Ensconsin-dependent changes in microtubule organization and LINC complex-dependent changes in nucleus-nucleus interactions result in quantitatively distinct myonuclear positioning defects

Mol Biol Cell. 2021 Nov 1;32(21):ar27. doi: 10.1091/mbc.E21-06-0324. Epub 2021 Sep 15.

Abstract

Nuclear movement is a fundamental process of eukaryotic cell biology. Skeletal muscle presents an intriguing model to study nuclear movement because its development requires the precise positioning of multiple nuclei within a single cytoplasm. Furthermore, there is a high correlation between aberrant nuclear positioning and poor muscle function. Although many genes that regulate nuclear movement have been identified, the mechanisms by which these genes act are not known. Using Drosophila melanogaster muscle development as a model system and a combination of live-embryo microscopy and laser ablation of nuclei, we have found that clustered nuclei encompass at least two phenotypes that are caused by distinct mechanisms. Specifically, Ensconsin is necessary for productive force production to drive any movement of nuclei, whereas Bocksbeutel and Klarsicht are necessary to form distinct populations of nuclei that move to different cellular locations. Mechanistically, Ensconsin regulates the number of growing microtubules that are used to move nuclei, whereas Bocksbeutel and Klarsicht regulate interactions between nuclei.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biological Transport
  • Cell Nucleus / metabolism
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / metabolism
  • Kinesins
  • Microtubule Proteins / metabolism
  • Microtubule-Associated Proteins / metabolism*
  • Microtubule-Associated Proteins / physiology
  • Microtubule-Organizing Center / metabolism*
  • Microtubules / metabolism
  • Muscle, Skeletal / metabolism*
  • Nuclear Envelope / metabolism

Substances

  • Drosophila Proteins
  • Microtubule Proteins
  • Microtubule-Associated Proteins
  • Kinesins