The centrosome cycle: Centriole biogenesis, duplication and inherent asymmetries (original) (raw)
Luders, J. & Stearns, T. Microtubule-organizing centres: a re-evaluation. Nat. Rev. Mol. Cell Biol.8, 161–167 (2007). PubMed Google Scholar
Goetz, S. C. & Anderson, K. V. The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet.11, 331–344 (2010). PubMedPubMed CentralCAS Google Scholar
Carvalho-Santos, Z., Azimzadeh, J., Pereira-Leal, J. B. & Bettencourt-Dias, M. Evolution: Tracing the origins of centrioles, cilia, and flagella. J. Cell Biol.194, 165–175 (2011). PubMedPubMed CentralCAS Google Scholar
Nigg, E. A. & Raff, J. W. Centrioles, centrosomes, and cilia in health and disease. Cell139, 663–678 (2009). PubMedCAS Google Scholar
Vaughan, S. & Dawe, H. R. Common themes in centriole and centrosome movements. Trends Cell Biol.21, 57–66 (2011). PubMedCAS Google Scholar
Bettencourt-Dias, M., Hildebrandt, F., Pellman, D., Woods, G. & Godinho, S. A. Centrosomes and cilia in human disease. Trends Genet.27, 307–315 (2011). PubMedPubMed CentralCAS Google Scholar
Avidor-Reiss, T. The cellular and developmental program connecting the centrosome and cilium duplication cycle. Semin. Cell Dev. Biol.21, 139–141 (2010). PubMed Google Scholar
Khodjakov, A. et al. De novo formation of centrosomes in vertebrate cells arrested during S phase. J. Cell Biol.158, 1171–1181 (2002). PubMedPubMed CentralCAS Google Scholar
Dammermann, A., Maddox, P. S., Desai, A. & Oegema, K. SAS-4 is recruited to a dynamic structure in newly forming centrioles that is stabilized by the γ-tubulin-mediated addition of centriolar microtubules. J. Cell Biol.180, 771–785 (2008). PubMedPubMed CentralCAS Google Scholar
Loncarek, J., Hergert, P., Magidson, V. & Khodjakov, A. Control of daughter centriole formation by the pericentriolar material. Nat. Cell Biol.10, 322–328 (2008). PubMedPubMed CentralCAS Google Scholar
Strnad, P. et al. Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Dev. Cell13, 203–213 (2007). PubMedPubMed CentralCAS Google Scholar
Andersen, J. S. et al. Proteomic characterization of the human centrosome by protein correlation profiling. Nature426, 570–574 (2003). PubMedCAS Google Scholar
Jakobsen, L. et al. Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods. EMBO J.30, 1520–1535 (2011). PubMedPubMed CentralCAS Google Scholar
Strnad, P. & Gonczy, P. Mechanisms of procentriole formation. Trends Cell Biol.18, 389–396 (2008). PubMedCAS Google Scholar
Dobbelaere, J. et al. A genome-wide RNAi screen to dissect centriole duplication and centrosome maturation in Drosophila. PLoS Biol.6, e224 (2008). PubMedPubMed Central Google Scholar
Kleylein-Sohn, J. et al. Plk4-induced centriole biogenesis in human cells. Dev. Cell13, 190–202 (2007). PubMedCAS Google Scholar
Rodrigues-Martins, A. et al. DSAS-6 organizes a tube-like centriole precursor, and its absence suggests modularity in centriole assembly. Curr. Biol.17, 1465–1472 (2007). PubMedCAS Google Scholar
Rodrigues-Martins, A., Riparbelli, M., Callaini, G., Glover, D. M. & Bettencourt-Dias, M. Revisiting the role of the mother centriole in centriole biogenesis. Science316, 1046–1050 (2007). PubMedCAS Google Scholar
Peel, N., Stevens, N. R., Basto, R. & Raff, J. W. Overexpressing centriole-replication proteins in vivo induces centriole overduplication and de novo formation. Curr. Biol.17, 834–843 (2007). PubMedPubMed CentralCAS Google Scholar
Puklowski, A. et al. The SCF–FBXW5 E3-ubiquitin ligase is regulated by PLK4 and targets HsSAS-6 to control centrosome duplication. Nat. Cell Biol.13, 1004–1009 (2011). PubMedCAS Google Scholar
Kitagawa, D., Busso, C., Fluckiger, I. & Gonczy, P. Phosphorylation of SAS-6 by ZYG-1 is critical for centriole formation in C. elegans embryos. Dev. Cell17, 900–907 (2009). PubMedCAS Google Scholar
Bettencourt-Dias, M. et al. SAK/PLK4 is required for centriole duplication and flagella development. Curr. Biol.15, 2199–2207 (2005). PubMedCAS Google Scholar
Habedanck, R., Stierhof, Y. D., Wilkinson, C. J. & Nigg, E. A. The Polo kinase Plk4 functions in centriole duplication. Nat. Cell Biol.7, 1140–1146 (2005). PubMedCAS Google Scholar
Cunha-Ferreira, I. et al. The SCF/Slimb ubiquitin ligase limits centrosome amplification through degradation of SAK/PLK4. Curr. Biol.19, 43–49 (2009). PubMedCAS Google Scholar
Guderian, G., Westendorf, J., Uldschmid, A. & Nigg, E. A. Plk4 trans-autophosphorylation regulates centriole number by controlling βTrCP-mediated degradation. J. Cell Sci.123, 2163–2169 (2010). PubMedCAS Google Scholar
Holland, A. J., Lan, W., Niessen, S., Hoover, H. & Cleveland, D. W. Polo-like kinase 4 kinase activity limits centrosome overduplication by autoregulating its own stability. J. Cell Biol.188, 191–198 (2010). PubMedPubMed CentralCAS Google Scholar
Rogers, G. C., Rusan, N. M., Roberts, D. M., Peifer, M. & Rogers, S. L. The SCF Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J. Cell Biol.184, 225–239 (2009). PubMedPubMed CentralCAS Google Scholar
Sillibourne, J. E. et al. Autophosphorylation of polo-like kinase 4 and its role in centriole duplication. Mol. Biol. Cell21, 547–561 (2010). PubMedPubMed CentralCAS Google Scholar
Kitagawa, D. et al. PP2A phosphatase acts upon SAS-5 to ensure centriole formation in C. elegans embryos. Dev. Cell20, 550–562 (2011). PubMedCAS Google Scholar
Song, M. H., Liu, Y., Anderson, D. E., Jahng, W. J. & O'Connell, K. F. Protein phosphatase 2A-SUR-6/B55 regulates centriole duplication in C. elegans by controlling the levels of centriole assembly factors. Dev. Cell20, 563–571 (2011). PubMedPubMed CentralCAS Google Scholar
Dammermann, A. et al. Centriole assembly requires both centriolar and pericentriolar material proteins. Dev. Cell7, 815–829 (2004). PubMedCAS Google Scholar
Pelletier, L., O'Toole, E., Schwager, A., Hyman, A. A. & Muller-Reichert, T. Centriole assembly in Caenorhabditis elegans. Nature444, 619–623 (2006). PubMedCAS Google Scholar
Nakazawa, Y., Hiraki, M., Kamiya, R. & Hirono, M. SAS-6 is a cartwheel protein that establishes the 9-fold symmetry of the centriole. Curr. Biol.17, 2169–2174 (2007). PubMedCAS Google Scholar
Gopalakrishnan, J. et al. Self-assembling SAS-6 multimer is a core centriole building block. J. Biol. Chem.285, 8759–8770 (2010). PubMedPubMed CentralCAS Google Scholar
Stevens, N. R., Dobbelaere, J., Brunk, K., Franz, A. & Raff, J. W. Drosophila Ana2 is a conserved centriole duplication factor. J. Cell Biol.188, 313–323 (2010). PubMedPubMed CentralCAS Google Scholar
van Breugel, M. et al. Structures of SAS-6 suggest its organization in centrioles. Science331, 1196–1199 (2011). PubMedCAS Google Scholar
Kohlmaier, G. et al. Overly long centrioles and defective cell division upon excess of the SAS-4-related protein CPAP. Curr. Biol.19, 1012–1018 (2009). PubMedPubMed CentralCAS Google Scholar
Schmidt, T. I. et al. Control of centriole length by CPAP and CP110. Curr. Biol.19, 1005–1011 (2009). PubMedCAS Google Scholar
Tang, C. J., Fu, R. H., Wu, K. S., Hsu, W. B. & Tang, T. K. CPAP is a cell-cycle regulated protein that controls centriole length. Nat. Cell Biol.11, 825–831 (2009). PubMedCAS Google Scholar
Azimzadeh, J. et al. hPOC5 is a centrin-binding protein required for assembly of full-length centrioles. J. Cell Biol.185, 101–114 (2009). PubMedPubMed CentralCAS Google Scholar
Singla, V., Romaguera-Ros, M., Garcia-Verdugo, J. M. & Reiter, J. F. Ofd1, a human disease gene, regulates the length and distal structure of centrioles. Dev. Cell18, 410–424 (2010). PubMedPubMed CentralCAS Google Scholar
Spektor, A., Tsang, W. Y., Khoo, D. & Dynlacht, B. D. Cep97 and CP110 suppress a cilia assembly program. Cell130, 678–690 (2007). PubMedCAS Google Scholar
Tsang, W. Y. et al. CP110 suppresses primary cilia formation through its interaction with CEP290, a protein deficient in human ciliary disease. Dev. Cell15, 187–197 (2008). PubMedPubMed CentralCAS Google Scholar
D'Angiolella, V. et al. SCF(Cyclin F) controls centrosome homeostasis and mitotic fidelity through CP110 degradation. Nature466, 138–142 (2010). PubMedPubMed CentralCAS Google Scholar
Korzeniewski, N., Cuevas, R., Duensing, A. & Duensing, S. Daughter centriole elongation is controlled by proteolysis. Mol. Biol. Cell21, 3942–3951 (2010). PubMedPubMed CentralCAS Google Scholar
Bornens, M. Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol.14, 25–34 (2002). CASPubMed Google Scholar
Cizmecioglu, O. et al. Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome. J. Cell Biol.191, 731–739 (2010). PubMedPubMed CentralCAS Google Scholar
Dzhindzhev, N. S. et al. Asterless is a scaffold for the onset of centriole assembly. Nature467, 714–718 (2010). PubMedCAS Google Scholar
Hatch, E. M., Kulukian, A., Holland, A. J., Cleveland, D. W. & Stearns, T. Cep152 interacts with Plk4 and is required for centriole duplication. J. Cell Biol.191, 721–729 (2010). PubMedPubMed CentralCAS Google Scholar
Conduit, P. T. et al. Centrioles regulate centrosome size by controlling the rate of Cnn incorporation into the PCM. Curr. Biol.20, 2178–2186 (2010). PubMedCAS Google Scholar
Stevens, N. R., Roque, H. & Raff, J. W. DSas-6 and Ana2 coassemble into tubules to promote centriole duplication and engagement. Dev. Cell19, 913–919 (2010). PubMedPubMed CentralCAS Google Scholar
Tsou, M. F. & Stearns, T. Mechanism limiting centrosome duplication to once per cell cycle. Nature442, 947–951 (2006). PubMedCAS Google Scholar
Tsou, M. F. et al. Polo kinase and separase regulate the mitotic licensing of centriole duplication in human cells. Dev. Cell17, 344–354 (2009). PubMedPubMed CentralCAS Google Scholar
Uhlmann, F., Wernic, D., Poupart, M. A., Koonin, E. V. & Nasmyth, K. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell103, 375–386 (2000). PubMedCAS Google Scholar
Nigg, E. A. Centrosome duplication: of rules and licenses. Trends Cell Biol.17, 215–221 (2007). PubMedCAS Google Scholar
Schöckel, L., Möckel, M., Mayer, B., Boos, D. & Stemmann, O. Cleavage of cohesin rings coordinates the separation of centrioles and chromatids. Nat. Cell Biol. 13, 966–972 (2011).
Mayor, T., Stierhof, Y. D., Tanaka, K., Fry, A. M. & Nigg, E. A. The centrosomal protein C-Nap1 is required for cell cycle-regulated centrosome cohesion. J. Cell Biol.151, 837–846 (2000). PubMedPubMed CentralCAS Google Scholar
Bahe, S., Stierhof, Y. D., Wilkinson, C. J., Leiss, F. & Nigg, E. A. Rootletin forms centriole-associated filaments and functions in centrosome cohesion. J. Cell Biol.171, 27–33 (2005). PubMedPubMed CentralCAS Google Scholar
Yang, J., Adamian, M. & Li, T. Rootletin interacts with C-Nap1 and may function as a physical linker between the pair of centrioles/basal bodies in cells. Mol. Biol. Cell17, 1033–1040 (2006). PubMedPubMed CentralCAS Google Scholar
Graser, S., Stierhof, Y. D. & Nigg, E. A. Cep68 and Cep215 (Cdk5rap2) are required for centrosome cohesion. J. Cell Sci.120, 4321–4331 (2007). CASPubMed Google Scholar
Piel, M., Meyer, P., Khodjakov, A., Rieder, C. L. & Bornens, M. The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J. Cell Biol.149, 317–330 (2000). PubMedPubMed CentralCAS Google Scholar
Piel, M., Nordberg, J., Euteneuer, U. & Bornens, M. Centrosome-dependent exit of cytokinesis in animal cells. Science291, 1550–1553 (2001). PubMedCAS Google Scholar
Fry, A. M. et al. C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J. Cell Biol.141, 1563–1574 (1998). PubMedPubMed CentralCAS Google Scholar
Helps, N. R., Luo, X., Barker, H. M. & Cohen, P. T. NIMA-related kinase 2 (Nek2), a cell-cycle-regulated protein kinase localized to centrosomes, is complexed to protein phosphatase 1. Biochem. J.349, 509–518 (2000). PubMedPubMed CentralCAS Google Scholar
Bertran, M. T. et al. Nek9 is a Plk1-activated kinase that controls early centrosome separation through Nek6/7 and Eg5. EMBO J.30, 2634–2647 (2011). PubMedPubMed CentralCAS Google Scholar
Mardin, B. R. et al. Components of the Hippo pathway cooperate with Nek2 kinase to regulate centrosome disjunction. Nat. Cell Biol.12, 1166–1176 (2010). PubMedPubMed CentralCAS Google Scholar
Mardin, B. R., Agircan, F. G., Lange, C. & Schiebel, E. Plk1 Controls the Nek2A-PP1γ antagonism in centrosome disjunction. Curr. Biol.21, 1145–1151 (2011). PubMedCAS Google Scholar
Hergovich, A. et al. The MST1 and hMOB1 tumor suppressors control human centrosome duplication by regulating NDR kinase phosphorylation. Curr. Biol.19, 1692–1702 (2009). PubMedCAS Google Scholar
Hardy, P. A. & Zacharias, H. Reappraisal of the Hansemann-Boveri hypothesis on the origin of tumors. Cell Biol. Int.29, 983–992 (2005). PubMed Google Scholar
Ganem, N. J., Godinho, S. A. & Pellman, D. A mechanism linking extra centrosomes to chromosomal instability. Nature460, 278–282 (2009). PubMedPubMed CentralCAS Google Scholar
Silkworth, W. T., Nardi, I. K., Scholl, L. M. & Cimini, D. Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation in cancer cells. PLoS One4, e6564 (2009). PubMedPubMed Central Google Scholar
Kwon, M. et al. Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev.22, 2189–2203 (2008). PubMedPubMed CentralCAS Google Scholar
Nigg, E. A. Centrosome aberrations: cause or consequence of cancer progression? Nat. Rev. Cancer2, 815–825 (2002). PubMedCAS Google Scholar
Sibon, O. C., Kelkar, A., Lemstra, W. & Theurkauf, W. E. DNA-replication/DNA-damage-dependent centrosome inactivation in Drosophila embryos. Nat. Cell Biol.2, 90–95 (2000). PubMedCAS Google Scholar
Hut, H. M. et al. Centrosomes split in the presence of impaired DNA integrity during mitosis. Mol. Biol. Cell14, 1993–2004 (2003). PubMedPubMed CentralCAS Google Scholar
Kramer, A. et al. Centrosome-associated Chk1 prevents premature activation of cyclin-B–Cdk1 kinase. Nat. Cell Biol.6, 884–891 (2004). PubMed Google Scholar
Matsuyama, M. et al. Nuclear Chk1 prevents premature mitotic entry. J. Cell Sci.124, 2113–2119 (2011). PubMedCAS Google Scholar
Balczon, R. et al. Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea-arrested Chinese hamster ovary cells. J. Cell Biol.130, 105–115 (1995). PubMedCAS Google Scholar
Inanc, B., Dodson, H. & Morrison, C. G. A centrosome-autonomous signal that involves centriole disengagement permits centrosome duplication in G2 phase after DNA damage. Mol. Biol. Cell21, 3866–3877 (2010). PubMedPubMed CentralCAS Google Scholar
Loncarek, J., Hergert, P. & Khodjakov, A. Centriole reduplication during prolonged interphase requires procentriole maturation governed by Plk1. Curr. Biol.20, 1277–1282 (2010). PubMedPubMed CentralCAS Google Scholar
Wang, W. J., Soni, R. K., Uryu, K. & Bryan Tsou, M. F. The conversion of centrioles to centrosomes: essential coupling of duplication with segregation. J. Cell Biol.193, 727–739 (2011). PubMedPubMed CentralCAS Google Scholar
Hoyer-Fender, S. Centriole maturation and transformation to basal body. Semin. Cell Dev. Biol.21, 142–147 (2010). PubMed Google Scholar
Paintrand, M., Moudjou, M., Delacroix, H. & Bornens, M. Centrosome organization and centriole architecture: their sensitivity to divalent cations. J. Struct. Biol.108, 107–128 (1992). PubMedCAS Google Scholar
Graser, S. et al. Cep164, a novel centriole appendage protein required for primary cilium formation. J. Cell Biol.179, 321–330 (2007). PubMedPubMed CentralCAS Google Scholar
Mahjoub, M. R., Xie, Z. & Stearns, T. Cep120 is asymmetrically localized to the daughter centriole and is essential for centriole assembly. J. Cell Biol.191, 331–346 (2010). PubMedPubMed CentralCAS Google Scholar
Anderson, C. T. & Stearns, T. Centriole age underlies asynchronous primary cilium growth in mammalian cells. Curr. Biol.19, 1498–1502 (2009). PubMedPubMed CentralCAS Google Scholar
Yamashita, Y. M., Jones, D. L. & Fuller, M. T. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science301, 1547–1550 (2003). PubMedCAS Google Scholar
Rusan, N. M. & Peifer, M. A role for a novel centrosome cycle in asymmetric cell division. J. Cell Biol.177, 13–20 (2007). PubMedPubMed CentralCAS Google Scholar
Rebollo, E. et al. Functionally unequal centrosomes drive spindle orientation in asymmetrically dividing Drosophila neural stem cells. Dev. Cell12, 467–474 (2007). PubMedCAS Google Scholar
Januschke, J. & Gonzalez, C. The interphase microtubule aster is a determinant of asymmetric division orientation in Drosophila neuroblasts. J. Cell Biol.188, 693–706 (2010). PubMedPubMed CentralCAS Google Scholar
Januschke, J., Llamazares, S., Reina, J. & Gonzalez, C. Drosophila neuroblasts retain the daughter centrosome. Nat. Commun.2, 243 (2011). PubMed Google Scholar
Wang, X. et al. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature461, 947–955 (2009). PubMedPubMed CentralCAS Google Scholar
Fuentealba, L. C., Eivers, E., Geissert, D., Taelman, V. & De Robertis, E. M. Asymmetric mitosis: Unequal segregation of proteins destined for degradation. Proc. Natl Acad. Sci. USA105, 7732–7737 (2008). PubMedPubMed CentralCAS Google Scholar
Lambert, J. D. & Nagy, L. M. Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature420, 682–686 (2002). PubMedCAS Google Scholar