Abstract
Cell polarity - the morphological and functional differentiation of cellular compartments in a directional manner - is required for processes such as orientation of cell division, directed cellular growth and motility. How the interplay of components within the complexity of a cell leads to cell polarity is still heavily debated. In this Review, we focus on one specific aspect of cell polarity: the non-uniform accumulation of proteins on the cell membrane. In cells, this is achieved through reaction-diffusion and/or cytoskeleton-based mechanisms. In reaction-diffusion systems, components are transformed into each other by chemical reactions and are moving through space by diffusion. In cytoskeleton-based processes, cellular components (i.e. proteins) are actively transported by microtubules (MTs) and actin filaments to specific locations in the cell. We examine how minimal systems - in vitro reconstitutions of a particular cellular function with a minimal number of components - are designed, how they contribute to our understanding of cell polarity (i.e. protein accumulation), and how they complement in vivo investigations. We start by discussing the Min protein system from Escherichia coli, which represents a reaction-diffusion system with a well-established minimal system. This is followed by a discussion of MT-based directed transport for cell polarity markers as an example of a cytoskeleton-based mechanism. To conclude, we discuss, as an example, the interplay of reaction-diffusion and cytoskeleton-based mechanisms during polarity establishment in budding yeast.
Highlights
According to the second law of thermodynamics, any system of particles naturally tends to maximize its entropy, increasing the disorder of the system
A main role of the cytoskeleton in polarity establishment and maintenance is the active, directed transport of cargo through the cell; for example, by motor proteins walking along cytoskeletal filaments or cytoplasmic flows that are generated by cytoskeletal network contractions (Theurkauf, 1994; Serbus et al, 2005; Yi et al, 2013; Suzuki et al, 2017). Both MTs and actin filaments are involved in cell polarity, but this Review focuses on MTs – highly dynamic intrinsically polarized filaments whose properties can be influenced by a wealth of MT-associated proteins (MAPs)
Polarity establishment in budding yeast Polarity establishment in budding yeast is a classical system for pattern formation (Bi and Park, 2012; Martin, 2015) (Fig. 4A), where a Cdc42-based protein pattern on the cell membrane marks the site of bud emergence (Bi and Park, 2012)
Summary
According to the second law of thermodynamics, any system of particles naturally tends to maximize its entropy, increasing the disorder of the system. The first reconstitution of the Min dynamics showed that, in presence of ATP, MinD and MinE spontaneously self-organize on a flat, supported lipid bilayer into traveling waves and spirals (Loose et al, 2008) (Fig. 1B) This observation revealed the minimal requirements for Min patterns: MinD, MinE, a membrane and ATP. Oscillations to occur, and (3) that the emerging protein waves are based on reaction–diffusion processes, namely the attachment and detachment of proteins on a membrane To this qualitative information, the reconstituted system facilitated investigations on how features of the system quantitatively influence the protein dynamics, revealing that the MinE to MinD ratio influences the wave velocity and wavelength (see Table S2).
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