Chimera proteins with affinity for membranes and microtubule tips polarize in the membrane of fission yeast cells Journal Article

Author(s): Recouvreux, Pierre; Sokolowski, Thomas R; Grammoustianou, Aristea; TenWolde, Pieter R; Dogterom, Marileen
Article Title: Chimera proteins with affinity for membranes and microtubule tips polarize in the membrane of fission yeast cells
Affiliation IST Austria
Abstract: Cell polarity refers to a functional spatial organization of proteins that is crucial for the control of essential cellular processes such as growth and division. To establish polarity, cells rely on elaborate regulation networks that control the distribution of proteins at the cell membrane. In fission yeast cells, a microtubule-dependent network has been identified that polarizes the distribution of signaling proteins that restricts growth to cell ends and targets the cytokinetic machinery to the middle of the cell. Although many molecular components have been shown to play a role in this network, it remains unknown which molecular functionalities are minimally required to establish a polarized protein distribution in this system. Here we show that a membrane-binding protein fragment, which distributes homogeneously in wild-type fission yeast cells, can be made to concentrate at cell ends by attaching it to a cytoplasmic microtubule end-binding protein. This concentration results in a polarized pattern of chimera proteins with a spatial extension that is very reminiscent of natural polarity patterns in fission yeast. However, chimera levels fluctuate in response to microtubule dynamics, and disruption of microtubules leads to disappearance of the pattern. Numerical simulations confirm that the combined functionality of membrane anchoring and microtubule tip affinity is in principle sufficient to create polarized patterns. Our chimera protein may thus represent a simple molecular functionality that is able to polarize the membrane, onto which additional layers of molecular complexity may be built to provide the temporal robustness that is typical of natural polarity patterns.
Keywords: Cell polarity; Microtubules; Fission yeast; Membrane diffusion; Tip tracking
Journal Title: PNAS
Volume: 113
Issue 7
ISSN: 1091-6490
Publisher: National Academy of Sciences  
Date Published: 2016-02-16
Start Page: 1811
End Page: 1816
DOI: 10.1073/pnas.1419248113
Notes: We thank Sophie Martin, Ken Sawin, Stephen Huisman, and Damian Brunner for strains; Julianne Teapal, Marcel Janson, Sergio Rincon, and Phong Tran for technical assistance; Andrew Mugler and Bela Mulder for discussions; and Sander Tans, Phong Tran, and Anne Paoletti for critical reading of the manuscript. This work is part of the research program of the “ Stichting voor Fundamenteel Onderzoek de Materie, ” which is financially supported by the “ Nederlandse organisatie voor Wete nschappelijk Onderzoek (NWO). ”
Open access: yes (repository)