Acknowledgement
This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. NRF-2019R1A2C22002726).
References
- Antao, N.V., Marcet-Ortega, M., Cifani, P., Kentsis, A., and Foley, E.A. (2019). A cancer-associated missense mutation in PP2A-Aα increases centrosome clustering during mitosis. iScience 19, 74-82. https://doi.org/10.1016/j.isci.2019.07.018
- Balczon, R., Bao, L., Zimmer, W.E., Brown, K., Zinkowski, R.P., and Brinkley, B.R. (1995). 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. https://doi.org/10.1083/jcb.130.1.105
- Basto, R., Brunk, K., Vinadogrova, T., Peel, N., Franz, A., Khodjakov, A., and Raff, J.W. (2008). Centrosome amplification can initiate tumorigenesis in flies. Cell 133, 1032-1042. https://doi.org/10.1016/j.cell.2008.05.039
- Baudoin, N.C., Nicholson, J.M., Soto, K., Martin, O., Chen, J., and Cimini, D. (2020). Asymmetric clustering of centrosomes defines the early evolution of tetraploid cells. Elife 9, e54565. https://doi.org/10.7554/eLife.54565
- Bettencourt-Dias, M., Rodrigues-Martins, A., Carpenter, L., Riparbelli, M., Lehmann, L., Gatt, M.K., Carmo, N., Balloux, F., Callaini, G., and Glover, D.M. (2005). SAK/PLK4 is required for centriole duplication and flagella development. Curr. Biol. 15, 2199-2207. https://doi.org/10.1016/j.cub.2005.11.042
- Burigotto, M., Mattivi, A., Migliorati, D., Magnani, G., Valentini, C., Roccuzzo, M., Offterdinger, M., Pizzato, M., Schmidt, A., Villunger, A., et al. (2021). Centriolar distal appendages activate the centrosomePIDDosome-p53 signalling axis via ANKRD26. EMBO J. 40, e104844.
- Cabral, G., Sans, S.S., Cowan, C.R., and Dammermann, A. (2013). Multiple mechanisms contribute to centriole separation in C. elegans. Curr. Biol. 23, 1380-1387. https://doi.org/10.1016/j.cub.2013.06.043
- Castellanos, E., Dominguez, P., and Gonzalez, C. (2008). Centrosome dysfunction in Drosophila neural stem cells causes tumors that are not due to genome instability. Curr. Biol. 18, 1209-1214. https://doi.org/10.1016/j.cub.2008.07.029
- Chan, J.Y. (2011). A clinical overview of centrosome amplification in human cancers. Int. J. Biol. Sci. 7, 1122-1144. https://doi.org/10.7150/ijbs.7.1122
- Chang, J., Cizmecioglu, O., Hoffmann, I., and Rhee, K. (2010). PLK2 phosphorylation is critical for CPAP function in procentriole formation during the centrosome cycle. EMBO J. 29, 2395-2406. https://doi.org/10.1038/emboj.2010.118
- Chiba, S., Okuda, M., Mussman, J.G., and Fukasawa, K. (2000). Genomic convergence and suppression of centrosome hyperamplification in primary p53-/- cells in prolonged culture. Exp. Cell Res. 258, 310-321. https://doi.org/10.1006/excr.2000.4916
- Coelho, P.A., Bury, L., Shahbazi, M.N., Liakath-Ali, K., Tate, P.H., Wormald, S., Hindley, C.J., Huch, M., Archer, J., Skarnes, W.C., et al. (2015). Overexpression of Plk4 induces centrosome amplification, loss of primary cilia and associated tissue hyperplasia in the mouse. Open Biol. 5, 150209. https://doi.org/10.1098/rsob.150209
- Davoli, T. and de Lange, T. (2011). The causes and consequences of polyploidy in normal development and cancer. Annu. Rev. Cell Dev. Biol. 27, 585-610. https://doi.org/10.1146/annurev-cellbio-092910-154234
- Dikovskaya, D., Schiffmann, D., Newton, I.P., Oakley, A., Kroboth, K., Sansom, O., Jamieson, T.J., Meniel, V., Clarke, A., and Nathke, I.S. (2007). Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J. Cell Biol. 176, 183-195. https://doi.org/10.1083/jcb.200610099
- Drosopoulos, K., Tang, C., Chao, W.C.H., and Linardopoulos, S. (2014). APC/C is an essential regulator of centrosome clustering. Nat. Commun. 5, 3686. https://doi.org/10.1038/ncomms4686
- Dzhindzhev, N.S., Tzolovsky, G., Lipinszki, Z., Schneider, S., Lattao, R., Fu, J., Debski, J., Dadlez, M., and Glover, D.M. (2014). Plk4 phosphorylates Ana2 to trigger Sas6 recruitment and procentriole formation. Curr. Biol. 24, 2526-2532. https://doi.org/10.1016/j.cub.2014.08.061
- Edgar, B.A. and Orr-Weaver, T.L. (2001). Endoreplication cell cycles: more for less. Cell 105, 297-306. https://doi.org/10.1016/S0092-8674(01)00334-8
- Fan, G., Sun, L., Shan, P., Zhang, X., Huan, J., Zhang, X., Li, D., Wang, T., Wei, T., Zhang, X., et al. (2015). Loss of KLF14 triggers centrosome amplification and tumorigenesis. Nat. Commun. 6, 8450. https://doi.org/10.1038/ncomms9450
- Fava, L.L., Schuler, F., Sladky, V., Haschka, M.D., Soratroi, C., Eiterer, L., Demetz, E., Weiss, G., Geley, S., Nigg, E.A., et al. (2017). The PIDDosome activates p53 in response to supernumerary centrosomes. Genes Dev. 31, 34-45. https://doi.org/10.1101/gad.289728.116
- Fu, J., Lipinszki, Z., Rangone, H., Min, M., Mykura, C., Chao-Chu, J., Schneider, S., Dzhindzhev, N.S., Gottardo, M., Riparbelli, M.G., et al. (2016). Conserved molecular interactions in centriole-to-centrosome conversion. Nat. Cell Biol. 18, 87-99. https://doi.org/10.1038/ncb3274
- Fukasawa, K., Choi, T., Kuriyama, R., Rulong, S., and Vande Woude, G.F. (1996). Abnormal centrosome amplification in the absence of p53. Science 271, 1744-1747. https://doi.org/10.1126/science.271.5256.1744
- Galipeau, P.C., Cowan, D.S., Sanchez, C.A., Barrett, M.T., Emond, M.J., Levine, D.S., Rabinovitch, P.S., and Reid, B.J. (1996). 17p (p53) allelic losses, 4N (G2/tetraploid) populations, and progression to aneuploidy in Barrett's esophagus. Proc. Natl. Acad. Sci. U. S. A. 93, 7081-7084. https://doi.org/10.1073/pnas.93.14.7081
- Galofre, C., Asensio, E., Ubach, M., Torres, I.M., Quintanilla, I., Castells, A., and Camps, J. (2020). Centrosome reduction in newly-generated tetraploid cancer cells obtained by separase depletion. Sci. Rep. 10, 9152. https://doi.org/10.1038/s41598-020-65975-1
- Ganem, N.J., Cornils, H., Chiu, S.Y., O'Rourke, K.P., Arnaud, J., Yimlamai, D., Thery, M., Camargo, F.D., and Pellman, D. (2014). Cytokinesis failure triggers hippo tumor suppressor pathway activation. Cell 158, 833-848. https://doi.org/10.1016/j.cell.2014.06.029
- Ganem, N.J., Godinho, S.A., and Pellman, D. (2009). A mechanism linking extra centrosomes to chromosomal instability. Nature 460, 278-282. https://doi.org/10.1038/nature08136
- Ganier, O., Schnerch, D., Oertle, P., Lim, R.Y., Plodinec, M., and Nigg, E.A. (2018). Structural centrosome aberrations promote non-cell-autonomous invasiveness. EMBO J. 37, e98576. https://doi.org/10.15252/embj.201798576
- Godinho, S.A. and Pellman, D. (2014). Causes and consequences of centrosome abnormalities in cancer. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130467. https://doi.org/10.1098/rstb.2013.0467
- Godinho, S.A., Picone, R., Burute, M., Dagher, R., Su, Y., Leung, C.T., Polyak, K., Brugge, J.S., Thery, M., and Pellman, D. (2014). Oncogene-like induction of cellular invasion from centrosome amplification. Nature 510, 167-171. https://doi.org/10.1038/nature13277
- Habedanck, R., Stierhof, Y.D., Wilkinson, C.J., and Nigg, E.A. (2005). The Polo kinase Plk4 functions in centriole duplication. Nat. Cell Biol. 7, 1140-1146. https://doi.org/10.1038/ncb1320
- Hirono, M. (2014). Cartwheel assembly. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130458. https://doi.org/10.1098/rstb.2013.0458
- Holland, A.J. and Cleveland, D.W. (2009). Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat. Rev. Mol. Cell Biol. 10, 478-487. https://doi.org/10.1038/nrm2718
- Inanc, B., Dodson, H., and Morrison, C.G. (2010). A centrosome-autonomous signal that involves centriole disengagement permits centrosome duplication in G2 phase after DNA damage. Mol. Biol. Cell 21, 3866-3877. https://doi.org/10.1091/mbc.E10-02-0124
- Jung, G.I. and Rhee, K. (2021). Triple deletion of TP53, PCNT, and CEP215 promotes centriole amplification in the M phase. Cell Cycle 20, 1500-1517. https://doi.org/10.1080/15384101.2021.1950386
- Kim, J., Kim, J., and Rhee, K. (2019). PCNT is critical for the association and conversion of centrioles to centrosomes during mitosis. J. Cell Sci. 132, jcs225789. https://doi.org/10.1242/jcs.225789
- Kim, J., Lee, K., and Rhee, K. (2015). PLK1 regulation of PCNT cleavage ensures fidelity of centriole separation during mitotic exit. Nat. Commun. 6, 10076. https://doi.org/10.1038/ncomms10076
- Kleylein-Sohn, J., Westendorf, J., Le Clech, M., Habedanck, R., Stierhof, Y.D., and Nigg, E.A. (2007). Plk4-induced centriole biogenesis in human cells. Dev. Cell 13, 190-202. https://doi.org/10.1016/j.devcel.2007.07.002
- Kohlmaier, G., Loncarek, J., Meng, X., McEwen, B.F., Mogensen, M.M., Spektor, A., Dynlacht, B.D., Khodjakov, A., and Gonczy, P. (2009). Overly long centrioles and defective cell division upon excess of the SAS-4-related protein CPAP. Curr. Biol. 19, 1012-1018. https://doi.org/10.1016/j.cub.2009.05.018
- Kong, D., Sahabandu, N., Sullenberger, C., Vasquez-Limeta, A., Luvsanjav, D., Lukasik, K., and Loncarek, J. (2020). Prolonged mitosis results in structurally aberrant and over-elongated centrioles. J. Cell Biol. 219, e201910019. https://doi.org/10.1083/jcb.201910019
- Krzywicka-Racka, A. and Sluder, G. (2011). Repeated cleavage failure does not establish centrosome amplification in untransformed human cells. J. Cell Biol. 194, 199-207. https://doi.org/10.1083/jcb.201101073
- Kulukian, A., Holland, A.J., Vitre, B., Naik, S., Cleveland, D.W., and Fuchs, E. (2015). Epidermal development, growth control, and homeostasis in the face of centrosome amplification. Proc. Natl. Acad. Sci. U. S. A. 112, E6311-E6320.
- Kuznetsova, A.Y., Seget, K., Moeller, G.K., de Pagter, M.S., de Roos, J.A., Durrbaum, M., Kuffer, C., Muller, S., Zaman, G.J., Kloosterman, W.P., et al. (2015). Chromosomal instability, tolerance of mitotic errors and multidrug resistance are promoted by tetraploidization in human cells. Cell Cycle 14, 2810-2820. https://doi.org/10.1080/15384101.2015.1068482
- Kwon, M., Bagonis, M., Danuser, G., and Pellman, D. (2015). Direct microtubule-binding by Myosin-10 orients centrosomes toward retraction fibers and subcortical actin clouds. Dev. Cell 34, 323-337. https://doi.org/10.1016/j.devcel.2015.06.013
- Kwon, M., Godinho, S.A., Chandhok, N.S., Ganem, N.J., Azioune, A., Thery, M., and Pellman, D. (2008). Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev. 22, 2189-2203. https://doi.org/10.1101/gad.1700908
- Lambrus, B.G., Daggubati, V., Uetake, Y., Scott, P.M., Clutario, K.M., Sluder, G., and Holland, A.J. (2016). A USP28-53BP1-p53-p21 signaling axis arrests growth after centrosome loss or prolonged mitosis. J. Cell Biol. 214, 143-153. https://doi.org/10.1083/jcb.201604054
- Lambrus, B.G. and Holland, A.J. (2017). A new mode of mitotic surveillance. Trends Cell Biol. 27, 314-321. https://doi.org/10.1016/j.tcb.2017.01.004
- Larsson, L.I., Bjerregaard, B., and Talts, J.F. (2008). Cell fusions in mammals. Histochem. Cell Biol. 129, 551-561. https://doi.org/10.1007/s00418-008-0411-1
- Leber, B., Maier, B., Fuchs, F., Chi, J., Riffel, P., Anderhub, S., Wagner, L., Ho, A.D., Salisbury, J.L., Boutros, M., et al. (2010). Proteins required for centrosome clustering in cancer cells. Sci. Transl. Med. 2, 33ra38. https://doi.org/10.1126/scitranslmed.3000915
- Lee, K. and Rhee, K. (2012). Separase-dependent cleavage of pericentrin B is necessary and sufficient for centriole disengagement during mitosis. Cell Cycle 11, 2476-2485. https://doi.org/10.4161/cc.20878
- Levine, M.S., Bakker, B., Boeckx, B., Moyett, J., Lu, J., Vitre, B., Spierings, D.C., Lansdorp, P.M., Cleveland, D.W., Lambrechts, D., et al. (2017). Centrosome amplification is sufficient to promote spontaneous tumorigenesis in mammals. Dev. Cell 40, 313-322.e5. https://doi.org/10.1016/j.devcel.2016.12.022
- Liao, Z., Zhang, H., Fan, P., Huang, Q., Dong, K., Qi, Y., Song, J., Chen, L., Liang, H., Chen, X., et al. (2019). High PLK4 expression promotes tumor progression and induces epithelial-mesenchymal transition by regulating the Wnt/β-catenin signaling pathway in colorectal cancer. Int. J. Oncol. 54, 479-490.
- Loncarek, J., Hergert, P., and Khodjakov, A. (2010). Centriole reduplication during prolonged interphase requires procentriole maturation governed by Plk1. Curr. Biol. 20, 1277-1282. https://doi.org/10.1016/j.cub.2010.05.050
- Marteil, G., Guerrero, A., Vieira, A.F., de Almeida, B.P., Machado, P., Mendonca, S., Mesquita, M., Villarreal, B., Fonseca, I., Francia, M.E., et al. (2018). Over-elongation of centrioles in cancer promotes centriole amplification and chromosome missegregation. Nat. Commun. 9, 1258. https://doi.org/10.1038/s41467-018-03641-x
- Marthiens, V., Rujano, M.A., Pennetier, C., Tessier, S., Paul-Gilloteaux, P., and Basto, R. (2013). Centrosome amplification causes microcephaly. Nat. Cell Biol. 15, 731-740. https://doi.org/10.1038/ncb2746
- Matsuo, K., Ohsumi, K., Iwabuchi, M., Kawamata, T., Ono, Y., and Takahashi, M. (2012). Kendrin is a novel substrate for separase involved in the licensing of centriole duplication. Curr. Biol. 22, 915-921. https://doi.org/10.1016/j.cub.2012.03.048
- McCoy, R.C., Demko, Z., Ryan, A., Banjevic, M., Hill, M., Sigurjonssen, S., Robinowitz, M., Fraser, H., and Petrov, D.A. (2015). Common variants spanning PLK4 are associated with mitotic-origin aneuploidy in human embryos. Science 348, 235-238. https://doi.org/10.1126/science.aaa3337
- Mikeladze-Dvali, T., von Tobel, L., Strnad, P., Knott, G., Leonhardt, H., Schermelleh, L., and Gonczy, P. (2012). Analysis of centriole elimination during C. elegans oogenesis. Development 139, 1670-1679. https://doi.org/10.1242/dev.075440
- Nigg, E.A. (2006). Origins and consequences of centrosome abberations in human cancers. Int. J. Cancer 119, 2717-2723. https://doi.org/10.1002/ijc.22245
- Nigg, E.A. and Holland, A.J. (2018). Once and only once: mechanisms of centriole duplication and their deregulation in disease. Nat. Rev. Mol. Cell Biol. 19, 297-312. https://doi.org/10.1038/nrm.2017.127
- Nigg, E.A. and Raff, J.W. (2009). Centrioles, centrosomes, and cilia in health and disease. Cell 139, 663-678. https://doi.org/10.1016/j.cell.2009.10.036
- O'Connell, K.F., Caron, C., Kopish, K.R., Hurd, D.D., Kemphues, K.J., Li, Y., and White, J.G. (2001). The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo. Cell 105, 547-558. https://doi.org/10.1016/S0092-8674(01)00338-5
- Ohta, M., Ashikawa, T., Nozaki, Y., Kozuka-Hata, H., Goto, H., Inagaki, M., Oyama, M., and Kitagawa, D. (2014). Direct interaction of Plk4 with STIL ensures formation of a single procentriole per parental centriole. Nat. Commun. 5, 5267. https://doi.org/10.1038/ncomms6267
- Olaharski, A.J., Sotelo, R., Solorza-Luna, G., Gonsebatt, M.E., Guzman, P., Mohar, A., and Eastmond, D.A. (2006). Tetraploidy and chromosomal instability are early events during cervical carcinogenesis. Carcinogenesis 27, 337-343. https://doi.org/10.1093/carcin/bgi218
- Pihan, G.A., Wallace, J., Zhou, Y., and Doxsey, S.J. (2003). Centrosome abnormalities and chromosome instability occur together in pre-invasive carcinomas. Cancer Res. 63, 1398-1404.
- Potapova, T.A., Seidel, C.W., Box, A.C., Rancati, G., and Li, R. (2016). Transcriptome analysis of tetraploid cells identifies cyclin D2 as a facilitator of adaptation to genome doubling in the presence of p53. Mol. Biol. Cell 27, 3065-3084. https://doi.org/10.1091/mbc.E16-05-0268
- Quintyne, N.J., Reing, J.E., Hoffelder, D.R., Gollin, S.M., and Saunders, W.S. (2005). Spindle multipolarity is prevented by centrosomal clustering. Science 307, 127-129. https://doi.org/10.1126/science.1104905
- Raff, J.W. and Basto, R. (2017). Centrosome amplification and cancer: a question of sufficiency. Dev. Cell 40, 217-218. https://doi.org/10.1016/j.devcel.2017.01.009
- Reider, C.L. (2011). Mitosis in vertebrates: the G2/M and M/A transitions and their associated checkpoints. Chromosome Res. 19, 291-306. https://doi.org/10.1007/s10577-010-9178-z
- Sabino, D., Gogendeau, D., Gambarotto, D., Nano, M., Pennetier, C., Dingli, F., Arras, G., Loew, D., and Basto, R. (2015). Moesin is a major regulator of centrosome behavior in epithelial cells with extra centrosomes. Curr. Biol. 25, 879-889. https://doi.org/10.1016/j.cub.2015.01.066
- Sala, R., Farrell, K.C., and Stearns, T. (2020). Growth disadvantage associated with centrosome amplification drives population-level centriole number homeostasis. Mol. Biol. Cell 31, 2646-2656. https://doi.org/10.1091/mbc.e19-04-0195
- Schmidt, T.I., Kleylein-Sohn, J., Westendorf, J., Le Clech, M., Lavoie, S.B., Stierhof, Y.D., and Nigg, E.A. (2009). Control of centriole length by CPAP and CP110. Curr. Biol. 19, 1005-1011. https://doi.org/10.1016/j.cub.2009.05.016
- Schnerch, D. and Nigg, E.A. (2016). Structural centrosome aberrations favor proliferation by abrogating microtubule-dependent tissue integrity of breast epithelial mammospheres. Oncogene 35, 2711-2722. https://doi.org/10.1038/onc.2015.332
- Seo, M.Y., Jang, W., and Rhee, K. (2015). Integrity of the pericentriolar material is essential for maintaining centriole association during M phase. PLoS One 10, e0138905. https://doi.org/10.1371/journal.pone.0138905
- Sercin, O., Larsimont, J.C., Karambelas, A.E., Marthiens, V., Moers, V., Boeckx, B., Le Mercier, M., Lambrechts, D., Basto, R., and Blanpain, C. (2016). Transient PLK4 overexpression accelerates tumorigenesis in p53-deficient epidermis. Nat. Cell Biol. 18, 100-110. https://doi.org/10.1038/ncb3270
- Shukla, A., Kong, D., Sharma, M., Magidson, V., and Loncarek, J. (2015). Plk1 relieves centriole block to reduplication by promoting daughter centriole maturation. Nat. Commun. 6, 8077. https://doi.org/10.1038/ncomms9077
- Sullenberger, C., Vasquez-Limeta, A., Kong, D., and Loncarek, J. (2020). With age comes maturity: biochemical and structural transformation of a human centriole in the making. Cells 9, 1429. https://doi.org/10.3390/cells9061429
- Tsou, M.F. and Stearns, T. (2006). Mechanism limiting centrosome duplication to once per cell cycle. Nature 442, 947-951. https://doi.org/10.1038/nature04985
- Tsuchiya, Y., Yoshiba, S., Gupta, A., Watanabe, K., and Kitagawa, D. (2016). Cep295 is a conserved scaffold protein required for generation of a bona fide mother centriole. Nat. Commun. 7, 12567. https://doi.org/10.1038/ncomms12567
- Vitre, B., Holland, A.J., Kulukian, A., Shoshani, O., Hirai, M., Wang, Y., Maldonado, M., Cho, T., Boubaker, J., Swing, D.A., et al. (2015). Chronic centrosome amplification without tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 112, E6321-E6330.
- Wang, W.J., Soni, R.K., Uryu, K., and Tsou, M.F. (2011). The conversion of centrioles to centrosomes: essential coupling of duplication with segregation. J. Cell Biol. 193, 727-739. https://doi.org/10.1083/jcb.201101109
- Watanabe, Y., Honda, S., Konishi, A., Arakawa, S., Murohashi, M., Yamaguchi, H., Torii, S., Tanabe, M., Tanaka, S., Warabi, E., et al. (2016). Autophagy controls centrosome number by degrading Cep63. Nat. Commun. 7, 13508. https://doi.org/10.1038/ncomms13508
- Wong, C. and Stearns, T. (2003). Centrosome number is controlled by a centrosome-intrinsic block to reduplication. Nat. Cell Biol. 5, 539-544. https://doi.org/10.1038/ncb993
- Wu, Q., Yu, X., Liu, L., Sun, S., and Sun, S. (2021). Centrosome-phagy: implications for human diseases. Cell Biosci. 11, 49. https://doi.org/10.1186/s13578-021-00557-w
- Zack, T.I., Schumacher, S.E., Carter, S.L., Cherniack, A.D., Saksena, G., Tabak, B., Lawrence, M.S., Zhsng, C.Z., Wala, J., Mermel, C.H., et al. (2013). Pan-cancer patterns of somatic copy number alteration. Nat. Genet. 45, 1134-1140. https://doi.org/10.1038/ng.2760