Trends in Cell Biology
OpinionThe centrosome in vertebrates: more than a microtubule-organizing center
Section snippets
Centrioles and the centrosome
We begin our argument with a definition of what a centrosome is in vertebrates. Despite recent advances in light microscopy, in the living cell, this organelle still appears as one or two dots, usually located near the nucleus (Fig. 1a). To appreciate fully its structural complexity, the centrosome must be viewed by electron microscopy. With this technique, it is seen to contain two ‘centrioles’, each of which comprises a pinwheel of nine triplet MT ‘blades’ distributed evenly around the
Centrosome functions based on microtubule nucleation
The MTOC activity of the centrosome includes the nucleation and organization of those MTs that form the interphase cytoplasmic MT array (Fig. 1c) and the mitotic spindle (Fig. 1d), as well as cilia (Fig. 1b,f). The first two activities are centred on the nucleation of MTs by sites inside the pericentriolar material, whereas the last activity involves the nucleation of MTs directly from the centriole.
Centrosome function(s) unrelated to MTOC activity
When the centrosome is surgically removed from BSC-1 cells during S phase 13, or destroyed in CV-1 or PtK1 cells during G2 phase by laser ablation 12, the cells continue to progress into and complete mitosis, but the resultant progeny arrest in G1 (Fig. 3a). Importantly, this G1 arrest occurs in spite of the fact that the (now) acentrosomal cells appear to contain normal amounts of microtubules that are organized in a way similar to those of controls. Furthermore, when the MTs in CV-1 (Fig. 4)
Concluding remarks
Traditionally, research on the centrosome in higher animals has focused its ability to nucleate and organize MT arrays during interphase and mitosis. It is now evident, however, that the centrosome is more than just an MTOC. In fact, although the MTOC functions of this organelle are its most visible activity, we argue that they are not essential for the survival and reproduction of individual cells. This is because, with the exception of cilia/flagella formation, functional MT arrays can be
Acknowledgements
C.L.R. and A.K. are supported, in part, by NIH-GMS grants 40198 and 59363.
References (49)
- et al.
Identification and function of the centrosome centromatrix
Biol. Cell
(1999) - et al.
Microsurgical removal of centrosomes blocks cell reproduction and centriole generation in BSC-1 cells
Cell
(1991) Centriole and basal body formation during ciliogenesis revisited
Biol. Cell
(1991)- et al.
De novo formation of centrioles in parthenogenetically activated, diploidized rabbit embryos
Biol. Cell
(1991) Bipolar meiotic spindle formation without chromatin
Curr. Biol.
(1998)The chromosome cycle and the centrosome cycle in the mitotic cycle
Int. Rev. Cytol.
(1987)A model for the proposed roles of different microtubule-based motor proteins in establishing spindle bipolarity
Curr. Biol.
(1998)Centrosome-independent mitotic spindle formation in vertebrates
Curr. Biol.
(2000)- et al.
Morphogenetic properties of microtubules and mitotic spindle assembly
Cell
(1996) Kinetics and regulation of de novo centriole assembly: implications for the mechanism of centriole duplication
Curr. Biol.
(2001)
Dynein and dynactin are localized to astral microtubules and at cortical sites in mitotic epithelial cells
Curr. Biol.
Zygotic development without functional mitotic centrosomes
Curr. Biol.
Exit from mitosis: spindle pole power
Cell
The Bub2p spindle checkpoint links nuclear migration with mitotic exit
Mol. Cell
Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking FIG3B motor protein
Cell
Life cycle analysis of mammalian cells. 1. A method for localizing metabolic events within the life cycle, and its application to the action of colcemid and sublethal doses of X-radiation
Biophys. J.
Mitosis in the Drosophila embryo – in and out of control
Trends Genet.
The Cell in Development and Inheritance
Polar organization of gamma-tubulin in acentriolar mitotic spindles of Drosophila melanogaster cells
J. Cell Sci.
Molecular characteristics of the centrosome
Int. Rev. Cytol.
Glutamylation of centriole and cytoplasmic tubulin in proliferating non-neuronal cells
Cell Motil. Cytoskeleton.
The respective contribution of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells
J. Cell Biol.
Flexible-substratum technique for viewing cells from the side: some in vivo properties of primary (9+0) cilia in cultured kidney epithelia
J. Cell Sci.
‘It takes two to tango’: Understanding how centrosome duplication is regulated throughout the cell cycle
Genes Dev.
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