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A Polarised Population of Dynamic Microtubules Mediates Homeostatic Length Control in Animal Cells

Picone, R; Ren, XY; Ivanovitch, KD; Clarke, JDW; McKendry, RA; Baum, B; (2010) A Polarised Population of Dynamic Microtubules Mediates Homeostatic Length Control in Animal Cells. PLOS BIOL , 8 (11) , Article e1000542. 10.1371/journal.pbio.1000542. Green open access

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Abstract

Because physical form and function are intimately linked, mechanisms that maintain cell shape and size within strict limits are likely to be important for a wide variety of biological processes. However, while intrinsic controls have been found to contribute to the relatively well-defined shape of bacteria and yeast cells, the extent to which individual cells from a multicellular animal control their plastic form remains unclear. Here, using micropatterned lines to limit cell extension to one dimension, we show that cells spread to a characteristic steady-state length that is independent of cell size, pattern width, and cortical actin. Instead, homeostatic length control on lines depends on a population of dynamic microtubules that lead during cell extension, and that are aligned along the long cell axis as the result of interactions of microtubule plus ends with the lateral cell cortex. Similarly, during the development of the zebrafish neural tube, elongated neuroepithelial cells maintain a relatively well-defined length that is independent of cell size but dependent upon oriented microtubules. A simple, quantitative model of cellular extension driven by microtubules recapitulates cell elongation on lines, the steady-state distribution of microtubules, and cell length homeostasis, and predicts the effects of microtubule inhibitors on cell length. Together this experimental and theoretical analysis suggests that microtubule dynamics impose unexpected limits on cell geometry that enable cells to regulate their length. Since cells are the building blocks and architects of tissue morphogenesis, such intrinsically defined limits may be important for development and homeostasis in multicellular organisms.

Type: Article
Title: A Polarised Population of Dynamic Microtubules Mediates Homeostatic Length Control in Animal Cells
Open access status: An open access version is available from UCL Discovery
DOI: 10.1371/journal.pbio.1000542
Publisher version: http://dx.doi.org/10.1371/journal.pbio.1000542
Language: English
Additional information: © 2010 Picone et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. RP was funded by EPSRC Studentship (A.J.S.) awarded as part of the CoMPLEX Doctoral Training Centre (UCL) and IRC in Nanotechnology (Cambridge, UCL, Bristol). BB was funded by Cancer Research UK, Wellcome, UCL and the Royal Society. RAM was funded by UCL and the Royal Society and XR and JC were funded by the BBSRC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Keywords: DROSOPHILA-MELANOGASTER, EPITHELIAL-CELLS, SIZE REGULATION, NEBULIN RULER, S2 CELLS, MORPHOGENESIS, FIBROBLASTS, DIVISION, GROWTH, ACTIN
UCL classification: UCL > Provost and Vice Provost Offices
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > UCL BEAMS
UCL > Provost and Vice Provost Offices > UCL BEAMS > Faculty of Maths and Physical Sciences
UCL > Provost and Vice Provost Offices > UCL BEAMS > Faculty of Maths and Physical Sciences > London Centre for Nanotechnology
URI: https://discovery.ucl.ac.uk/id/eprint/569519
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