Endosomal Wnt signaling proteins control microtubule nucleation in dendrites

Alexis T. Weiner, Dylan Y. Seebold, Pedro Torres-Gutierrez, Christin Folker, Rachel D. Swope, Gregory O. Kothe, Jessica G. Stoltz, Madeleine K. Zalenski, Christopher Kozlowski, Dylan J. Barbera, Mit A. Patel, Pankajam Thyagarajan, Matthew Shorey, Derek M.R. Nye, Matthew Keegan, Kana Behari, Song Song, Jeffrey D. Axelrod, Melissa M. Rolls

Research output: Contribution to journalArticle

1 Scopus citations

Abstract

Dendrite microtubules are polarized with minus-end-out orientation in Drosophila neurons. Nucleation sites concentrate at dendrite branch points, but how they localize is not known. Using Drosophila, we found that canonical Wnt signaling proteins regulate localization of the core nucleation protein γTubulin (γTub). Reduction of frizzleds (fz), arrow (low-density lipoprotein receptor-related protein [LRP] 5/6), dishevelled (dsh), casein kinase Iγ, G proteins, and Axin reduced γTub-green fluorescent protein (GFP) at branch points, and two functional readouts of dendritic nucleation confirmed a role for Wnt signaling proteins. Both dsh and Axin localized to branch points, with dsh upstream of Axin. Moreover, tethering Axin to mitochondria was sufficient to recruit ectopic γTub-GFP and increase microtubule dynamics in dendrites. At dendrite branch points, Axin and dsh colocalized with early endosomal marker Rab5, and new microtubule growth initiated at puncta marked with fz, dsh, Axin, and Rab5. We propose that in dendrites, canonical Wnt signaling proteins are housed on early endosomes and recruit nucleation sites to branch points.

Original languageEnglish (US)
Article numbere3000647
JournalPLoS biology
Volume18
Issue number3
DOIs
StatePublished - Mar 2020

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Agricultural and Biological Sciences(all)

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    Weiner, A. T., Seebold, D. Y., Torres-Gutierrez, P., Folker, C., Swope, R. D., Kothe, G. O., Stoltz, J. G., Zalenski, M. K., Kozlowski, C., Barbera, D. J., Patel, M. A., Thyagarajan, P., Shorey, M., Nye, D. M. R., Keegan, M., Behari, K., Song, S., Axelrod, J. D., & Rolls, M. M. (2020). Endosomal Wnt signaling proteins control microtubule nucleation in dendrites. PLoS biology, 18(3), [e3000647]. https://doi.org/10.1371/journal.pbio.3000647