Ase1/Prc1-dependent spindle elongation corrects merotely during anaphase in fission yeast

Journal of Cell Biology

Volumn 187, Issue 3, 2009, Pages 399-412

  Courtheoux, Thibault ^a,b   Gay, Guillaume ^a,b   Gachet, Yannick ^a,b   Tournier, Sylvie ^a,b  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ASE1 PROTEIN; PRC1 PROTEIN; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG; ASE1 PROTEIN, S POMBE; MICROTUBULE ASSOCIATED PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ANAPHASE; ARTICLE; CENTROMERE; CHROMOSOME; NONHUMAN; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; SPINDLE CELL; YEAST; BIOLOGICAL MODEL; GENETICS; METABOLISM; MICROTUBULE; MITOSIS SPINDLE; PHYSIOLOGY; SCHIZOSACCHAROMYCES; ULTRASTRUCTURE;

SCHIZOSACCHAROMYCETACEAE;

ANAPHASE; KINETOCHORES; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; MODELS, BIOLOGICAL; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 75549087870     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200902093     Document Type: Article

References (63)

1. Alexandru, G., F. Uhlmann, K. Mechtler, M.A. Poupart, and K. Nasmyth. 2001. Phosphorylation of the cohesin subunit Scc1 by Polo/Cdc5 kinase regulates sister chromatid separation in yeast. Cell. 105:459-472. doi:10.1016/S0092-8674(01)00362-2
2. Andrews, P.D., Y. Ovechkina, N. Morrice, M. Wagenbach, K. Duncan, L. Wordeman, and J.R. Swedlow. 2004. Aurora B regulates MCAK at the mitotic centromere. Dev. Cell. 6:253-268. doi:10.1016/S1534-5807(04)00025-5
3. Arai, R., and I. Mabuchi. 2002. F-actin ring formation and the role of F-actin cables in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 115:887-898.
4. Botvinick, E.L., V. Venugopalan, J.V. Shah, L.H. Liaw, and M.W. Berns. 2004. Controlled ablation of microtubules using a picosecond laser. Biophys. J. 87:4203-4212. doi:10.1529/biophysj.104.049528
5. BrustMascher, I., G. Civelekoglu-Scholey, M. Kwon, A. Mogilner, and J.M. Scholey. 2004. Model for anaphase B: role of three mitotic motors in a switch from poleward flux to spindle elongation. Proc. Natl. Acad. Sci. USA. 101:15938-15943. doi:10.1073/pnas.0407044101
6. Cahill, D.P., C. Lengauer, J. Yu, G.J. Riggins, J.K. Willson, S.D. Markowitz, K.W. Kinzler, and B. Vogelstein. 1998. Mutations of mitotic checkpoint genes in human cancers. Nature. 392:300-303. doi:10.1038/32688
7. Cheeseman, I.M., and A. Desai. 2008. Molecular architecture of the kinetochore-microtubule interface. Nat. Rev. Mol. Cell Biol. 9:33-46. doi:10.1038/nrm2310
8. Choi, S.H., M.P. Peli-Gulli, I. McLeod, A. Sarkeshik, J.R. Yates III, V. Simanis, and D. McCollum. 2009. Phosphorylation state defines discrete roles for monopolin in chromosome attachment and spindle elongation. Curr. Biol. 19:985-995.
9. Cimini, D., B. Howell, P. Maddox, A. Khodjakov, F. Degrassi, and E.D. Salmon. 2001. Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J. Cell Biol. 153:517-527. doi:10.1083/jcb.153.3.517
10. Cimini, D., B. Moree, J.C. Canman, and E.D. Salmon. 2003. Merotelic kinetochore orientation occurs frequently during early mitosis in mammalian tissue cells and error correction is achieved by two different mechanisms. J. Cell Sci. 116:4213-4225. doi:10.1242/jcs.00716
11. Cimini, D., L.A. Cameron, and E.D. Salmon. 2004. Anaphase spindle mechanics prevent missegregation of merotelically oriented chromosomes. Curr. Biol. 14:2149-2155. doi:10.1016/j.cub.2004.11.029
12. Cimini, D., X. Wan, C.B. Hirel, and E.D. Salmon. 2006. Aurora kinase promotes turnover of kinetochore microtubules to reduce chromosome segregation errors. Curr. Biol. 16:1711-1718. doi:10.1016/j.cub.2006.07.022
13. Civelekoglu-Scholey, G., D.J. Sharp, A. Mogilner, and J.M. Scholey. 2006. Model of chromosome motility in Drosophila embryos: adaptation of a general mechanism for rapid mitosis. Biophys. J. 90:3966-3982. doi:10.1529/biophysj.105.078691
14. Cleveland, D.W., Y. Mao, and K.F. Sullivan. 2003. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell. 112:407-421. doi:10.1016/S0092-8674(03)00115-6
15. Courtheoux, T., G. Gay, C. Reyes, S. Goldstone, Y. Gachet, and S. Tournier. 2007. Dynein participates in chromosome segregation in fission yeast. Biol. Cell. 99:627-637. doi:10.1042/BC20070047
16. Ding, R., K.L. McDonald, and J.R. McIntosh. 1993. Threedimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J. Cell Biol. 120:141-151. doi:10.1083/jcb.120.1.141
17. Gachet, Y., S. Tournier, J.B. Millar, and J.S. Hyams. 2004. Mechanism controlling perpendicular alignment of the spindle to the axis of cell division in fission yeast. EMBO J. 23:1289-1300. doi:10.1038/sj.emboj.7600156
18. Gachet, Y., C. Reyes, T. Courthéoux, S. Goldstone, G. Gay, C. Serrurier, and S. Tournier. 2008. Sister kinetochore recapture in fission yeast occurs by two distinct mechanisms, both requiring Dam1 and Klp2. Mol. Biol. Cell. 19:1646-1662. doi:10.1091/mbc.E07-09-0910
19. Ganem, N.J., S.A. Godinho, and D. Pellman. 2009. A mechanism linking extra centrosomes to chromosomal instability. Nature. 460:278-282.
20. Gardner, M.K., and D.J. Odde. 2006. Modeling of chromosome motility during mitosis. Curr. Opin. Cell Biol. 18:639-647. doi:10.1016/j.ceb. 2006.10.006
21. Gardner, M.K., C.G. Pearson, B.L. Sprague, T.R. Zarzar, K. Bloom, E.D. Salmon, and D.J. Odde. 2005. Tension-dependent regulation of microtubule dynamics at kinetochores can explain metaphase congression in yeast. Mol. Biol. Cell. 16:3764-3775. doi:10.1091/mbc.E05-04-0275
22. Gardner, M.K., J. Haase, K. Mythreye, J.N. Molk, M. Anderson, A.P. Joglekar, E.T. O'Toole, M. Winey, E.D. Salmon, D.J. Odde, and K. Bloom. 2008. The microtubule-based motor Kar3 and plus end-binding protein Bim1 provide structural support for the anaphase spindle. J. Cell Biol. 180:91-100. doi:10.1083/jcb.200710164
23. Gregan, J., C.G. Riedel, A.L. Pidoux, Y. Katou, C. Rumpf, A. Schleiffer, S.E. Kearsey, K. Shirahige, R.C. Allshire, and K. Nasmyth. 2007. The kinetochore proteins Pcs1 and Mde4 and heterochromatin are required to prevent merotelic orientation. Curr. Biol. 17:1190-1200. doi:10.1016/j.cub.2007.06.044
24. Griffiths, K., H. Masuda, S. Dhut, and T. Toda. 2008. Fission yeast dam1-A8 mutant is resistant to and rescued by an anti-microtubule agent. Biochem. Biophys. Res. Commun. 368:670-676. doi:10.1016/j.bbrc.2008.01. 156
25. Heald, R., R. Tournebize, T. Blank, R. Sandaltzopoulos, P. Becker, A. Hyman, and E. Karsenti. 1996. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature. 382:420-425. doi:10.1038/382420a0
26. Joglekar, A.P., and A.J. Hunt. 2002. A simple, mechanistic model for directional instability during mitotic chromosome movements. Biophys. J. 83:42-58. doi:10.1016/S0006-3495(02)75148-5
27. Kenney, R.D., and R. Heald. 2006. Essential roles for cohesin in kinetochore and spindle function in Xenopus egg extracts. J. Cell Sci. 119:5057-5066. doi:10.1242/jcs.03277
28. Khodjakov, A., R.W. Cole, B.F. McEwen, K.F. Buttle, and C.L. Rieder. 1997. Chromosome fragments possessing only one kinetochore can congress to the spindle equator. J. Cell Biol. 136:229-240. doi:10.1083/jcb.136.2.229
29. Kolomeisky, A.B., and M.E. Fisher. 2001. Force-velocity relation for growing microtubules. Biophys. J. 80:149-154. doi:10.1016/S0006-3495(01) 76002-X
30. Loïodice, I., J. Staub, T.G. Setty, N.P. Nguyen, A. Paoletti, and P.T. Tran. 2005. Ase1p organizes antiparallel microtubule arrays during interphase and mitosis in fission yeast. Mol. Biol. Cell. 16:1756-1768. doi:10.1091/mbc.E04-10-0899
31. Mallavarapu, A., K. Sawin, and T. Mitchison. 1999. A switch in microtubule dynamics at the onset of anaphase B in the mitotic spindle of Schizosaccharomyces pombe. Curr. Biol. 9:1423-1426. doi:10.1016/S0960- 9822(00)80090-1
32. Maresca, T.J., and E.D. Salmon. 2009. Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity. J. Cell Biol. 184:373-381. doi:10.1083/jcb.200808130
33. Marko, J.F. 2008. Micromechanical studies of mitotic chromosomes. Chromosome Res. 16:469-497. doi:10.1007/s10577-008-1233-7
34. Mayer, M.L., I. Pot, M. Chang, H. Xu, V. Aneliunas, T. Kwok, R. Newitt, R. Aebersold, C. Boone, G.W. Brown, and P. Hieter. 2004. Identification of protein complexes required for efficient sister chromatid cohesion. Mol. Biol. Cell. 15:1736-1745. doi:10.1091/mbc.E03-08-0619
35. McIntosh, J.R., E.L. Grishchuk, M.K. Morphew, A.K. Efremov, K. Zhudenkov, V.A. Volkov, I.M. Cheeseman, A. Desai, D.N. Mastronarde, and F.I. Ataullakhanov. 2008. Fibrils connect microtubule tips with kinetochores: a mechanism to couple tubulin dynamics to chromosome motion. Cell. 135:322-333. doi:10.1016/j.cell.2008.08.038
36. Mogilner, A., R. Wollman, G. Civelekoglu-Scholey,and J. Scholey. 2006. Modeling mitosis. Trends Cell Biol. 16:88-96. doi:10.1016/j.tcb.2005.12. 007
37. Moreno, S., A. Klar, and P. Nurse. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795-823. doi:10.1016/0076-6879(91)94059-L
38. Mulvihill, D.P., C. Barretto, and J.S. Hyams. 2001. Localization of fission yeast type II myosin, Myo2, to the cytokinetic actin ring is regulated by phosphorylation of a C-terminal coiled-coil domain and requires a functional septation initiation network. Mol. Biol. Cell. 12:4044-4053.
39. Nasmyth, K., and A. Schleiffer. 2004. From a single double helix to paired double helices and back. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359:99-108. doi:10.1098/rstb.2003.1417
40. Nicklas, R.B. 1988. The forces that move chromosomes in mitosis. Annu. Rev. Biophys. Biophys. Chem. 17:431-449. doi:10.1146/annurev.bb.17.060188. 002243
41. Norden, C., M. Mendoza, J. Dobbelaere, C.V. Kotwaliwale, S. Biggins, and Y. Barral. 2006. The NoCut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell. 125:85-98. doi:10.1016/j.cell.2006.01.045
42. O'Toole, E.T., M. Winey, and J.R. McIntosh. 1999. High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell. 10:2017-2031.
43. Pellman, D., M. Bagget, Y.H. Tu, G.R. Fink, and H. Tu. 1995. Two microtubule-associated proteins required for anaphase spindle movement in Saccharomyces cerevisiae. J. Cell Biol. 130:1373-1385. doi:10.1083/jcb.130.6.1373
44. Pidoux, A.L., S. Uzawa, P.E. Perry, W.Z. Cande, and R.C. Allshire. 2000. Live analysis of lagging chromosomes during anaphase and their effect on spindle elongation rate in fission yeast. J. Cell Sci. 113:4177-4191.
45. Sakuno, T., K. Tada, and Y. Watanabe. 2009. Kinetochore geometry defined by cohesion within the centromere. Nature. 458:852-858. doi:10.1038/nature07876
46. Samejima, I., T. Matsumoto, Y. Nakaseko, D. Beach, and M. Yanagida. 1993. Identification of seven new cut genes involved in Schizosaccharomyces pombe mitosis. J. Cell Sci. 105:135-143.
47. Tanaka, T.U., N. Rachidi, C. Janke, G. Pereira, M. Galova, E. Schiebel, M.J. Stark, and K. Nasmyth. 2002. Evidence that the Ipl1-Sli15 (Aurorakinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell. 108:317-329. doi:10.1016/S0092-8674(02)00633-5
48. Tanaka, K., E. Kitamura, Y. Kitamura, and T.U. Tanaka. 2007. Molecular mechanisms of microtubule-dependent kinetochore transport toward spindle poles. J. Cell Biol. 178:269-281. doi:10.1083/jcb.200702141
49. Tatebayashi, K., J. Kato, and H. Ikeda. 1998. Isolation of a Schizosaccharomyces pombe rad21ts mutant that is aberrant in chromosome segregation, microtubule function, DNA repair and sensitive to hydroxyurea: possible involvement of Rad21 in ubiquitin-mediated proteolysis. Genetics. 148:49-57.
50. Thompson, S.L., and D.A. Compton. 2008. Examining the link between chromosomal instability and aneuploidy in human cells. J. Cell Biol. 180:665-672. doi:10.1083/jcb.200712029
51. Tighe, A., V.L. Johnson, M. Albertella, and S.S. Taylor. 2001. Aneuploid colon cancer cells have a robust spindle checkpoint. EMBO Rep. 2:609-614. doi:10.1093/embo-reports/kve127
52. Toba, S., T.M. Watanabe, L. Yamaguchi-Okimoto, Y.Y. Toyoshima, and H. Higuchi. 2006. Overlapping hand-over-hand mechanism of single molecular motility of cytoplasmic dynein. Proc. Natl. Acad. Sci. USA. 103:5741-5745. doi:10.1073/pnas.0508511103
53. Tolić Nørrelykke, I.M., L. Sacconi, G. Thon, and F.S. Pavone. 2004. Positioning and elongation of the fission yeast spindle by microtubule-based pushing. Curr. Biol. 14:1181-1186. doi:10.1016/j.cub. 2004.06.029
54. Tomonaga, T., K. Nagao, Y. Kawasaki, K. Furuya, A. Murakami, J. Morishita, T. Yuasa, T. Sutani, S.E. Kearsey, F. Uhlmann, et al. 2000. Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase. Genes Dev. 14:2757-2770. doi:10.1101/gad.832000
55. Tournier, S., Y. Gachet, V. Buck, J.S. Hyams, and J.B. Millar. 2004. Disruption of astral microtubule contact with the cell cortex activates a Bub1, Bub3, and Mad3-dependent checkpoint in fission yeast. Mol. Biol. Cell. 15:3345-3356. doi:10.1091/mbc.E04-03-0256
56. Toyoda, Y., K. Furuya, G. Goshima, K. Nagao, K. Takahashi, and M. Yanagida. 2002. Requirement of chromatid cohesion proteins rad21/scc1 and mis4/scc2 for normal spindle-kinetochore interaction in fission yeast. Curr. Biol. 12:347-358. doi:10.1016/S0960-9822(02)00692-9
57. Uchida, K.S., K. Takagaki, K. Kumada, Y. Hirayama, T. Noda, and T. Hirota. 2009. Kinetochore stretching inactivates the spindle assembly check-point. J. Cell Biol. 184:383-390. doi:10.1083/jcb.200811028
58. Uhlmann, F., F. Lottspeich, and K. Nasmyth. 1999. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature. 400:37-42. doi:10.1038/21831
59. Wise, D.A., and B.R. Brinkley. 1997. Mitosis in cells with unreplicated genomes (MUGs): spindle assembly and behavior of centromere fragments. Cell Motil. Cytoskeleton. 36:291-302. doi:10.1002/(SICI)1097-0169(1997)36: 3〈291::AIDCM9〉3.0.CO;2A
60. Wu, J.Q., J.R. Kuhn, D.R. Kovar, and T.D. Pollard. 2003. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev. Cell. 5:723-734. doi:10.1016/S153- 45807(03)00324-1
61. Yamashita, A., M. Sato, A. Fujita, M. Yamamoto, and T. Toda. 2005. The roles of fission yeast ase1 in mitotic cell division, meiotic nuclear oscillation, and cytokinesis checkpoint signaling. Mol. Biol. Cell. 16:1378-1395. doi:10.1091/mbc.E04-10-0859
62. Yanagida, M. 1998. Fission yeast cut mutations revisited: control of anaphase. Trends Cell Biol. 8:144-149. doi:10.1016/S0962-89-24(98)01236-7
63. Yokobayashi, S., M. Yamamoto, and Y. Watanabe. 2003. Cohesins determine the attachment manner of kinetochores to spindle microtubules at meiosis I in fission yeast. Mol. Cell. Biol. 23:3965-3973.doi:10.1128/MCB.23.11.3965- 3973.2003