Cortical microtubule nucleation can organise the cytoskeleton of Drosophila oocytes to define the anteroposterior axis

Elife. 2015 Sep 25:4:e06088. doi: 10.7554/eLife.06088.

Abstract

Many cells contain non-centrosomal arrays of microtubules (MTs), but the assembly, organisation and function of these arrays are poorly understood. We present the first theoretical model for the non-centrosomal MT cytoskeleton in Drosophila oocytes, in which bicoid and oskar mRNAs become localised to establish the anterior-posterior body axis. Constrained by experimental measurements, the model shows that a simple gradient of cortical MT nucleation is sufficient to reproduce the observed MT distribution, cytoplasmic flow patterns and localisation of oskar and naive bicoid mRNAs. Our simulations exclude a major role for cytoplasmic flows in localisation and reveal an organisation of the MT cytoskeleton that is more ordered than previously thought. Furthermore, modulating cortical MT nucleation induces a bifurcation in cytoskeletal organisation that accounts for the phenotypes of polarity mutants. Thus, our three-dimensional model explains many features of the MT network and highlights the importance of differential cortical MT nucleation for axis formation.

Keywords: D. melanogaster; cell biology; cytoplasmic streaming; cytoskeleton; developmental biology; mRNA transport; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Polarity*
  • Drosophila Proteins / biosynthesis
  • Drosophila*
  • Homeodomain Proteins / biosynthesis
  • Microtubules / metabolism*
  • Models, Theoretical
  • Oocytes / physiology*
  • Protein Multimerization
  • RNA, Messenger / biosynthesis
  • Trans-Activators / biosynthesis

Substances

  • Drosophila Proteins
  • Homeodomain Proteins
  • RNA, Messenger
  • Trans-Activators
  • bcd protein, Drosophila
  • osk protein, Drosophila