Pur-alpha regulates cytoplasmic stress granule dynamics and ameliorates FUS toxicity

Acta Neuropathol. 2016 Apr;131(4):605-20. doi: 10.1007/s00401-015-1530-0. Epub 2016 Jan 4.

Abstract

Amyotrophic lateral sclerosis is characterized by progressive loss of motor neurons in the brain and spinal cord. Mutations in several genes, including FUS, TDP43, Matrin 3, hnRNPA2 and other RNA-binding proteins, have been linked to ALS pathology. Recently, Pur-alpha, a DNA/RNA-binding protein was found to bind to C9orf72 repeat expansions and could possibly play a role in the pathogenesis of ALS. When overexpressed, Pur-alpha mitigates toxicities associated with Fragile X tumor ataxia syndrome (FXTAS) and C9orf72 repeat expansion diseases in Drosophila and mammalian cell culture models. However, the function of Pur-alpha in regulating ALS pathogenesis has not been fully understood. We identified Pur-alpha as a novel component of cytoplasmic stress granules (SGs) in ALS patient cells carrying disease-causing mutations in FUS. When cells were challenged with stress, we observed that Pur-alpha co-localized with mutant FUS in ALS patient cells and became trapped in constitutive SGs. We also found that FUS physically interacted with Pur-alpha in mammalian neuronal cells. Interestingly, shRNA-mediated knock down of endogenous Pur-alpha significantly reduced formation of cytoplasmic stress granules in mammalian cells suggesting that Pur-alpha is essential for the formation of SGs. Furthermore, ectopic expression of Pur-alpha blocked cytoplasmic mislocalization of mutant FUS and strongly suppressed toxicity associated with mutant FUS expression in primary motor neurons. Our data emphasizes the importance of stress granules in ALS pathogenesis and identifies Pur-alpha as a novel regulator of SG dynamics.

Keywords: ALS; Amyotrophic lateral sclerosis; C9orf72; FUS; Motor neuron diseases; Neurodegeneration; Primary motor neurons; Pur-alpha; RNA-binding proteins; Stress granules; TDP-43.

MeSH terms

  • Amyotrophic Lateral Sclerosis / pathology
  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Arsenites / pharmacology
  • Brain / cytology
  • Carrier Proteins / metabolism
  • Cells, Cultured
  • Cytoplasmic Granules / drug effects
  • Cytoplasmic Granules / metabolism*
  • DNA Helicases
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Doxycycline / pharmacology
  • Embryo, Mammalian
  • Enzyme Inhibitors / pharmacology
  • Female
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics*
  • Humans
  • Male
  • Microtubule-Associated Proteins / metabolism
  • Motor Neurons / metabolism*
  • Poly-ADP-Ribose Binding Proteins
  • RNA Helicases
  • RNA Recognition Motif Proteins
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • RNA-Binding Protein FUS / genetics
  • RNA-Binding Protein FUS / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Sodium Compounds / pharmacology
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • Anti-Bacterial Agents
  • Arsenites
  • Carrier Proteins
  • DNA-Binding Proteins
  • Enzyme Inhibitors
  • MAP2 protein, human
  • Microtubule-Associated Proteins
  • PURA protein, human
  • Poly-ADP-Ribose Binding Proteins
  • RNA Recognition Motif Proteins
  • RNA, Small Interfering
  • RNA-Binding Protein FUS
  • Sodium Compounds
  • Transcription Factors
  • sodium arsenite
  • DNA Helicases
  • G3BP1 protein, human
  • RNA Helicases
  • Doxycycline