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Optical flow analysis reveals that Kinesin-mediated advection impacts on the orientation of microtubules in the Drosophila oocyte

View ORCID ProfileMaik Drechsler, View ORCID ProfileLukas F. Lang, Layla Al-Khatib, Hendrik Dirks, Martin Burger, View ORCID ProfileCarola-Bibiane Schönlieb, Isabel M. Palacios
doi: https://doi.org/10.1101/556043
Maik Drechsler
aSchool of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK
bDepartment of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
cDepartment of Zoology and Developmental Biology, University of Osnabrück, Barbarastraße 11, 49076 Osnabrück, Germany
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  • For correspondence: madrechs@uos.de i.palacios@qmul.ac.uk
Lukas F. Lang
dDepartment of Applied Mathematics and Theoretical Physics, University of Cambridge, Wilberforce Road, Cambridge CB3 0WA, UK
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Layla Al-Khatib
aSchool of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK
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Hendrik Dirks
eInstitute for Computational and Applied Mathematics, University of Münster, Einsteinstraße 62, 48149 Münster, Germany
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Martin Burger
fDepartment of Mathematics, Friedrich-Alexander Universität Erlangen-Nürnberg, Cauerstraße 11, 91058 Erlangen, Germany
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Carola-Bibiane Schönlieb
dDepartment of Applied Mathematics and Theoretical Physics, University of Cambridge, Wilberforce Road, Cambridge CB3 0WA, UK
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Isabel M. Palacios
aSchool of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK
bDepartment of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
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  • For correspondence: madrechs@uos.de i.palacios@qmul.ac.uk
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ABSTRACT

The orientation of microtubule networks is exploited by motors to deliver cargoes to specific intracellular destinations, and is thus essential for cell polarity and function. Reconstituted in vitro systems have largely contributed to understanding the molecular framework regulating the behavior of microtubule filaments. In cells however, microtubules are exposed to various biomechanical forces that might impact on their orientation, but little is known about it. Oocytes, which display forceful cytoplasmic streaming, are excellent model systems to study the impact of motion forces on cytoskeletons in vivo. Here we implement variational optical flow analysis as a new approach to analyze the polarity of microtubules in the Drosophila oocyte, a cell that displays distinct Kinesin-dependent streaming. After validating the method as robust for describing microtubule orientation from confocal movies, we find that increasing the speed of flows results in aberrant plus end growth direction. Furthermore, we find that in oocytes where Kinesin is unable to induce cytoplasmic streaming, the growth direction of microtubule plus ends is also altered. These findings lead us to propose that cytoplasmic streaming - and thus motion by advection – contributes to the correct orientation of MTs in vivo. Finally, we propose a possible mechanism for a specialised cytoplasmic actin network (the actin mesh) to act as a regulator of flow speeds; to counteract the recruitment of Kinesin to microtubules.

HIGHLIGHT SUMMARY Cytoskeletal networks do not exist in isolation, but experience crowded and dynamic intracellular environments. However, microtubule-environment interactions are not well understood, and such system-environment interactions are an unresolved question in biology that demands bridging across disciplines. Here we introduce an optical flow motion estimation approach to study microtubule orientation in the Drosophila oocyte, a cell displaying substantial cytoplasmic streaming. We show that microtubule polarity is affected by the regime of these flows, and furthermore, that the presence of flows is necessary for MTs to adopt their proper polarity. With these findings we are contributing to further understanding how microtubules organize in their impacting natural environment.

Footnotes

  • https://doi.org/10.5281/zenodo.2573254

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted March 09, 2020.
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Optical flow analysis reveals that Kinesin-mediated advection impacts on the orientation of microtubules in the Drosophila oocyte
Maik Drechsler, Lukas F. Lang, Layla Al-Khatib, Hendrik Dirks, Martin Burger, Carola-Bibiane Schönlieb, Isabel M. Palacios
bioRxiv 556043; doi: https://doi.org/10.1101/556043
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Optical flow analysis reveals that Kinesin-mediated advection impacts on the orientation of microtubules in the Drosophila oocyte
Maik Drechsler, Lukas F. Lang, Layla Al-Khatib, Hendrik Dirks, Martin Burger, Carola-Bibiane Schönlieb, Isabel M. Palacios
bioRxiv 556043; doi: https://doi.org/10.1101/556043

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