Key Points
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Cell polarity can be defined as a structurally and functionally asymmetric organization, in which the non-random positioning of each organelle, the function of which contributes to cell asymmetry, is preserved and transmitted through cell division.
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Each cytoskeletal or membrane organelle has its own physico-chemical properties and an overall orientated dynamics that must be coupled to that of other organelles in order to contribute efficiently to cell polarity.
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Organelle polarity can be propagated to the whole cell. Microtubules and the ancestral asymmetric centriole or basal body/axoneme organelle are particularly well designed to organize and transmit cell polarity.
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Two important groups of eukaryotic cells, cilium- or flagellum-dependent swimming cells and actin-dependent migrating cells, reveal common design principles, particularly concerning the cell-wide extension of the microtubule network from a nucleus-associated organizing centre.
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The conservative mode of duplication of the centriole or basal body seems to be a core mechanism for the transmission of polarities through cell division in both types of cell architecture.
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Juxtaposition of cortical contraction and cell adhesion is a core mechanism of cell-orientating processes in animal cells. Organelle positioning that is observed in tissues in response to external signalling cues can be studied in individual cells using experimental approaches, whereby the pattern of adhesion is precisely controlled.
Abstract
In spite of conspicuous differences in their polarized architecture, swimming unicellular eukaryotes and migrating cells from metazoa display a conserved hierarchical interlocking of the main cellular compartments, in which the microtubule network has a dominant role. A microtubule array can organize the distribution of endomembranes owing to a cell-wide and polarized extension around a unique nucleus-associated structure. The nucleus-associated structure in animal cells contains a highly conserved organelle, the centriole or basal body. This organelle has a defined polarity that can be transmitted to the cell. Its conservative mode of duplication seems to be a core mechanism for the transmission of polarities through cell division.
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Acknowledgements
The author would like to thank M. Piel and M. Théry, who helped considerably in the writing of this account through thorough discussions on most of the issues covered. They have produced original research with creative approaches over the past years, which inspired the shaping of this review. They also contributed significantly and generously towards the figures of this manuscript. This manuscript also benefited from discussions with P. Bastin and J. Beisson.
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Glossary
- Endomembrane
-
One of an intracellular dynamic array of membrane-bound organelles that have distinct components and functions. A constant flow of membranes and proteins occurs through these organelles.
- Centrosome
-
A single-copy structure that is generally localized at the cell centre because of its microtubule-nucleating and -anchoring activity. The centrosome is physically associated with the nucleus and duplicates once during the cell cycle. A centrosome can be isolated, whereas a microtubule-organizing centre (MTOC) is not specifically an isolatable structure. Whereas a centrosome is necessarily an MTOC, the reverse is not true.
- Centriole
-
A structure that is similar to the basal body organelle. A pair of centrioles is required to form the centrosome in animal cells. The oldest centriole in the pair can convert to the basal body of a primary cilium in many types of differentiated cells.
- Basal body/axoneme
-
The basal body is a nine-fold microtubule-based cylindrical structure at the base of the axoneme, a (9 + 2) microtubule structure in the flagellum. This ancient structure is present at the apparition of the early eukaryotic cells.
- Microfilament
-
A cytoskeletal filament with a 6-nm diameter that consists of polymerized actin. Microfilaments form the main component of the cellular contractile machinery.
- Cytotaxis
-
An epigenetic process that confers a structural memory in cell reproduction.
- Blebbing
-
The formation of blebs. Blebs are spherical cellular protrusions that occur in many physiological situations and depend on membrane–cortex adhesion.
- Centrin
-
One of a set of proteins that are associated with centrosomal structures in most eukaryotes. Centrins belong to two ancient subfamilies of the calcium-binding, EF-hand superfamily of proteins that are defined by calmodulin.
- Cytokinesis
-
The separation of a cell into two, marked by ingression of the cleavage furrow between the two nuclei.
- Karyokinesis
-
The physical separation of the daughter nuclei at the end of mitosis.
- Lamellipodium
-
A thin, flat extension at the cell periphery that is filled with a branching meshwork of actin filaments.
- Focal adhesion
-
A cellular structure that links the extracellular matrix on the outside of the cell to the actin cytoskeleton inside the cell through integrin receptors.
- Actomyosin
-
A complex of myosin and actin filaments that is responsible for a range of cellular movements in eukaryotic cells. Myosins can translocate vesicles or other cargo on actin filaments.
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Bornens, M. Organelle positioning and cell polarity. Nat Rev Mol Cell Biol 9, 874–886 (2008). https://doi.org/10.1038/nrm2524
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DOI: https://doi.org/10.1038/nrm2524
