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


Type

Article

Change log

Authors

Khuc Trong, Philipp 
Doerflinger, Hélène 
Dunkel, Jörn 
St Johnston, Daniel  ORCID logo  https://orcid.org/0000-0001-5582-3301
Goldstein, Raymond E 

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.

Description

Keywords

D. melanogaster, cell biology, cytoplasmic streaming, cytoskeleton, developmental biology, mRNA transport, stem cells, Animals, Cell Polarity, Drosophila, Drosophila Proteins, Homeodomain Proteins, Microtubules, Models, Theoretical, Oocytes, Protein Multimerization, RNA, Messenger, Trans-Activators

Journal Title

Elife

Conference Name

Journal ISSN

2050-084X
2050-084X

Volume Title

4

Publisher

eLife Sciences Publications, Ltd
Sponsorship
European Research Council (247333)
Wellcome Trust (092096/Z/10/Z)
Wellcome Trust (095927/B/11/Z)
Wellcome Trust (080007/Z/06/Z)
Cancer Research Uk (None)
This work was supported in part by the Boehringer Ingelheim Fonds and EPSRC (P. K. T.), core support from the Wellcome Trust [092096] and Cancer Research UK [A14492] (H. D.), the MIT Solomon Buchsbaum Award (J. D.), a Wellcome Trust Principal Research Fellowship [080007] (D. StJ.), the Leverhulme Trust, and the European Research Council Advanced Investigator Grant [247333] (R. E. G.).