Force and length-dependent catastrophe activities explain interphase microtubule organization in fission yeast

REPORT Force- and length-dependent catastrophe activities explain interphase microtubule organization in fission yeast Dietrich Foethke, Tatyana Makushok, Damian Brunner* and Franc¸ois Ne´de´lec* Cell Biology and Biophysics, European Molecular Biology Laboratory, Heidelberg, Germany * Corresponding authors. D Brunner or F Ne´de´lec, Cell Biology and Biophysics, European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany. Tel.: þ 49 6221 387 8597; Fax: þ 49 6221 387 8512; E-mails: brunner@embl.de or nedelec@embl.de Received 26.6.08; accepted 28.11.08 The cytoskeleton is essential for the maintenance of cell morphology in eukaryotes. In fission yeast, for example, polarized growth sites are organized by actin, whereas microtubules (MTs) acting upstream control where growth occurs. Growth is limited to the cell poles when MTs undergo catastrophes there and not elsewhere on the cortex. Here, we report that the modulation of MT dynamics by forces as observed in vitro can quantitatively explain the localization of MT catastrophes in Schizosaccharomyces pombe. However, we found that it is necessary to add length- dependent catastrophe rates to make the model fully consistent with other previously measured traits of MTs. We explain the measured statistical distribution of MT–cortex contact times and re- examine the curling behavior of MTs in unbranched straight tea1D cells. Importantly, the model demonstrates that MTs together with associated proteins such as depolymerizing kinesins are, in principle, sufficient to mark the cell poles. Molecular Systems Biology 17 March 2009; doi:10.1038/msb.2008.76 Subject Categories: cell and tissue architecture Keywords: cell; cytoskeleton; force; mechanics; simulations This is an open-access article distributed under the terms of the Creative Commons Attribution Licence, which permits distribution and reproduction in any medium, provided the original author and source are credited. Creation of derivative works is permitted but the resulting work may be distributed only under the same or similar licence to this one. This licence does not permit commercial exploitation without specific permission. The fission yeast Schizosaccharomyces pombe is a convenient model to study cell morphogenesis (Hayles and Nurse, 2001). Wild-type cells are simple elongated rods growing at the cell poles and dividing in the middle. Yet, previous studies have outlined an interesting interplay between shape, growth and cytoskeletal organization. The first component is the rigid cell wall surrounding yeast cells that maintains cell shape independently of the cytoskeleton. Second, the actin cytoske- leton is essential for cell growth and cell wall remodeling (La Carbona et al, 2006). Lastly, although microtubules (MTs) are not required for growth per se, they control the location of growth sites by depositing specific marker proteins (Mata and Nurse, 1997; Brunner and Nurse, 2000; Sawin and Snaith, 2004). Abnormal deposition, occurring for example in mutants where MTs are shorter, results in cells that are either bent or branched (Sawin and Nurse, 1998; Snaith and Sawin, 2005). MTs also position the nucleus (Tran et al, 2001; Loiodice et al, 2005) and thus define the site of cytokinesis (Daga and Chang, 2005; Tolic-Norrelykke et al, 2005) and the partitioning of the cell into daughter cells. Hence, by controlling cell growth and division, MTs impact the evolution of shape in the cell lineage. As MTs are constrained within the cell, the converse is also true with MT organization being dependent on cell shape. For the rigid S. pombe cells, the two processes occur on very different timescales; with MT lifetimes being in the order of minutes, whereas cells typically double in size after 3 h. Consequently, individual MTs are enclosed in a boundary that is effectively constant during their lifetime. This means that it is valid to first study how MTs depend on cell shape, and to later include cell shape changes. We use here computer simulation for the first step, calculating the dynamic spatial organization of MTs within a fixed cell shape. This approach complements other efforts where cell morphogenesis is modeled with reaction–diffusion equations (Csikasz-Nagy et al, 2008) by focusing on the MT cytoskeleton. & 2009 EMBO and Macmillan Publishers Limited Molecular Systems Biology 2009 1 Molecular Systems Biology 5; Article number 241; doi:10.1038/msb.2008.76 Citation: Molecular Systems Biology 5:241 & 2009 EMBO and Macmillan Publishers Limited All rights reserved 1744-4292/09 www.molecularsystemsbiology.com Interphase MTs in fission yeast are typically forming 2–6 bundles, which are usually attached to the nucleus at their middle (Tran et al, 2001) (Figure 1). Antiparallel MTs overlap at their static minus ends, whereas the plus ends are dynamic and grow from the overlap zone toward the cell poles (Tran et al, 2001; Hoog et al, 2007). Such bundles transmit forces produced at the cell poles by MT polym

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