Loss of One Engrailed1 Allele Enhances Induced α-Synucleinopathy

J Parkinsons Dis. 2019;9(2):315-326. doi: 10.3233/JPD-191590.

Abstract

Background: Parkinson's disease (PD) is a synucleinopathy that has multiple neuropathological characteristics, with nigrostriatal dopamine system degeneration being a core feature. Current models of PD pathology typically fail to recapitulate several attributes of the pathogenic process and neuropathology. We aimed to define the effects of combining a mouse model exhibiting multiple PD-like changes with intrastriatal injections of α-synuclein (α-syn) pre-formed fibril (PFFs) aggregates. We employed the heterozygous Engrailed 1 (En1+/-) mouse that features several pathophysiological hallmarks of clinical PD.

Objective: To test the hypothesis that the neuropathological changes in the En1+/- mice will promote formation of α-syn aggregates following intrastriatal injections of pathogenic human α-syn PFFs.

Methods: We unilaterally injected PFFs into the striata of 1-month-old En1+/- and control wild-type mice and euthanized animals at 3 months for post-mortem analysis.

Results: Using immunohistochemistry and unbiased stereology, we established that PFF-injected En1+/- mice exhibited a near-threefold increase in pS129-α-syn-positive neurons in the substantia nigra compared to PFF-injected wild-type mice. The PFF-injected En1+/- mice also displayed significant increases in pS129-α-syn-positive neurons in the amygdala and ventral tegmental area; regions of known PD pathology with projections to the striatum. Additionally, we observed amplified pS129-α-syn-positive aggregation in En1+/- mice in multiple cortical regions.

Conclusions: Following intrastriatal injection of PFFs, absence of an En1 allele leads to additional aggregation of pathological α-syn, potentially due to En1-loss mediated nigrostriatal impairment. We propose that further development of this double-hit model could result in a PD mouse model that predicts which experimental therapies will be effective in PD.

Keywords: Parkinson’s disease; engrailed; misfolded proteins; mouse models; neurodegeneration; propagation; proteinopathy; α-Synuclein.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Amygdala / drug effects
  • Amygdala / metabolism
  • Amygdala / pathology
  • Animals
  • Brain / drug effects
  • Brain / metabolism*
  • Brain / pathology
  • Cerebral Cortex / drug effects
  • Cerebral Cortex / metabolism
  • Cerebral Cortex / pathology
  • Gene Knockdown Techniques
  • Homeodomain Proteins / genetics*
  • Humans
  • Immunohistochemistry
  • Mice
  • Neostriatum / drug effects
  • Neostriatum / metabolism
  • Neostriatum / pathology
  • Parkinson Disease / genetics
  • Parkinson Disease / metabolism
  • Parkinson Disease / pathology
  • Protein Aggregates*
  • Protein Aggregation, Pathological / genetics*
  • Protein Aggregation, Pathological / metabolism
  • Protein Aggregation, Pathological / pathology
  • Substantia Nigra / drug effects
  • Substantia Nigra / metabolism
  • Substantia Nigra / pathology
  • Synucleinopathies / genetics*
  • Synucleinopathies / metabolism
  • Synucleinopathies / pathology
  • Ventral Tegmental Area / drug effects
  • Ventral Tegmental Area / metabolism
  • Ventral Tegmental Area / pathology
  • alpha-Synuclein / pharmacology*

Substances

  • En1 protein, mouse
  • Homeodomain Proteins
  • Protein Aggregates
  • alpha-Synuclein