Physical Mechanisms Redirecting Cell Polarity and Cell Shape in Fission Yeast

Abstract

Summary The fission yeast Schizosaccharomyces pombe has a cylindrical rod-shape that is organized and maintained by interactions between the microtubule, cell membrane, and actin cytoskeleton; i.e., microtubules deliver factors to the cell tips that subsequently recruit the actin machinery to direct localized cell growth [1]. Mutations affecting any components in this pathway lead to bent, branched, or round cells [2]. In this context, the cytoskeleton controls cell polarity and thus dictates cell shape. Here, we use soft-lithography techniques to construct microfluidic channels in order to control the shape of cells. We show that by physically forcing wildtype rod-shaped cells to grow bent, they will re-organize their cytoskeleton and re-direct cell polarity to make new ectopic cell tips. In addition, by physically forcing bent or round mutant cells to conform to the wildtype rod-shape, cells will reverse their mutational phenotypes by re-organizing their cytoskeleton to maintain proper wildtype-like microtubule, cell membrane proteins, and actin localizations. Our study provides direct evidence that the cytoskeleton controls cell polarity and cell shape and demonstrates that cell shape also controls the organization of the cytoskeleton, in a feedback loop. We present a model of the feedback loop which explains how fission yeast cells maintain a rod-shape, and how perturbation of specific parameters of the loop can lead to different cell shapes.

Cytoskeletal dynamics in fission yeast: A review of models for polarization and division

“…Dynamic landmarks activate autocatalytic actin polymerization: presumably, actin filaments in cables and patches further recruit actin nucleators. This could be consistent with experiments suggesting positive feedback in the polarization system (Terenna et al, 2008). Autocatalytic polymerization amplifies local noise, polarizing the cell and breaking symmetry.…”

“…Since shorter microtubules are more stable, more force comes from the closer tip and the microtubule system centers the nucleus, as suggested by an earlier computational model (Tran et al, 2001). These results extend easily to microtubule dynamics in differently shaped cells, such as those in recent experiments where they are confined (Minc et al, 2009;Terenna et al, 2008). …”

“…According to recent experiments, normal cell shape and microtubule organization reinforce each other (Minc et al, 2009;Terenna et al, 2008). The rod shape directs elongating microtubules to the ends of the cell [see Figs.…”

Experiments inside a box lead to out-of-the-box ideas on cellular organization

“…In 2008 already Terenna et al (2008) grew fission yeast in microfabricated channels and showed directly how cell shape and microtubule organization are coupled and control cell polarity. The most dramatic changes in cell shape were created by Minc et al (2011).…”

A common mechanism for protein cluster formation

“…1b). 29,30 Unlike in the GTPase-based system, the energy necessary to maintain diffusion-counteracting self-focusing mechanism is consumed not within the cluster itself, but rather by the polymerizing microtubules (GTP) and molecular motors (ATP) that move along the several nuclear pore complex and vesicle coat proteins including COPI, COPII and clathrin. 21,22 While these proteins are remarkably diverse in the way they interact with each other, all of them are capable of forming spatially extended polymeric lattices.…”