Condensin and the spindle midzone prevent cytokinesis failure induced by chromatin bridges in C. elegans embryos

Current Biology

Volumn 23, Issue 11, 2013, Pages 937-946

  Bembenek, Joshua N ^b,c   Verbrugghe, Koen J C ^a   Khanikar, Jayshree ^a   Csankovszki, Györgyi ^b   Chan, Raymond C ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS; MAMMALIA;

ADENOSINE TRIPHOSPHATASE; AIR-2 PROTEIN, C ELEGANS; AURORA B KINASE; CAENORHABDITIS ELEGANS PROTEIN; CHROMATIN; CONDENSIN; DNA BINDING PROTEIN; MULTIPROTEIN COMPLEX;

ANIMAL; ANIMAL EMBRYO; CAENORHABDITIS ELEGANS; CHROMATIN; CYTOKINESIS; CYTOLOGY; EMBRYOLOGY; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; OOCYTE CLEAVAGE; SPINDLE APPARATUS; TIME;

ADENOSINE TRIPHOSPHATASES; ANIMALS; AURORA KINASE B; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMATIN; CLEAVAGE STAGE, OVUM; CYTOKINESIS; DNA-BINDING PROTEINS; EMBRYO, NONMAMMALIAN; MICROSCOPY, FLUORESCENCE; MULTIPROTEIN COMPLEXES; SPINDLE APPARATUS; TIME FACTORS;

EID: 84878524196     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2013.04.028     Document Type: Article

References (49)

1. P. Steigemann, C. Wurzenberger, M.H. Schmitz, M. Held, J. Guizetti, S. Maar, and D.W. Gerlich Aurora B-mediated abscission checkpoint protects against tetraploidization Cell 136 2009 473 484
2. J.G. Carlton, A. Caballe, M. Agromayor, M. Kloc, and J. Martin-Serrano ESCRT-III governs the Aurora B-mediated abscission checkpoint through CHMP4C Science 336 2012 220 225
3. C. Norden, M. Mendoza, J. Dobbelaere, C.V. Kotwaliwale, S. Biggins, and Y. Barral The NoCut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage Cell 125 2006 85 98
4. M. Carmena, S. Ruchaud, and W.C. Earnshaw Making the Auroras glow: regulation of Aurora A and B kinase function by interacting proteins Curr. Opin. Cell Biol. 21 2009 796 805
5. S. Ruchaud, M. Carmena, and W.C. Earnshaw Chromosomal passengers: conducting cell division Nat. Rev. Mol. Cell Biol. 8 2007 798 812
6. M. Mendoza, C. Norden, K. Durrer, H. Rauter, F. Uhlmann, and Y. Barral A mechanism for chromosome segregation sensing by the NoCut checkpoint Nat. Cell Biol. 11 2009 477 483
7. L. Capalbo, E. Montembault, T. Takeda, Z.I. Bassi, D.M. Glover, and P.P. D'Avino The chromosomal passenger complex controls the function of endosomal sorting complex required for transport-III Snf7 proteins during cytokinesis Open Biol 2 2012 120070
8. T. Hirano Condensins: universal organizers of chromosomes with diverse functions Genes Dev. 26 2012 1659 1678
9. C. D'Ambrosio, G. Kelly, K. Shirahige, and F. Uhlmann Condensin-dependent rDNA decatenation introduces a temporal pattern to chromosome segregation Curr. Biol. 18 2008 1084 1089
10. D. D'Amours, F. Stegmeier, and A. Amon Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA Cell 117 2004 455 469
11. B.D. Lavoie, E. Hogan, and D. Koshland In vivo requirements for rDNA chromosome condensation reveal two cell-cycle-regulated pathways for mitotic chromosome folding Genes Dev. 18 2004 76 87
12. N. Nakazawa, R. Mehrotra, M. Ebe, and M. Yanagida Condensin phosphorylated by the Aurora-B-like kinase Ark1 is continuously required until telophase in a mode distinct from Top2 J. Cell Sci. 124 2011 1795 1807
13. K.S. Collette, E.L. Petty, N. Golenberg, J.N. Bembenek, and G. Csankovszki Different roles for Aurora B in condensin targeting during mitosis and meiosis J. Cell Sci. 124 2011 3684 3694
14. D. Gerlich, T. Hirota, B. Koch, J.M. Peters, and J. Ellenberg Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells Curr. Biol. 16 2006 333 344
15. F. Mora-Bermúdez, D. Gerlich, and J. Ellenberg Maximal chromosome compaction occurs by axial shortening in anaphase and depends on Aurora kinase Nat. Cell Biol. 9 2007 822 831
16. M. Brauchle, K. Baumer, and P. Gönczy Differential activation of the DNA replication checkpoint contributes to asynchrony of cell division in C. elegans embryos Curr. Biol. 13 2003 819 827
17. C.W. Conn, A.L. Lewellyn, and J.L. Maller The DNA damage checkpoint in embryonic cell cycles is dependent on the DNA-to-cytoplasmic ratio Dev. Cell 7 2004 275 281
18. M. Dasso, and J.W. Newport Completion of DNA replication is monitored by a feedback system that controls the initiation of mitosis in vitro: studies in Xenopus Cell 61 1990 811 823
19. S.E. Encalada, J. Willis, R. Lyczak, and B. Bowerman A spindle checkpoint functions during mitosis in the early Caenorhabditis elegans embryo Mol. Biol. Cell 16 2005 1056 1070
20. O.C. Sibon, V.A. Stevenson, and W.E. Theurkauf DNA-replication checkpoint control at the Drosophila midblastula transition Nature 388 1997 93 97
21. Y. Wei, S. Multi, C.R. Yang, J. Ma, Q.H. Zhang, Z.B. Wang, M. Li, L. Wei, Z.J. Ge, and C.H. Zhang Spindle assembly checkpoint regulates mitotic cell cycle progression during preimplantation embryo development PLoS ONE 6 2011 e21557
22. P.H. O'Farrell, J. Stumpff, and T.T. Su Embryonic cleavage cycles: how is a mouse like a fly? Curr. Biol. 14 2004 R35 R45
23. B. Sönnichsen, L.B. Koski, A. Walsh, P. Marschall, B. Neumann, M. Brehm, A.M. Alleaume, J. Artelt, P. Bettencourt, and E. Cassin Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans Nature 434 2005 462 469
24. J.N. Bembenek, J.G. White, and Y. Zheng A role for separase in the regulation of RAB-11-positive vesicles at the cleavage furrow and midbody Curr. Biol. 20 2010 259 264
25. T.R. Heallen, H.P. Adams, T. Furuta, K.J. Verbrugghe, and J.M. Schumacher An Afg2/Spaf-related Cdc48-like AAA ATPase regulates the stability and activity of the C. elegans Aurora B kinase AIR-2 Dev. Cell 15 2008 603 616
26. L. Lewellyn, A. Carvalho, A. Desai, A.S. Maddox, and K. Oegema The chromosomal passenger complex and centralspindlin independently contribute to contractile ring assembly J. Cell Biol. 193 2011 155 169
27. K.A. Hagstrom, V.F. Holmes, N.R. Cozzarelli, and B.J. Meyer C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis Genes Dev. 16 2002 729 742
28. S. Kaitna, P. Pasierbek, M. Jantsch, J. Loidl, and M. Glotzer The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous Chromosomes during meiosis Curr. Biol. 12 2002 798 812
29. J.M. Schumacher, A. Golden, and P.J. Donovan AIR-2: An Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos J. Cell Biol. 143 1998 1635 1646
30. K.J. Verbrugghe, and J.G. White SPD-1 is required for the formation of the spindle midzone but is not essential for the completion of cytokinesis in C. elegans embryos Curr. Biol. 14 2004 1755 1760
31. A.F. Severson, D.R. Hamill, J.C. Carter, J. Schumacher, and B. Bowerman The aurora-related kinase AIR-2 recruits ZEN-4/CeMKLP1 to the mitotic spindle at metaphase and is required for cytokinesis Curr. Biol. 10 2000 1162 1171
32. M. Diogon, F. Wissler, S. Quintin, Y. Nagamatsu, S. Sookhareea, F. Landmann, H. Hutter, N. Vitale, and M. Labouesse The RhoGAP RGA-2 and LET-502/ROCK achieve a balance of actomyosin-dependent forces in C. elegans epidermis to control morphogenesis Development 134 2007 2469 2479
33. T.Q. Nguyen, H. Sawa, H. Okano, and J.G. White The C. elegans septin genes, unc-59 and unc-61, are required for normal postembryonic cytokineses and morphogenesis but have no essential function in embryogenesis J. Cell Sci. 113 2000 3825 3837
34. A.J. Piekny, and P.E. Mains Rho-binding kinase (LET-502) and myosin phosphatase (MEL-11) regulate cytokinesis in the early Caenorhabditis elegans embryo J. Cell Sci. 115 2002 2271 2282
35. A.S. Maddox, L. Lewellyn, A. Desai, and K. Oegema Anillin and the septins promote asymmetric ingression of the cytokinetic furrow Dev. Cell 12 2007 827 835
36. J.D. Lieb, E.E. Capowski, P. Meneely, and B.J. Meyer DPY-26, a link between dosage compensation and meiotic chromosome segregation in the nematode Science 274 1996 1732 1736
37. J.H. Stear, and M.B. Roth Characterization of HCP-6, a C. elegans protein required to prevent chromosome twisting and merotelic attachment Genes Dev. 16 2002 1498 1508
38. C.J. Tsai, D.G. Mets, M.R. Albrecht, P. Nix, A. Chan, and B.J. Meyer Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit Genes Dev. 22 2008 194 211
39. G. Csankovszki, K. Collette, K. Spahl, J. Carey, M. Snyder, E. Petty, U. Patel, T. Tabuchi, H. Liu, and I. McLeod Three distinct condensin complexes control C. elegans chromosome dynamics Curr. Biol. 19 2009 9 19
40. P.T. Chuang, D.G. Albertson, and B.J. Meyer DPY-27:a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome Cell 79 1994 459 474
41. L.C. Green, P. Kalitsis, T.M. Chang, M. Cipetic, J.H. Kim, O. Marshall, L. Turnbull, C.B. Whitchurch, P. Vagnarelli, and K. Samejima Contrasting roles of condensin I and condensin II in mitotic chromosome formation J. Cell Sci. 125 2012 1591 1604
42. A.M. Ladouceur, R. Ranjan, and P.S. Maddox Cell size: chromosomes get slapped by a midzone ruler Curr. Biol. 21 2011 R388 R390
43. E.K. Kieserman, and R. Heald Mitotic chromosome size scaling in Xenopus Cell Cycle 10 2011 3863 3870
44. G. Neurohr, A. Naegeli, I. Titos, D. Theler, B. Greber, J. Díez, T. Gabaldón, M. Mendoza, and Y. Barral A midzone-based ruler adjusts chromosome compaction to anaphase spindle length Science 332 2011 465 468
45. S. Brenner The genetics of Caenorhabditis elegans Genetics 77 1974 71 94
46. Ahringer, J. (2006). Reverse genetics. In WormBook, The C. elegans Research Community, ed. WormBook, doi/10.1895/wormbook.1.47.1, http://www.wormbook.org.
47. K.J. Verbrugghe, and R.C. Chan Imaging C. elegans embryos using an epifluorescent microscope and open source software J. Vis. Exp. 49 2011 e2625
48. R.C. Chan, A.F. Severson, and B.J. Meyer Condensin restructures chromosomes in preparation for meiotic divisions J. Cell Biol. 167 2004 613 625
49. Shaham (ed.), S. Methods in cell biology. In WormBook, The C. elegans Research Community, ed. WormBook, doi/10.1895/wormbook.1.49.1, http://www.wormbook.org.