Aggregation-prone Tau impairs mitochondrial import, which affects organelle morphology and neuronal complexity

J Cell Sci. 2023 Jul 1;136(13):jcs260993. doi: 10.1242/jcs.260993. Epub 2023 Jul 7.

Abstract

Mitochondrial protein import is essential for organellar biogenesis, and thereby for the sufficient supply of cytosolic ATP - which is particularly important for cells with high energy demands like neurons. This study explores the prospect of import machinery perturbation as a cause of neurodegeneration instigated by the accumulation of aggregating proteins linked to disease. We found that the aggregation-prone Tau variant (TauP301L) reduces the levels of components of the import machinery of the outer (TOM20, encoded by TOMM20) and inner membrane (TIM23, encoded by TIMM23) while associating with TOM40 (TOMM40). Intriguingly, this interaction affects mitochondrial morphology, but not protein import or respiratory function; raising the prospect of an intrinsic rescue mechanism. Indeed, TauP301L induced the formation of tunnelling nanotubes (TNTs), potentially for the recruitment of healthy mitochondria from neighbouring cells and/or the disposal of mitochondria incapacitated by aggregated Tau. Consistent with this, inhibition of TNT formation (and rescue) reveals Tau-induced import impairment. In primary neuronal cultures, TauP301L induced morphological changes characteristic of neurodegeneration. Interestingly, these effects were mirrored in cells where the import sites were blocked artificially. Our results reveal a link between aggregation-prone Tau and defective mitochondrial import relevant to disease.

Keywords: Mitochondria; Mitochondrial import; Mitochondrial morphology; Neurodegeneration; Neuronal complexity; Tau.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Membrane Transport Proteins* / metabolism
  • Mitochondria* / metabolism
  • Mitochondrial Membrane Transport Proteins / metabolism
  • Mitochondrial Proteins / metabolism
  • Neurons / metabolism
  • Protein Transport / physiology
  • Receptors, Cell Surface / metabolism

Substances

  • Membrane Transport Proteins
  • Receptors, Cell Surface
  • Mitochondrial Proteins
  • Mitochondrial Membrane Transport Proteins