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

Picone, Remigio; Ren, Xiaoyun; Ivanovitch, Kenzo; Clarke, Jon; McKendry, Rachel A.; Baum, Buzz

doi:10.1371/journal.pbio.1000542

Cited by 70 publications

(65 citation statements)

References 69 publications

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“…Our results also have implications for possible mechanisms which determine the mean length of the MT cytoskeleton, as it has been studied experimentally in Ref. [9]. For a fixed stiffness k of the opposing elastic force, the average force generated by the MT ensemble corresponds to an average length of MTs.…”

Section: Resultssupporting

confidence: 59%

Cooperative dynamics of microtubule ensembles: Polymerization forces and rescue-induced oscillations

Zelinski¹,

Kierfeld²

2013

Phys. Rev. E

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We investigate the cooperative dynamics of an ensemble of N microtubules growing against an elastic barrier. Microtubules undergo so-called catastrophes, which are abrupt stochastic transitions from a growing to a shrinking state, and rescues, which are transitions back to the growing state. Microtubules can exert pushing or polymerization forces on an obstacle, such as an elastic barrier if the growing end is in contact with the obstacle. We use dynamical mean-field theory and stochastic simulations to analyze a model where each microtubule undergoes catastrophes and rescues and where microtubules interact by force sharing. For zero rescue rate, cooperative growth terminates in a collective catastrophe. The maximal polymerization force before catastrophes grows linearly with N for small N or a stiff elastic barrier, in agreement with available experimental results, whereas it crosses over to a logarithmic dependence for larger N or a soft elastic barrier. For a nonzero rescue rate and a soft elastic barrier, the dynamics becomes oscillatory with both collective catastrophe and rescue events, which are part of a robust limit cycle. Both the average and maximal polymerization forces then grow linearly with N , and we investigate their dependence on tubulin on-rates and rescue rates, which can be involved in cellular regulation mechanisms. We further investigate the robustness of the collective catastrophe and rescue oscillations with respect to different catastrophe models.

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Section: Resultssupporting

confidence: 59%

Cooperative dynamics of microtubule ensembles: Polymerization forces and rescue-induced oscillations

Zelinski¹,

Kierfeld²

2013

Phys. Rev. E

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“…3G). We noted the absence of MTs oriented along the long axis of the cell and that are required to drive cell elongation (Picone et al, 2010). This population of MTs could be rescued by co-expression of siRNA-resistant HA-FHOD1wt, along with rescue of cell shape (Fig.…”

Section: Fhod1 Coordinates Mt and Actin Cytoskeletons During Cell Sprmentioning

confidence: 78%

Spatiotemporal organization of Aurora-B by APC/CCdh1 after mitosis coordinates cell spreading via FHOD1

Floyd

Whiffin

Gavilán

et al. 2013

Journal of Cell Science

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Spatiotemporal regulation of mitotic kinase activity underlies the extensive rearrangement of cellular components required for cell division. One highly dynamic mitotic kinase is Aurora kinase B (AurB), which has multiple roles defined by the changing localization of the chromosome passenger complex (CPC) as cells progress through mitosis, including regulation of cytokinesis and abscission. Like other mitotic kinases, AurB is a target of the anaphase-promoting complex (APC/C) ubiquitin ligase during mitotic exit, but it is not known if APC/C-mediated destruction plays any specific role in controling AurB activity. Here we have examined the contribution of APC/CCdh1 to organization of AurB activity as cells exit mitosis and re-enter interphase. We report that APC/CCdh1-dependent proteolysis restricts a cell cortex-associated pool of active AurB in space and time. In early G1 phase this pool of AurB is found at protrusions associated with cell spreading. AurB retention at the cortex depends on a formin, FHOD1, critically required to organize the cytoskeleton after division. We identify AurB phosphorylation sites in FHOD1 and show that phosphomutant FHOD1 is impaired in post-mitotic assembly of oriented actin cables. We propose that Cdh1 contributes to spatiotemporal organization of AurB activity and that organization of FHOD1 activity by AurB contributes to daughter cell spreading after mitosis.

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“…In other systems, both microtubule dynamics and actomyosin signaling have been implicated in the control of cell height (Levina et al, 2001;Picone et al, 2010). We tested whether either of these cytoskeletal signaling systems is essential for intestinal epithelial cell elongation.…”

Section: Mechanisms Controlling Growth Of Epithelial Girth In the Earmentioning

confidence: 99%

Cell dynamics in fetal intestinal epithelium: implications for intestinal growth and morphogenesis

et al. 2011

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SUMMARYThe cellular mechanisms that drive growth and remodeling of the early intestinal epithelium are poorly understood. Current dogma suggests that the murine fetal intestinal epithelium is stratified, that villi are formed by an epithelial remodeling process involving the de novo formation of apical surface at secondary lumina, and that radial intercalation of the stratified cells constitutes a major intestinal lengthening mechanism. Here, we investigate cell polarity, cell cycle dynamics and cell shape in the fetal murine intestine between E12.5 and E14.5. We show that, contrary to previous assumptions, this epithelium is pseudostratified. Furthermore, epithelial nuclei exhibit interkinetic nuclear migration, a process wherein nuclei move in concert with the cell cycle, from the basal side (where DNA is synthesized) to the apical surface (where mitosis takes place); such nuclear movements were previously misinterpreted as the radial intercalation of cells. We further demonstrate that growth of epithelial girth between E12.5 and E14.5 is driven by microtubule-and actinomyosin-dependent apicobasal elongation, rather than by progressive epithelial stratification as was previously thought. Finally, we show that the actin-binding protein Shroom3 is crucial for the maintenance of the single-layered pseudostratified epithelium. In mice lacking Shroom3, the epithelium is disorganized and temporarily stratified during villus emergence. These results favor an alternative model of intestinal morphogenesis in which the epithelium remains single layered and apicobasally polarized throughout early intestinal development.

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

Abstract: An analysis of cells grown on micro-patterned lines, and of cells during zebrafish development, identifies a population of microtubules that align along the long axis of cells to mediate homeostatic length control.

Cited by 70 publications

References 69 publications

Cooperative dynamics of microtubule ensembles: Polymerization forces and rescue-induced oscillations

Cooperative dynamics of microtubule ensembles: Polymerization forces and rescue-induced oscillations

Spatiotemporal organization of Aurora-B by APC/CCdh1 after mitosis coordinates cell spreading via FHOD1

Cell dynamics in fetal intestinal epithelium: implications for intestinal growth and morphogenesis

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