Axon morphogenesis and maintenance require an evolutionary conserved safeguard function of Wnk kinases antagonizing Sarm and Axed

Neuron. 2021 Sep 15;109(18):2864-2883.e8. doi: 10.1016/j.neuron.2021.07.006. Epub 2021 Aug 11.

Abstract

The molecular and cellular mechanisms underlying complex axon morphogenesis are still poorly understood. We report a novel, evolutionary conserved function for the Drosophila Wnk kinase (dWnk) and its mammalian orthologs, WNK1 and 2, in axon branching. We uncover that dWnk, together with the neuroprotective factor Nmnat, antagonizes the axon-destabilizing factors D-Sarm and Axundead (Axed) during axon branch growth, revealing a developmental function for these proteins. Overexpression of D-Sarm or Axed results in axon branching defects, which can be blocked by overexpression of dWnk or Nmnat. Surprisingly, Wnk kinases are also required for axon maintenance of adult Drosophila and mouse cortical pyramidal neurons. Requirement of Wnk for axon maintenance is independent of its developmental function. Inactivation of dWnk or mouse Wnk1/2 in mature neurons leads to axon degeneration in the adult brain. Therefore, Wnk kinases are novel signaling components that provide a safeguard function in both developing and adult axons.

Keywords: Drosophila mechanosensory neuron; Wallerian; Wnk kinase; axon branching; axon degeneration; axon maintenance; axon morphogenesis; cortical pyramidal neuron; de novo protein synthesis; neurodevelopment; neuroprotection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Armadillo Domain Proteins / antagonists & inhibitors
  • Armadillo Domain Proteins / biosynthesis*
  • Armadillo Domain Proteins / genetics
  • Axons / metabolism*
  • Cell Line, Tumor
  • Cytoskeletal Proteins / antagonists & inhibitors
  • Cytoskeletal Proteins / biosynthesis*
  • Cytoskeletal Proteins / genetics
  • Drosophila Proteins / antagonists & inhibitors
  • Drosophila Proteins / biosynthesis*
  • Drosophila Proteins / genetics
  • Drosophila melanogaster
  • Evolution, Molecular*
  • Female
  • HEK293 Cells
  • Humans
  • Male
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Morphogenesis / physiology*
  • Pregnancy
  • Protein Serine-Threonine Kinases / biosynthesis*
  • Protein Serine-Threonine Kinases / genetics

Substances

  • Armadillo Domain Proteins
  • Cytoskeletal Proteins
  • Drosophila Proteins
  • SARM1 protein, mouse
  • axed protein, Drosophila
  • Protein Serine-Threonine Kinases
  • WNK protein, Drosophila