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Review
. 2003 Apr 17;422(6933):766-74.
doi: 10.1038/nature01602.

Adaptation of core mechanisms to generate cell polarity

W James Nelson  1
Affiliations
Review

Adaptation of core mechanisms to generate cell polarity

W James Nelson. Nature. .

Abstract

Cell polarity is defined as asymmetry in cell shape, protein distributions and cell functions. It is characteristic of single-cell organisms, including yeast and bacteria, and cells in tissues of multi-cell organisms such as epithelia in worms, flies and mammals. This diversity raises several questions: do different cell types use different mechanisms to generate polarity, how is polarity signalled, how do cells react to that signal, and how is structural polarity translated into specialized functions? Analysis of evolutionarily diverse cell types reveals that cell-surface landmarks adapt core pathways for cytoskeleton assembly and protein transport to generate cell polarity.

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Figures

Figure 1
Figure 1
Diversity of shapes of polarized cells (not to scale). Fucus zygote exposed to a light gradient showing polarized distributions of ion channels/dihydropyridine receptors (red circles) and F-actin (blue line) in the rhizoid cell (bottom) compared to the thallus cell (top). Fission yeast (Schizosaccharomyces pombe) showing polarized distributions of actin (purple) and microtubules (blue dotted line) in the long axis of the cell, and the nucleus positioned in the centre of the cell. Drosophila neuroblast delaminated from the ventral neuroectoderm with an asymmetric plane of division that will yield a large ‘apical’ neuroblast stem cell and a small ‘basal’ ganglion mother cell. Caulobacter crescentus predivisional cell showing polarized distributions of the flagellum (swarmer cell, top) and stalk (stalked cell, bottom). Invertebrate/vertebrate transporting epithelium showing organization of polarized epithelial cells (apical membrane, green; basolateral membrane, blue) in a tube that separates two biological compartments and regulates vectorial transport of ions/solutes (red arrow) between those compartments. Budding yeast (Saccharomyces cerevisiae) forming a daughter cell ‘bud’ from the mother cell next to the previous site of cytokinesis (bud scar, red disc), and orienting actin cables (purple) for transport of vesicles (black circles) from the mother to daughter cell. Mammalian basket cell interneuron showing the distribution of the soma/dendrite (black) and axon (red; image courtesy of D. Madison, Stanford University School of Medicine).
Figure 2
Figure 2
Protein pathways for generating cell polarity in budding yeast. a, Axial and bipolar budding patterns. b, A complex of proteins is assembled at the bud tip that orients the actin cytoskeleton, astral microtubules and vesicle delivery to the bud. c, Hierarchical organization of regulators, processes and cellular machinery linking bud-site selection to assembly of an actin cap, anchoring/nucleation of actin cables, and vesicle targeting that results in polarized membrane growth at the bud.
Figure 3
Figure 3
Protein pathways for generating cell polarity in fission yeast. a, Distribution of actin (cables and cortical patches) and microtubule cytoskeletons relative to the ‘old’ and ‘new’ ends of the cell, which grow during the G1 and G2 phases of the cell cycle, respectively. b, Hypothetical organization of proteins in cortical actin patches, and interactions of microtubule plus ends with the cell end/cortical actin patch (for details, see text).
Figure 4
Figure 4
Organization of polarized epithelial cells and the apical junctional complex. a, Polarized epithelial cells form a monolayer in which the apical (unbounded surface) is separated at the boundary with the basal and lateral membranes (bounded surfaces) by the apical junctional complex (top). The main part of the panel shows molecular organization of the apical junctional complex. In vertebrates, the apical junctional complex is separated into structurally and functionally different sub-domains comprising membrane proteins (Crumbs, JAM (junctional adhesion molecule), nectin, occludin/claudin and cadherin) linked to modular protein scaffolds, which in turn bind mostly to the actin cytoskeleton, although links to microtubules are possible. In invertebrates (C. elegans and Drosophila), the apical junctional complex is similarly organized, except that the ‘tight junction’ function is provided by the septate junction localized below the cadherin (adherens) junction. b, Simplified scheme for how different protein complexes in the apical junctional complex regulate cell–cell adhesion (cadherin complex), and apical membrane (Bazooka and Crumbs complexes) and lateral membrane (Lethal giant larvae, Scribble and Disc large complex) identity. For details see text.
Figure 5
Figure 5
Generation of cell polarity in epithelia. a, Formation of the cellular blastoderm in early Drosophila embryogenesis (for details, see text). b, Schematic representation of polarized epithelial cells. Left, organization of the actin and microtubule cytoskeletons; right, organization of vesicle transport pathways to different plasma membrane domains either directly from the Golgi complex, or indirectly via apical or basal endosomes through endocytic or transcytotic pathways. c, Generation of the lateral membrane domain in cultured epithelial cells. Prior to cadherin-mediated cell–cell adhesion, the exocyst is cytosolic and vesicles fuse with the basal membrane. Upon cell–cell adhesion (step 1), the exocyst is recruited to cell–cell contacts and vesicles fuse with the forming lateral membrane. As more vesicles fuse, the lateral membrane increases in area around sixfold. Later (step 2), the exocyst and vesicle delivery are located in the apical region of the lateral membrane.
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