Dual targeting of brain region-specific kinases potentiates neurological rescue in Spinocerebellar ataxia type 1

EMBO J. 2021 Apr 1;40(7):e106106. doi: 10.15252/embj.2020106106. Epub 2021 Mar 11.

Abstract

A critical question in neurodegeneration is why the accumulation of disease-driving proteins causes selective neuronal loss despite their brain-wide expression. In Spinocerebellar ataxia type 1 (SCA1), accumulation of polyglutamine-expanded Ataxin-1 (ATXN1) causes selective degeneration of cerebellar and brainstem neurons. Previous studies revealed that inhibiting Msk1 reduces phosphorylation of ATXN1 at S776 as well as its levels leading to improved cerebellar function. However, there are no regulators that modulate ATXN1 in the brainstem-the brain region whose pathology is most closely linked to premature death. To identify new regulators of ATXN1, we performed genetic screens and identified a transcription factor-kinase axis (ZBTB7B-RSK3) that regulates ATXN1 levels. Unlike MSK1, RSK3 is highly expressed in the human and mouse brainstems where it regulates Atxn1 by phosphorylating S776. Reducing Rsk3 rescues brainstem-associated pathologies and deficits, and lowering Rsk3 and Msk1 together improves cerebellar and brainstem function in an SCA1 mouse model. Our results demonstrate that selective vulnerability of brain regions in SCA1 is governed by region-specific regulators of ATXN1, and targeting multiple regulators could rescue multiple degenerating brain areas.

Keywords: Ataxin-1; MSK1; RSK3; Spinocerebellar ataxia type 1; selective vulnerability.

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

  • Animals
  • Ataxin-1 / genetics
  • Ataxin-1 / metabolism
  • Brain Stem / metabolism*
  • Cell Line, Tumor
  • Cells, Cultured
  • Cerebellum / metabolism*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Drosophila melanogaster
  • HEK293 Cells
  • Humans
  • Mice
  • Phosphorylation
  • Protein Stability
  • Ribosomal Protein S6 Kinases, 90-kDa / genetics
  • Ribosomal Protein S6 Kinases, 90-kDa / metabolism*
  • Spinocerebellar Ataxias / genetics
  • Spinocerebellar Ataxias / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • Ataxin-1
  • Atxn1 protein, mouse
  • DNA-Binding Proteins
  • Transcription Factors
  • Zbtb7b protein, mouse
  • Ribosomal Protein S6 Kinases, 90-kDa
  • mitogen and stress-activated protein kinase 1
  • ribosomal protein S6 kinase, 90kDa, polypeptide 3

Associated data

  • GEO/GSE151276