5-HT) or norepinephrine (NE) neurons after intranasal administration. Here, we used this strategy to conjugate inhibitory oligonucleotides, siRNA and antisense oligonucleotide (ASO), with the triple monoamine reuptake inhibitor indatraline (IND), to selectively reduce α-synuclein expression in the brainstem monoamine nuclei of mice after intranasal delivery. Following internalization of the conjugated oligonucleotides in monoamine neurons, reduced levels of endogenous α-synuclein mRNA and protein were found in substantia nigra pars compacta (SNc), ventral tegmental area (VTA), dorsal raphe nucleus (DR), and locus coeruleus (LC). α-Synuclein knockdown by ∼20%-40% did not cause monoaminergic neurodegeneration and enhanced forebrain dopamine (DA) and 5-HT release. Conversely, a modest human α-synuclein overexpression in DA neurons markedly reduced striatal DA release. These results indicate that α-synuclein negatively regulates monoamine neurotransmission and set the stage for the testing of non-viral inhibitory oligonucleotides as disease-modifying agents in α-synuclein models of PD.

Keywords: 5-HT neurotransmission; ASO; DA neurotransmission; Parkinson’s disease; caudate putamen; intranasal administration; prefrontal cortex; siRNA; α-synuclein.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Administration, Intranasal
  • Animals
  • Cells, Cultured
  • Corpus Striatum / metabolism
  • Dopamine / metabolism
  • Dopaminergic Neurons / metabolism*
  • Gene Expression
  • Gene Expression Regulation
  • Gene Knockdown Techniques
  • Gene Transfer Techniques
  • Genetic Therapy
  • Humans
  • Mice
  • Neural Pathways
  • Oligonucleotides / administration & dosage
  • Oligonucleotides / genetics*
  • Parkinson Disease / genetics
  • Parkinson Disease / metabolism
  • Parkinson Disease / therapy
  • Prosencephalon / metabolism
  • RNA Interference
  • RNA, Small Interfering / genetics
  • Serotonin / metabolism
  • Signal Transduction
  • Substantia Nigra / metabolism
  • Substantia Nigra / physiopathology
  • Synaptic Transmission / genetics
  • alpha-Synuclein / genetics*

Substances

  • Oligonucleotides
  • RNA, Small Interfering
  • alpha-Synuclein
  • Serotonin
  • Dopamine