One to only two: a short history of the centrosome and its duplication

Abstract

This review discusses some of the history of the fundamental, but not fully solved problem of how the centrosome duplicates from one to only two as the cell prepares for mitosis. We start with some of the early descriptions of the centrosome and the remarkably prescient but then controversial inferences drawn concerning its function in the cell. For more than 100 years, one of the most difficult issues for the concept of the centrosome has been to integrate observations that centrosomes appear to be important for spindle assembly in animal cells yet are not evident in higher plant cells and some animal cells. This stirred debate over the existence of centrosomes and their importance. A parallel debate concerned the role of the centrioles in organizing centrosomes. The relatively recent elucidation of bipolar spindle assembly around chromatin allows a re-examination of the role of centrioles in controlling centrosome duplication in animal cells. The problem of how centrosomes precisely double in preparation for mitosis in animal cells has now moved to the mystery of how only one procentriole is assembled at each mother centriole

The interplay between centrosomes and the Hippo tumor suppressor pathway

“…Cells in G 0 or G 1 phase typically contain a single centrosome, comprised of two orthogonal centrioles surrounded by a cloud of pericentriolar material. Similar to DNA replication, centrosome duplication occurs only once during S-phase and generates two centrosomes for G 2 /M (Firat-Karalar and Stearns, 2014, Nigg and Stearns, 2011, Sluder, 2014, Tsou and Stearns, 2006a, Tsou and Stearns, 2006b). The two centrosomes present during mitosis facilitate the formation of a bipolar mitotic spindle and thus promote high fidelity chromosome segregation during anaphase (Hinchcliffe, 2014).…”

“…Extra centrosomes can be generated by mitotic or cytokinetic failures, which produce tetraploid cells with twice the normal number of centrosomes (Davoli and de Lange, 2011, Ganem et al, 2007, Meraldi et al, 2002). Alternatively, extra centrosomes can arise from cellular and/or genetic defects that promote centriole overduplication (Firat-Karalar and Stearns, 2014, Nigg and Stearns, 2011, Sluder, 2014). …”

Atypical centrioles during sexual reproduction

“…Centrioles, centrosomes, asters, and cilia were first discovered in the context of reproductive biology (Wheatley, 1982 ; Scheer, 2014 ; Sluder, 2014 ). Yet, despite a century-long realization that centrioles are fundamental to the initiation of new animal life, the mechanism of centriole inheritance during fertilization and the precise composition of zygotic centrioles remain unclear.…”

“…In the late twentieth century, antibodies against PCM and microtubular proteins (i.e., tubulin) were used to observe centrosomes (Heidemann and Kirschner, 1975 ; McGill and Brinkley, 1975 ; Connolly and Kalnins, 1978 ). Using these antibodies alone, in the absence of electron microscopy, the centriole cannot be identified directly; however, the presence of centrioles can be inferred from the ability to form PCM and to nucleate astral microtubules (Sluder, 2014 ). These inferences must be treated with caution, as tubulin and centrosome-enriched proteins can form centrosome-like structures lacking centrioles.…”

Centrosomes back in the limelight

“…Intriguingly, the onset of formation is preceded by a change in the distribution of the Plk4 kinase from being uniformly distributed around the proximal part of the parental centriole to being concentrated on a single site: this transition may represent a critical symmetry breaking event [38] (also see articles by Kip Sluder [49], as well as by Elif Firat-Karalar and Tim Stearns [50]). Does such Plk4 concentration occur next to a specific triplet microtubule?…”