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Premature polyadenylation-mediated loss of stathmin-2 is a hallmark of TDP-43-dependent neurodegeneration

Nat Neurosci. 2019 Feb;22(2):180-190. doi: 10.1038/s41593-018-0293-z. Epub 2019 Jan 14.

Abstract

Amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD) are associated with loss of nuclear transactive response DNA-binding protein 43 (TDP-43). Here we identify that TDP-43 regulates expression of the neuronal growth-associated factor stathmin-2. Lowered TDP-43 levels, which reduce its binding to sites within the first intron of stathmin-2 pre-messenger RNA, uncover a cryptic polyadenylation site whose utilization produces a truncated, non-functional mRNA. Reduced stathmin-2 expression is found in neurons trans-differentiated from patient fibroblasts expressing an ALS-causing TDP-43 mutation, in motor cortex and spinal motor neurons from patients with sporadic ALS and familial ALS with GGGGCC repeat expansion in the C9orf72 gene, and in induced pluripotent stem cell (iPSC)-derived motor neurons depleted of TDP-43. Remarkably, while reduction in TDP-43 is shown to inhibit axonal regeneration of iPSC-derived motor neurons, rescue of stathmin-2 expression restores axonal regenerative capacity. Thus, premature polyadenylation-mediated reduction in stathmin-2 is a hallmark of ALS-FTD that functionally links reduced nuclear TDP-43 function to enhanced neuronal vulnerability.

Publication types

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

MeSH terms

  • Amyotrophic Lateral Sclerosis / metabolism
  • Amyotrophic Lateral Sclerosis / pathology
  • DNA-Binding Proteins / metabolism*
  • Female
  • Humans
  • Membrane Proteins / metabolism*
  • Motor Cortex / metabolism
  • Motor Cortex / pathology
  • Motor Neurons / metabolism*
  • Motor Neurons / pathology
  • Nerve Degeneration / metabolism*
  • Nerve Degeneration / pathology
  • Polyadenylation
  • Spinal Cord / metabolism
  • Spinal Cord / pathology
  • Stathmin

Substances

  • DNA-Binding Proteins
  • Membrane Proteins
  • STMN2 protein, human
  • Stathmin
  • TARDBP protein, human