Centrosome Cycle

Abstract

During the cell division cycle, duplication of the centrosome and segregation of the two daughter centrosomes dictate the assembly of the mitotic spindle and thus determine the plane of the cleavage furrow. Recent results have both modified and reinforced views about the role of the centrosome in the control of cell cycle progression in animal cells.

Keywords: centriole; microtubules; cell division cycle; cytokinesis

Figure 1.

Cartoon of a centrosome isolated from vertebrate cells. The centrosome contains a mother centriole, possessing two sets of distally associated appendages, and a daughter centriole, which has assembled in the preceding cell cycle by orthogonal budding from the mother centriole. Schematic localization of γ‐tubulin, a marker of microtubule nucleation, and of centrin, an early marker of centrosome duplication, is indicated. Centrosomal‐associated centrin is confined within the distal lumen of each centriole, where a conspicuous luminal material is present, and γ‐tubulin is distributed in the pericentriolar matrix but is often closely associated with centrioles.

Figure 2.

The duplication cycle of the centrosome in animal cells. (a) The centrosome as observed in living cells stably expressing a centrin‐green fluorescent protein (GFP) fusion protein, which concentrates in the lumen of the two centrioles and which is an early marker of duplication (see Figure 1). The centrosome is observed as a centriole pair in G1. The initiation of procentriole budding at the G1‐S border, the separation of the daughter centrosomes in late G2 and the two centriole pairs at the mitotic poles can be monitored. (b) Corresponding cartoon. The duplication of the centriole pair involves the orthogonal budding of a procentriole on each centriole in late G1, the eventual maturation of the former daughter centriole in late G2, the semiconservative segregation of the two centriole pairs at the G2‐M transition. The disorientation of the centrioles from their orthogonal configuration takes place long before the end of cell division (not represented). The maturation of the centrosomal matrix involves a progressive accumulation from early G1, where it is mainly associated with the mother centriole, to M phase, and several structural and biochemical modifications in late G2, as demonstrated by the disappearance of the appendages and the appearance of a reactivity with antiphosphoepitope antibodies (this is represented by a darkening of the pericentriolar matrix). Finally, an abrupt dispersion or degradation of the matrix takes place at the metaphase to anaphase transition. The doubling of the centrosome–microtubule system parallels the doubling of chromosomes and accordingly could be involved in the maintenance of the cell mass and ploidy ratio. (c) Major kinase activities that are necessary, respectively, for the initiation of centrosome duplication, the duplication process and the separation of the duplicated centrosomes at the onset of mitosis. Ca, calcium; CaM, calmodulin; Cdk, cyclin‐dependent kinase.

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References

Adams IR and Kilmartin JV (1999) Localization of core spindle pole body (SPB) components during SPB duplication in Saccharomyces cerevisiae. Journal of Cell Biology 145: 809–823.

Adams IR and Kilmartin JV (2000) Spindle pole body duplication: a model for centrosome duplication? Trends in Cell Biology 10: 329–335.

Bailly E, Doree M, Nurse P and Bornens M (1989) p34cdc2 is located in both nucleus and cytoplasm; part is centrosomally associated at G2/M and enters vesicles at anaphase. EMBO Journal 8: 3985–3995.

Balczon R, Bao L, Zimmer WE, et al. (1995) Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea‐arrested Chinese hamster ovary cells. Journal of Cell Biology 130: 105–115.

Bobinnec Y, Khodjakov A, Mir LM, et al. (1998) Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells. Journal of Cell Biology 143: 1575–1589.

Bornens M (2002) Centrosome composition and microtubule anchoring mechanisms. Current Opinion in Cell Biology 14: 25–34.

Bullitt E, Rout MP, Kilmartin JV and Akey CW (1997) The yeast spindle pole body is assembled around a central crystal of Spc42p. Cell 89: 1077–1086.

Freed E, Lacey KR, Huie P, et al. (1999) Components of an SCF ubiquitin ligase localize to the centrosome and regulate the centrosome duplication cycle. Genes and Development 13: 2242–2257.

Gard DL, Hafezi S, Zhang T and Doxsey SJ (1990) Centrosome duplication continues in cycloheximide‐treated Xenopus blastulae in the absence of a detectable cell cycle. Journal of Cell Biology 110: 2033–2042.

Golsteyn RM, Mundt KE, Fry AM and Nigg EA (1995) Cell cycle regulation of the activity and subcellular localization of Plk1, a human protein kinase implicated in mitotic spindle function. Journal of Cell Biology 129: 1617–1628.

Haase SB, Winey M and Reed SI (2001) Multi‐step control of spindle pole body duplication by cyclin‐dependent kinase. Nature Cell Biology 3: 38–42.

Hinchcliffe EH, Li C, Thompson EA, Maller JL and Sluder G (1999) Requirement of Cdk2‐cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science 283: 851–854.

Hinchcliffe EH, Miller FJ, Cham M, Khodjakov A and Sluder G (2001) Requirement of a centrosomal activity for cell cycle progression through G1 into S phase. Science 291: 1499–1502.

Khodjakov A and Rieder CL (2001) Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. Journal of Cell Biology 153: 237–242.

Khodjakov A, Cole RW, Oakley BR and Rieder CL (2000) Centrosome‐independent mitotic spindle formation in vertebrates. Current Biology 10: 59–67.

King RW, Deshaies RJ, Peters JM and Kirschner MW (1996) How proteolysis drives the cell cycle. Science 274: 1652–1659.

Kumagai A and Dunphy WG (1996) Purification and molecular cloning of Plx1, a Cdc25‐regulatory kinase from Xenopus egg extracts. Science 273: 1377–1380.

Lange BM (2002) Integration of the centrosome in the cell cycle control, stress response and signal transduction pathways. Current Opinion in Cell Biology 14: 35–43.

Matsumoto Y and Maller J (2002) Calcium, calmodulin and caMKII requirement for initiation of centrosome duplication in Xenopus egg extracts. Science 295: 499–502.

Middendorp S, Küntziger T, Abraham Y et al. (2000) A role for centrin 3 in centrosome reproduction. Journal of Cell Biology 148: 405–416.

Nagano H, Hirai S, Okano K and Ikegami S (1981) Achromosomal cleavage of fertilized starfish eggs in the presence of aphidicolin. Developmental Biology 85: 409–415.

Nigg EA (2002) Centrosome aberrations: cause or consequence of cancer progression? Nature Reviews 2: 815–825.

Picard A, Harricane MC, Labbe JC and Doree M (1988) Germinal vesicle components are not required for the cell‐cycle oscillator of the early starfish embryo. Developmental Biology 128: 121–128.

Piel M, Meyer P, Khodjakov A, Rieder CL and Bornens M (2000) The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. Journal of Cell Biology 149: 317–330.

Piel M, Nordberg J, Euteneuer U and Bornens M (2001) Centrosome‐dependent exit of cytokinesis in animal cells. Science 291: 1550–1553.

Sluder G and Rieder CL (1985) Centriole number and the reproductive capacity of spindle poles. Journal of Cell Biology 100: 887–896.

Spang A, Courtney I, Fackler U, Matzner M and Schiebel E (1993) The calcium‐binding protein cell division cycle 31 of Saccharomyces cerevisiae is a component of the half bridge of the spindle pole body. Journal of Cell Biology 123: 405–416.

Tournier F and Bornens M (1994) Cell cycle regulation of centrosome function. In: Hyams JS and Lloyd CW (eds) Microtubules, pp 303–324. New York: Wiley.

Ueda M, Schliwa M and Euteneuer U (1999) Unusual centrosome cycle in Dictyostelium: correlation of dynamic behavior and structural changes. Molecular Biology of the Cell 10: 151–160.

Weiss E and Winey M (1996) The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint. Journal of Cell Biology 132: 111–123.

Further Reading

Bornens M (ed.) (1999) Centrosome, Part I–II. Biology of the Cell 91: 291–477.

Kalnins V (ed.) (1992) The Centrosome. New York: Academic Press.

Palazzo R and Schatten GP (eds) (2000) Centrosome in cell replication and early development. Current Topics in Developmental Biology 49: 1–483.

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How to Cite close
Bornens, Michel(May 2003) Centrosome Cycle. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1038/npg.els.0001362]