Insufficiency of BUBR1, a mitotic spindle checkpoint regulator, causes impaired ciliogenesis in vertebrates

Human Molecular Genetics

Volumn 20, Issue 10, 2011, Pages 2058-2070

  Miyamoto, Tatsuo ^a   Porazinski, Sean ^b   Wang, Huijia ^b   Borovina, Antonia ^c,d   Ciruna, Brian ^c,d   Shimizu, Atsushi ^e   Kajii, Tadashi ^f   Kikuchi, Akira ^g   Furutani Seiki, Makoto ^b   Matsuura, Shinya ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b University of Bath   (United Kingdom)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f Osaka University ^*

^g OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BUB1 RELATED PROTEIN; CELL CYCLE PROTEIN 20;

ANAPHASE; ANEUPLOIDY; ARTICLE; BRAIN DEVELOPMENT; CELL CYCLE G0 PHASE; CELL DIVISION; CELL MATURATION; CEREBELLUM; CHILDHOOD CANCER; CILIOGENESIS; CONTROLLED STUDY; DANDY WALKER SYNDROME; EMBRYO; EUKARYOTIC FLAGELLUM; HUMAN; HUMAN CELL; KIDNEY POLYCYSTIC DISEASE; MITOSIS SPINDLE; MORPHOGENESIS; MOSAIC VARIEGATED ANEUPLOIDY; NONHUMAN; ORYZIAS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; VERTEBRATE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL CYCLE PROTEINS; CELL LINE; CEREBELLUM; CHROMOSOME DISORDERS; CILIA; CYTOPLASMIC STRUCTURES; DOGS; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; MODELS, BIOLOGICAL; MOSAICISM; ORYZIAS; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASE COMPLEXES; VERTEBRATES; WNT PROTEINS;

ORYZIINAE; VERTEBRATA;

EID: 79955393977     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr090     Document Type: Article

References (34)

1. Baker, D.J., Chen, J. and van Deursen, J.M.A. (2005) The mitotic checkpoint in cancer and aging: what have mice taught us? Curr. Opin. Cell Biol., 17, 583-589.
2. Sullivan, M. and Morgan, D.O. (2007) Finishing mitosis, one step at a time. Nat. Rev. Mol. Cell Biol., 8, 894-903.
3. Choi, E., Choe, H., Min, J., Choi, J.Y., Kim, J. and Lee, H. (2009) BubR1 acetylation at prometaphase is required for modulating APC/C activity and timing of mitosis. EMBO J., 28, 2077-2089.
4. Kulukian, A., Han, J.S. and Cleveland, D.W. (2009) Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding. Dev. Cell, 16, 105-117.
5. Malureanu, L.A., Jeganathan, K.B., Hamada, M., Wasilewski, L., Davenport, J. and van Deursen, J.M. (2009) BubR1 N terminus acts as a soluble inhibitor of cyclin B degradation by APC/C(Cdc20) in interphase. Dev. Cell, 16, 118-131.
6. Peters, J.M. (2006) The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol., 7, 644-656.
7. Hanks, S., Coleman, K., Reid, S., Plaja, A., Firth, H., Fitzpatrick, D., Kidd, A., Méhes, K., Nash, R., Robin, N. et al. (2004) Constitutional aneuploidy and cancer predisposition caused by biallelic mutations in BUB1B. Nat. Genet., 36, 1159-1161.
8. Matsuura, S., Matsumoto, Y., Morishima, K.-I., Izumi, H., Matsumoto, H., Ito, E., Tsutsui, K., Kobayashi, J., Tauchi, H., Kajiwara, Y. et al. (2006) Monoallelic BUB1B mutations and defective mitotic-spindle checkpoint in seven families with premature chromatid separation (PCS) syndrome. Am. J. Med. Genet. A, 140, 358-367.
9. Ganner, A., Lienkamp, S., Schäfer, T., Romaker, D., Wegierski, T., Park, T.J., Spreitzer, S., Simons, M., Gloy, J., Kim, E. et al. (2009) Regulation of ciliary polarity by the APC/C. Proc. Natl Acad. Sci. USA, 106, 17799-17804.
10. Gerdes, J.M., Davis, E.E. and Katsanis, N. (2009) The vertebrate primary cilium in development, homeostasis, and disease. Cell, 137, 32-45.
11. Goetz, S.C. and Anderson, K.V. (2010) The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet., 11, 331-344.
12. Nigg, E.A. and Raff, J.W. (2009) Centrioles, centrosomes, and cilia in health and disease. Cell, 139, 663-678.
13. Matsuura, S., Ito, E., Tauchi, H., Komatsu, K., Ikeuchi, T. and Kajii, T. (2000) Chromosomal instability syndrome of total premature chromatid separation with mosaic variegated aneuploidy is defective in mitotic-spindle checkpoint. Am. J. Hum. Genet., 67, 483-486.
14. Izumi, H., Matsumoto, Y., Ikeuchi, T., Saya, H., Kajii, T. and Matsuura, S. (2009) BubR1 localizes to centrosomes and suppresses centrosome amplification via regulating Plk1 activity in interphase cells. Oncogene, 28, 2806-2820.
15. Simons, M., Gloy, J., Ganner, A., Bullerkotte, A., Bashkurov, M., Krönig, C., Schermer, B., Benzing, T., Cabello, O.A., Jenny, A. et al. (2005) Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet., 37, 537-543.
16. Park, T.J., Mitchell, B.J., Abitua, P.B., Kintner, C. and Wallingford, J.B. (2008) Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat. Genet., 40, 871-879.
17. Listovsky, T., Oren, Y.S., Yudkovsky, Y., Mahbubani, H.M., Weiss, A.M., Lebendiker, M. and Brandeis, M. (2004) Mammalian Cdh1/Fzr mediates its own degradation. EMBO J., 23, 1619-1626.
18. Nilsson, J., Yekezare, M., Minshull, J. and Pines, J. (2008) The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat. Cell Biol., 10, 1411-1420.
19. Furutani-Seiki, M. and Wittbrodt, J. (2004) Medaka and zebrafish, an evolutionary twin study. Mech. Dev., 121, 629-637.
20. Yu, H. (2007) Cdc20: a WD40 activator for a cell cycle degradation machine. Mol. Cell, 27, 3-16.
21. Shirayama, M., Toth, A., Galova, M. and Nasmyth, K. (1999) APC(Cdc20) promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5. Nature, 402, 203-207.
22. Wirth, K.G., Ricci, R., Gimenez-Abian, J.F., Taghybeeglu, S., Kudo, N.R., Jochum, W., Vasseur-Cognet, M. and Nasmyth, K. (2004) Loss of the anaphase-promoting complex in quiescent cells causes unscheduled hepatocyte proliferation. Genes Dev., 18, 88-98.
23. Konishi, Y., Stegmuller, J., Matsuda, T., Bonni, S. and Bonni, A. (2004) Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science, 303, 1026-1030.
24. Jaspersen, S.L., Charles, J.F. and Morgan, D.O. (1999) Inhibitory phosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr. Biol., 9, 227-236.
25. Clement, A., Solnica-Krezel, L. and Gould, K.L. (2011) The Cdc14B phosphatase contributes to ciliogenesis in zebrafish. Development, 138, 291-302.
26. Wasch, R., Robbins, J.A. and Cross, F.R. (2010) The emerging role of APC/CCdh1 in controlling differentiation, genomic stability and tumor suppression. Oncogene, 29, 1-10.
27. Tucker, R.W., Pardee, A.B. and Fujiwara, K. (1979) Centriole ciliation is related to quiescence and DNA synthesis in 3T3 cells. Cell, 17, 527-535.
28. Rieder, C.L., Jensen, C.G. and Jensen, L.C. (1979) The resorption of primary cilia during mitosis in a vertebrate (PtK1) cell line. J. Ultrastruct. Res., 68, 173-185.
29. Qin, H., Wang, Z., Diener, D. and Rosenbaum, J. (2007) Intraflagellar transport protein 27 is a small G protein involved in cell-cycle control. Curr. Biol., 17, 193-202.
30. Spektor, A., Tsang, W.Y., Khoo, D. and Dynlacht, B.D. (2007) Cep97 and CP110 suppress a cilia assembly program. Cell, 130, 678-690.
31. Aboualaiwi, W.A., Ratnam, S., Booth, R.L., Shah, J.V. and Nauli, S.M. (2011) Endothelial cells from humans and mice with polycystic kidney disease are characterized by polyploidy and chromosome segregation defects through survivin down-regulation. Hum. Mol. Genet., 20, 354-367.
32. Kishida, S., Hamao, K., Inoue, M., Hasegawa, M., Matsuura, Y., Mikoshiba, K., Fukuda, M. and Kikuchi, A. (2007) Dvl regulates endoand exocytotic processes through binding to synaptotagmin. Genes Cells, 12, 49-61.
33. Porazinski, SR, Wang, H. and Furutani-Seiki, M. (2011) Essential techniques for introducing medaka to a zebrafish laboratory-toward combined use of medaka and zebrafish for further genetic dissection of the function of the vertebrate genome. 'Vertebrate embryogenesis, Methods and Protocols' in the series Methods in Molecular Biology. Humana Press (in press).
34. Borovina, A., Superina, S., Voskas, D. and Ciruna, B. (2010) Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. Nat. Cell Biol., 12, 407-412.