P53 protects against genome instability following centriole duplication failure

Journal of Cell Biology

Volumn 210, Issue 1, 2015, Pages 63-77

  Lambrus, Bramwell G ^a   Uetake, Yumi ^b   Clutario, Kevin M ^a   Daggubati, Vikas ^a   Snyder, Michael ^a   Sluder, Greenfield ^b   Holland, Andrew J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUXIN; CENTRIN; GAMMA TUBULIN; HISTONE H2B; PALBOCICLIB; POLO LIKE KINASE 4; PROTEIN P53; TELOMERASE; PLK4 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; TP53 PROTEIN, HUMAN;

ARTICLE; CELL CYCLE ARREST; CELL DIVISION; CELL GROWTH; CELL PROLIFERATION; CENTRIOLE; CENTRIOLE DUPLICATION FAILURE; CHEMICAL GENETICS; CHROMOSOME SEGREGATION; CYTOKINESIS; GENE TARGETING; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; ORGANELLE BIOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; CELL CYCLE CHECKPOINT; CELL LINE; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

CELL CYCLE CHECKPOINTS; CELL LINE; CELL PROLIFERATION; CENTRIOLES; CHROMOSOME SEGREGATION; GENOMIC INSTABILITY; HUMANS; MICROTUBULES; MITOSIS; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84942293631     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201502089     Document Type: Article

References (67)

1. Arquint, C., and E.A. Nigg. 2014. STIL microcephaly mutations interfere with APC/C-mediated degradation and cause centriole amplification. Curr. Biol. 24:351-360. http://dx.doi.org/10.1016/j.cub.2013.12.016
2. Arquint, C., K.F. Sonnen, Y.D. Stierhof, and E.A. Nigg. 2012. Cell-cycleregulated expression of STIL controls centriole number in human cells. J. Cell Sci. 125:1342-1352. http://dx.doi.org/10.1242/jcs.099887
3. Basto, R., J. Lau, T. Vinogradova, A. Gardiol, C.G. Woods, A. Khodjakov, and J.W. Raff. 2006. Flies without centrioles. Cell. 125:1375-1386. http://dx.doi.org/10.1016/j.cell.2006.05.025
4. Bazzi, H., and K.V. Anderson. 2014. Acentriolar mitosis activates a p53-dependent apoptosis pathway in the mouse embryo. Proc. Natl. Acad. Sci. USA. 111:E1491-E1500. http://dx.doi.org/10.1073/pnas.1400568111
5. Berdougo, E., M.E. Terret, and P.V. Jallepalli. 2009. Functional dissection of mitotic regulators through gene targeting in human somatic cells. Methods Mol. Biol. 545:21-37.
6. Bettencourt-Dias, M., A. Rodrigues-Martins, L. Carpenter, M. Riparbelli, L. Lehmann, M.K. Gatt, N. Carmo, F. Balloux, G. Callaini, and D.M. Glover. 2005. SAK/PLK4 is required for centriole duplication and flagella development.Curr. Biol. 15:2199-2207. http://dx.doi.org/10.1016/j.cub.2005.11.042
7. Brownlee, C.W., J.E. Klebba, D.W. Buster, and G.C. Rogers. 2011. The Protein Phosphatase 2A regulatory subunit Twins stabilizes Plk4 to induce centriole amplification. J. Cell Biol. 195:231-243. http://dx.doi.org/10.1083/jcb.201107086
8. Coelho, P.A., L. Bury, B. Sharif, M.G. Riparbelli, J. Fu, G. Callaini, D.M. Glover, and M. Zernicka-Goetz. 2013. Spindle formation in the mouse embryo requires Plk4 in the absence of centrioles. Dev. Cell. 27:586-597. http://dx.doi.org/10.1016/j.devcel.2013.09.029
9. Cunha-Ferreira, I., A. Rodrigues-Martins, I. Bento, M. Riparbelli, W. Zhang, E. Laue, G. Callaini, D.M. Glover, and M. Bettencourt-Dias. 2009. The SCF/Slimb ubiquitin ligase limits centrosome amplification through degradation of SAK/PLK4. Curr. Biol. 19:43-49. http://dx.doi.org/10.1016/j.cub.2008.11.037
10. Cunha-Ferreira, I., I. Bento, A. Pimenta-Marques, S.C. Jana, M. Lince-Faria, P. Duarte, J. Borrego-Pinto, S. Gilberto, T. Amado, D. Brito, et al. 2013. Regulation of autophosphorylation controls PLK4 self-destruction and centriole number. Curr. Biol. 23:2245-2254. http://dx.doi.org/10.1016/j.cub.2013.09.037
11. Debec, A., W. Sullivan, and M. Bettencourt-Dias. 2010. Centrioles: active players or passengers during mitosis? Cell. Mol. Life Sci. 67:2173-2194. http://dx.doi.org/10.1007/s00018-010-0323-9
12. Dzhindzhev, N.S., G. Tzolovsky, Z. Lipinszki, S. Schneider, R. Lattao, J. Fu, J. Debski, M. Dadlez, and D.M. Glover. 2014. Plk4 phosphorylates Ana2 to trigger Sas6 recruitment and procentriole formation. Curr. Biol. 24:2526- 2532. http://dx.doi.org/10.1016/j.cub.2014.08.061
13. Eckerdt, F., T.M. Yamamoto, A.L. Lewellyn, and J.L. Maller. 2011. Identification of a polo-like kinase 4-dependent pathway for de novo centriole formation. Curr. Biol. 21:428-432. http://dx.doi.org/10.1016/j.cub.2011.01.072
14. Fry, D.W., P.J. Harvey, P.R. Keller, W.L. Elliott, M. Meade, E. Trachet, M. Albassam, X. Zheng, W.R. Leopold, N.K. Pryer, and P.L. Toogood. 2004. Specific inhibition of cyclin-dependent kinase 4/6 by PD 0332991 and associated antitumor activity in human tumor xenografts. Mol. Cancer Ther. 3:1427-1438.
15. Ganem, N.J., S.A. Godinho, and D. Pellman. 2009. A mechanism linking extra centrosomes to chromosomal instability. Nature. 460:278-282. http://dx.doi.org/10.1038/nature08136
16. Ganem, N.J., H. Cornils, S.Y. Chiu, K.P. O'Rourke, J. Arnaud, D. Yimlamai, M. Théry, F.D. Camargo, and D. Pellman. 2014. Cytokinesis failure triggers hippo tumor suppressor pathway activation. Cell. 158:833-848. http://dx.doi.org/10.1016/j.cell.2014.06.029
17. Gönczy, P. 2012. Towards a molecular architecture of centriole assembly. Nat. Rev. Mol. Cell Biol. 13:425-435. http://dx.doi.org/10.1038/nrm3373
18. Graser, S., Y.D. Stierhof, S.B. Lavoie, O.S. Gassner, S. Lamla, M. Le Clech, and E.A. Nigg. 2007. Cep164, a novel centriole appendage protein required for primary cilium formation. J. Cell Biol. 179:321-330. http://dx.doi.org/10.1083/jcb.200707181
19. Guderian, G., J. Westendorf, A. Uldschmid, and E.A. Nigg. 2010. Plk4 trans-autophosphorylation regulates centriole number by controlling βTrCP-mediated degradation. J. Cell Sci. 123:2163-2169. http://dx.doi.org/10.1242/jcs.068502
20. Habedanck, R., Y.D. Stierhof, C.J. Wilkinson, and E.A. Nigg. 2005. The Polo kinase Plk4 functions in centriole duplication. Nat. Cell Biol. 7:1140-1146. http://dx.doi.org/10.1038/ncb1320
21. Holland, A.J., and D.W. Cleveland. 2014. Polo-like kinase 4 inhibition: a strategy for cancer therapy? Cancer Cell. 26:151-153. http://dx.doi.org/10.1016/j.ccr.2014.07.017
22. Holland, A.J., W. Lan, S. Niessen, H. Hoover, and D.W. Cleveland. 2010. Pololike kinase 4 kinase activity limits centrosome overduplication by autoregulating its own stability. J. Cell Biol. 188:191-198. http://dx.doi.org/10.1083/jcb.200911102
23. Holland, A.J., D. Fachinetti, S. Da Cruz, Q. Zhu, B. Vitre, M. Lince-Faria, D. Chen, N. Parish, I.M. Verma, M. Bettencourt-Dias, and D.W. Cleveland. 2012a. Polo-like kinase 4 controls centriole duplication but does not directly regulate cytokinesis. Mol. Biol. Cell. 23:1838-1845. http://dx.doi.org/10.1091/mbc.E11-12-1043
24. Holland, A.J., D. Fachinetti, Q. Zhu, M. Bauer, I.M. Verma, E.A. Nigg, and D.W. Cleveland. 2012b. The autoregulated instability of Polo-like kinase 4 limits centrosome duplication to once per cell cycle. Genes Dev. 26:2684- 2689. http://dx.doi.org/10.1101/gad.207027.112
25. Hussein, D., and S.S. Taylor. 2002. Farnesylation of Cenp-F is required for G2/M progression and degradation after mitosis. J. Cell Sci. 115:3403-3414.
26. Insolera, R., H. Bazzi, W. Shao, K.V. Anderson, and S.H. Shi. 2014. Cortical neurogenesis in the absence of centrioles. Nat. Neurosci. 17:1528-1535. http://dx.doi.org/10.1038/nn.3831
27. Izquierdo, D., W.J. Wang, K. Uryu, and M.F. Tsou. 2014. Stabilization of cartwheel-less centrioles for duplication requires CEP295-mediated centriole-to-centrosome conversion. Cell Reports. 8:957-965. http://dx.doi.org/10.1016/j.celrep.2014.07.022
28. Khodjakov, A., and C.L. Rieder. 2001. Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. J. Cell Biol. 153:237-242. http://dx.doi.org/10.1083/jcb.153.1.237
29. Khodjakov, A., C.L. Rieder, G. Sluder, G. Cassels, O. Sibon, and C.L. Wang. 2002. De novo formation of centrosomes in vertebrate cells arrested during S phase. J. Cell Biol. 158:1171-1181. http://dx.doi.org/10.1083/jcb.200205102
30. Kitagawa, D., I. Vakonakis, N. Olieric, M. Hilbert, D. Keller, V. Olieric, M. Bortfeld, M.C. Erat, I. Flückiger, P. Gönczy, and M.O. Steinmetz. 2011. Structural basis of the 9-fold symmetry of centrioles. Cell. 144:364-375. http://dx.doi.org/10.1016/j.cell.2011.01.008
31. Klebba, J.E., D.W. Buster, A.L. Nguyen, S. Swatkoski, M. Gucek, N.M. Rusan, and G.C. Rogers. 2013. Polo-like kinase 4 autodestructs by generating its Slimb-binding phosphodegron. Curr. Biol. 23:2255-2261. http://dx.doi. org/10.1016/j.cub.2013.09.019
32. Ko, M.A., C.O. Rosario, J.W. Hudson, S. Kulkarni, A. Pollett, J.W. Dennis, and C.J. Swallow. 2005. Plk4 haploinsufficiency causes mitotic infidelity and carcinogenesis. Nat. Genet. 37:883-888. http://dx.doi.org/10.1038/ ng1605
33. La Terra, S., C.N. English, P. Hergert, B.F. McEwen, G. Sluder, and A. Khodjakov. 2005. The de novo centriole assembly pathway in HeLa cells: cell cycle progression and centriole assembly/maturation. J. Cell Biol. 168:713-722.http://dx.doi.org/10.1083/jcb.200411126
34. Lecland, N., A. Debec, A. Delmas, S. Moutinho-Pereira, N. Malmanche, A. Bouissou, C. Dupré, A. Jourdan, B. Raynaud-Messina, H. Maiato, and A. Guichet. 2013. Establishment and mitotic characterization of new Drosophila acentriolar cell lines from DSas-4 mutant. Biol. Open. 2:314- 323. http://dx.doi.org/10.1242/bio.20133327
35. Liu, L., C.Z. Zhang, M. Cai, J. Fu, G.G. Chen, and J. Yun. 2012. Downregulation of polo-like kinase 4 in hepatocellular carcinoma associates with poor prognosis. PLoS ONE. 7:e41293. http://dx.doi.org/10.1371/journal. pone.0041293
36. Marshall, W.F., Y. Vucica, and J.L. Rosenbaum. 2001. Kinetics and regulation of de novo centriole assembly. Implications for the mechanism of centriole duplication. Curr. Biol. 11:308-317. http://dx.doi.org/10.1016/S0960-9822(01)00094-X
37. Mason, J.M., D.C. Lin, X. Wei, Y. Che, Y. Yao, R. Kiarash, D.W. Cescon, G.C. Fletcher, D.E. Awrey, M.R. Bray, et al. 2014. Functional characterization of CFI-400945, a Polo-like kinase 4 inhibitor, as a potential anticancer agent. Cancer Cell. 26:163-176. http://dx.doi.org/10.1016/j. ccr.2014.05.006
38. Miki-Noumura, T. 1977. Studies on the de novo formation of centrioles: aster formation in the activated eggs of sea urchin. J. Cell Sci. 24:203-216.
39. Nigg, E.A., and J.W. Raff. 2009. Centrioles, centrosomes, and cilia in health and disease. Cell. 139:663-678. http://dx.doi.org/10.1016/j.cell.2009.10.036
40. Nishimura, K., T. Fukagawa, H. Takisawa, T. Kakimoto, and M. Kanemaki. 2009. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat. Methods. 6:917-922. http://dx.doi.org/10.1038/nmeth.1401
41. Ohta, M., T. Ashikawa, Y. Nozaki, H. Kozuka-Hata, H. Goto, M. Inagaki, M. Oyama, and D. Kitagawa. 2014. Direct interaction of Plk4 with STIL ensures formation of a single procentriole per parental centriole. Nat. Commun. 5:5267. http://dx.doi.org/10.1038/ncomms6267
42. Palazzo, R.E., E. Vaisberg, R.W. Cole, and C.L. Rieder. 1992. Centriole duplication in lysates of Spisula solidissima oocytes. Science. 256:219-221. http://dx.doi.org/10.1126/science.1566068
43. Peel, N., N.R. Stevens, R. Basto, and J.W. Raff. 2007. Overexpressing centriole- replication proteins in vivo induces centriole overduplication and de novo formation. Curr. Biol. 17:834-843. http://dx.doi.org/10.1016/j.cub.2007.04.036
44. Pellegrino, R., D.F. Calvisi, S. Ladu, V. Ehemann, T. Staniscia, M. Evert, F. Dombrowski, P. Schirmacher, and T. Longerich. 2010. Oncogenic and tumor suppressive roles of polo-like kinases in human hepatocellular carcinoma. Hepatology. 51:857-868.
45. Rodrigues-Martins, A., M. Riparbelli, G. Callaini, D.M. Glover, and M. Bettencourt-Dias. 2007. Revisiting the role of the mother centriole in centriole biogenesis. Science. 316:1046-1050. http://dx.doi.org/10.1126/science.1142950
46. Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J. Cell Biol. 184:225-239. http://dx.doi.org/10.1083/jcb.200808049
47. Silkworth, W.T., I.K. Nardi, L.M. Scholl, and D. Cimini. 2009. Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation in cancer cells. PLoS ONE. 4:e6564. http://dx.doi.org/10.1371/journal.pone.0006564
48. Sir, J.H., A.R. Barr, A.K. Nicholas, O.P. Carvalho, M. Khurshid, A. Sossick, S. Reichelt, C. D'Santos, C.G. Woods, and F. Gergely. 2011. A primary microcephaly protein complex forms a ring around parental centrioles. Nat. Genet. 43:1147-1153. http://dx.doi.org/10.1038/ng.971
49. Sir, J.H., M. Pütz, O. Daly, C.G. Morrison, M. Dunning, J.V. Kilmartin, and F. Gergely. 2013. Loss of centrioles causes chromosomal instability in vertebrate somatic cells. J. Cell Biol. 203:747-756. http://dx.doi. org/10.1083/jcb.201309038
50. Strnad, P., S. Leidel, T. Vinogradova, U. Euteneuer, A. Khodjakov, and P. Gönczy. 2007. Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Dev. Cell. 13:203-213. http://dx.doi.org/10.1016/j.devcel.2007.07.004
51. Suh, M.R., J.W. Han, Y.R. No, and J. Lee. 2002. Transient concentration of a γ-tubulin-related protein with a pericentrin-related protein in the formation of basal bodies and flagella during the differentiation of Naegleria gruberi. Cell Motil. Cytoskeleton. 52:66-81. http://dx.doi.org/10.1002/cm.10033
52. Szollosi, D., P. Calarco, and R.P. Donahue. 1972. Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J. Cell Sci. 11:521-541.
53. Szöllosi, D., and J.P. Ozil. 1991. De novo formation of centrioles in parthenogenetically activated, diploidized rabbit embryos. Biol. Cell. 72:61-66. http://dx.doi.org/10.1016/0248-4900(91)90079-3
54. Tang, C.J., R.H. Fu, K.S. Wu, W.B. Hsu, and T.K. Tang. 2009. CPAP is a cell-cycle regulated protein that controls centriole length. Nat. Cell Biol. 11:825-831. http://dx.doi.org/10.1038/ncb1889
55. Tang, C.J.C., S.Y. Lin, W.B. Hsu, Y.N. Lin, C.T. Wu, Y.C. Lin, C.W. Chang, K.S. Wu, and T.K. Tang. 2011. The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation. EMBO J. 30:4790-4804. http://dx.doi.org/10.1038/emboj.2011.378
56. Thompson, S.L., and D.A. Compton. 2010. Proliferation of aneuploid human cells is limited by a p53-dependent mechanism. J. Cell Biol. 188:369-381. http://dx.doi.org/10.1083/jcb.200905057
57. Tiscornia, G., O. Singer, M. Ikawa, and I.M. Verma. 2003. A general method for gene knockdown in mice by using lentiviral vectors expressing small interfering RNA. Proc. Natl. Acad. Sci. USA. 100:1844-1848. http://dx.doi.org/10.1073/pnas.0437912100
58. Tsou, M.F., and T. Stearns. 2006. Controlling centrosome number: licenses and blocks. Curr. Opin. Cell Biol. 18:74-78. http://dx.doi.org/10.1016/j.ceb.2005.12.008
59. Uetake, Y., and G. Sluder. 2010. Prolonged prometaphase blocks daughter cell proliferation despite normal completion of mitosis. Curr. Biol. 20:1666-1671. http://dx.doi.org/10.1016/j.cub.2010.08.018
60. Uetake, Y., and G. Sluder. 2012. Biomedical optical phase microscopy and nanoscopy. In Practical Methodology for Long-Term Recordings of Live Human Cells. Academic Press, Waltham, MA. 43-52.
61. Uetake, Y., J. Loncarek, J.J. Nordberg, C.N. English, S. La Terra, A. Khodjakov, and G. Sluder. 2007. Cell cycle progression and de novo centriole assembly after centrosomal removal in untransformed human cells. J. Cell Biol. 176:173-182. http://dx.doi.org/10.1083/jcb.200607073
62. van Breugel, M., M. Hirono, A. Andreeva, H.A. Yanagisawa, S. Yamaguchi, Y. Nakazawa, N. Morgner, M. Petrovich, I.O. Ebong, C.V. Robinson, et al. 2011. Structures of SAS-6 suggest its organization in centrioles. Science. 331:1196-1199. http://dx.doi.org/10.1126/science.1199325
63. van Breugel, M., R. Wilcken, S.H. McLaughlin, T.J. Rutherford, and C.M. Johnson. 2014. Structure of the SAS-6 cartwheel hub from Leishmania major. eLife. 3:e01812. http://dx.doi.org/10.7554/eLife.01812
64. Wang, W.J., R.K. Soni, K. Uryu, and M.F. Tsou. 2011. The conversion of centrioles to centrosomes: essential coupling of duplication with segregation. J. Cell Biol. 193:727-739. http://dx.doi.org/10.1083/jcb.201101109
65. Watson, P.A., H.H. Hanauske-Abel, A. Flint, and M. Lalande. 1991. Mimosine reversibly arrests cell cycle progression at the G1-S phase border. Cytometry. 12:242-246. http://dx.doi.org/10.1002/cyto.990120306
66. Wong, Y.L., J.V. Anzola, R.L. Davis, M. Yoon, A. Motamedi, A. Kroll, C.P. Seo, J.E. Hsia, S.K. Kim, J.W. Mitchell, et al. 2015. Reversible centriole depletion with an inhibitor of Polo-like kinase 4. Science. 348:1155-1160. http://dx.doi.org/10.1126/science.aaa5111
67. Yu, J., Y. Zheng, J. Dong, S. Klusza, W.M. Deng, and D. Pan. 2010. Kibra functions as a tumor suppressor protein that regulates Hippo signaling in conjunction with Merlin and Expanded. Dev. Cell. 18:288-299. http://dx.doi.org/10.1016/j.devcel.2009.12.012