Indirect Negative Effect of Mutant Ataxin-1 on Short- and Long-Term Synaptic Plasticity in Mouse Models of Spinocerebellar Ataxia Type 1

Cells. 2022 Jul 20;11(14):2247. doi: 10.3390/cells11142247.

Abstract

Spinocerebellar ataxia type 1 (SCA1) is an intractable progressive neurodegenerative disease that leads to a range of movement and motor defects and is eventually lethal. Purkinje cells (PC) are typically the first to show signs of degeneration. SCA1 is caused by an expansion of the polyglutamine tract in the ATXN1 gene and the subsequent buildup of mutant Ataxin-1 protein. In addition to its toxicity, mutant Ataxin-1 protein interferes with gene expression and signal transduction in cells. Recently, it is evident that ATXN1 is not only expressed in neurons but also in glia, however, it is unclear the extent to which either contributes to the overall pathology of SCA1. There are various ways to model SCA1 in mice. Here, functional deficits at cerebellar synapses were investigated in two mouse models of SCA1 in which mutant ATXN1 is either nonspecifically expressed in all cell types of the cerebellum (SCA1 knock-in (KI)), or specifically in Bergmann glia with lentiviral vectors expressing mutant ATXN1 under the control of the astrocyte-specific GFAP promoter. We report impairment of motor performance in both SCA1 models. In both cases, prominent signs of astrocytosis were found using immunohistochemistry. Electrophysiological experiments revealed alteration of presynaptic plasticity at synapses between parallel fibers and PCs, and climbing fibers and PCs in SCA1 KI mice, which is not observed in animals expressing mutant ATXN1 solely in Bergmann glia. In contrast, short- and long-term synaptic plasticity was affected in both SCA1 KI mice and glia-targeted SCA1 mice. Thus, non-neuronal mechanisms may underlie some aspects of SCA1 pathology in the cerebellum. By combining the outcomes of our current work with our previous data from the B05 SCA1 model, we further our understanding of the mechanisms of SCA1.

Keywords: Bergmann glia; DSE; LTD; PPD; PPF; Purkinje cells; spinocerebellar ataxia type 1; synaptic plasticity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ataxin-1 / genetics
  • Ataxin-1 / metabolism
  • Disease Models, Animal
  • Mice
  • Mice, Transgenic
  • Neuronal Plasticity
  • Purkinje Cells
  • Spinocerebellar Ataxias* / genetics
  • Spinocerebellar Ataxias* / pathology

Substances

  • Ataxin-1
  • Atxn1 protein, mouse

Grants and funding

The study was funded by the joint grant of Russian Foundation for Basic Research, Krasnoyarsk Territory and Krasnoyarsk Regional Fund of Science, 20-415-242905. Work at the Baltic Federal University was performed within the context of the “Priority 2030” project. O.I.M. and S.K. acknowledge funding from the Russian Science Foundation grant 21-515-53007.