Nonautonomous Movement of Chromosomes in Mitosis

Developmental Cell

Volumn 27, Issue 1, 2013, Pages 60-71

  Vladimirou, Elina ^a   Mchedlishvili, Nunu ^c,e   Gasic, Ivana ^c,d   Armond, JonathanW ^b   Samora, CatarinaP ^a,f   Meraldi, Patrick ^c,d   McAinsh, AndrewD ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c ETH ZURICH   (Switzerland)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f CRUK London Research Institute   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN; KINESIN 12; KINESIN 5; PROTEIN; PROTEIN KIF15; PROTEIN MAD1; UNCLASSIFIED DRUG; KIF11 PROTEIN, HUMAN; KIF15 PROTEIN, HUMAN;

ARTICLE; CENTROMERE; CHROMOSOME ARM; CHROMOSOME MOVEMENT; CHROMOSOMES AND CHROMOSOMAL PHENOMENA; COMPUTER SIMULATION; CONTROLLED STUDY; CROSS LINKING; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN CHROMOSOME; METAPHASE; MITOSIS; MITOSIS SPINDLE; OSCILLATION; PHENOTYPE; PRIORITY JOURNAL; CHROMATID; CHROMOSOME SEGREGATION; GENETICS; HELA CELL LINE; METABOLISM;

CHROMATIDS; CHROMOSOME SEGREGATION; CHROMOSOMES, HUMAN; HELA CELLS; HUMANS; KINESIN; KINETOCHORES; MITOSIS;

EID: 84891519583     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2013.08.004     Document Type: Article

References (51)

1. Amaro A.C., Samora C.P., Holtackers R., Wang E., Kingston I.J., Alonso M.C., Lampson M.A., McAinsh A.D., Meraldi P. Molecular control of kinetochore-microtubule dynamics and chromosome oscillations. Nat. Cell Biol. 2010, 12:319-329.
2. Binous H., Phillips R.J. Dynamic simulation of one and two particles sedimenting in viscoelastic suspensions of FENE dumbbells. J.Non-Newt. Fluid Mech. 1999, 83:93-130.
3. Boleti H., Karsenti E., Vernos I. Xklp2, a novel Xenopus centrosomal kinesin-like protein required for centrosome separation during mitosis. Cell 1996, 84:49-59.
4. Braun M., Drummond D.R., Cross R.A., McAinsh A.D. The kinesin-14 Klp2 organizes microtubules into parallel bundles by an ATP-dependent sorting mechanism. Nat. Cell Biol. 2009, 11:724-730.
5. Cai S., O'Connell C.B., Khodjakov A.L., Walczak C.E. Chromosome congression in the absence of kinetochore fibres. Nat. Cell Biol. 2009, 11:832-838.
6. Cameron L.A., Yang G., Cimini D., Canman J.C., Kisurina-Evgenieva O., Khodjakov A.L., Danuser G., Salmon E.D. Kinesin 5-independent poleward flux of kinetochore microtubules in PtK1 cells. J.Cell Biol. 2006, 173:173-179.
7. Chaly N., Brown D.L. The prometaphase configuration and chromosome order in early mitosis. J.Cell Sci. 1988, 91:325-335.
8. Chikashige Y., Ding D.Q., Funabiki H., Haraguchi T., Mashiko S., Yanagida M., Hiraoka Y. Telomere-led premeiotic chromosome movement in fission yeast. Science 1994, 264:270-273.
9. Civelekoglu-Scholey G., He B., Shen M., Wan X., Roscioli E., Bowden B., Cimini D. Dynamic bonds and polar ejection force distribution explain kinetochore oscillations in PtK1 cells. J.Cell Biol. 2013, 201:577-593.
10. Cole D.G., Saxton W.M., Sheehan K.B., Scholey J.M. A "slow" homotetrameric kinesin-related motor protein purified from Drosophila embryos. J.Biol. Chem. 1994, 269:22913-22916.
11. Crevel I.M.-T.C., Alonso M.C., Cross R.A. Monastrol stabilises an attached low-friction mode of Eg5. Curr. Biol. 2004, 14:R411-R412.
12. DeBonis S., Skoufias D.A., Lebeau L., Lopez R., Robin G., Margolis R.L., Wade R.H., Kozielski F. Invitro screening for inhibitors of the human mitotic kinesin Eg5 with antimitotic and antitumor activities. Mol. Cancer Ther. 2004, 3:1079-1090.
13. Fink G., Hajdo L., Skowronek K.J., Reuther C., Kasprzak A.A., Diez S. The mitotic kinesin-14 Ncd drives directional microtubule-microtubule sliding. Nat. Cell Biol. 2009, 11:717-723.
14. Funabiki H., Murray A.W. The Xenopus chromokinesin Xkid is essential for metaphase chromosome alignment and must be degraded to allow anaphase chromosome movement. Cell 2000, 102:411-424.
15. Ganem N.J., Upton K., Compton D.A. Efficient mitosis in human cells lacking poleward microtubule flux. Curr. Biol. 2005, 15:1827-1832.
16. Gardner M.K., Bouck D.C., Paliulis L.V., Meehl J.B., O'Toole E.T., Haase J., Soubry A., Joglekar A.P., Winey M., Salmon E.D., et al. Chromosome congression by Kinesin-5 motor-mediated disassembly of longer kinetochore microtubules. Cell 2008, 135:894-906.
17. Gartner M., Sunder-Plassmann N., Seiler J., Utz M., Vernos I., Surrey T., Giannis A. Development and biological evaluation of potent and specific inhibitors of mitotic Kinesin Eg5. ChemBioChem 2005, 6:1173-1177.
18. Gerlich D.W., Hirota T., Koch B., Peters J.-M., Ellenberg J. Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. Curr. Biol. 2006, 16:333-344.
19. Groen A.C., Needleman D.J., Brangwynne C.P., Gradinaru C., Fowler B., Mazitschek R., Mitchison T.J. A novel small-molecule inhibitor reveals a possible role of kinesin-5 in anastral spindle-pole assembly. J.Cell Sci. 2008, 121:2293-2300.
20. Hentrich C., Surrey T. Microtubule organization by the antagonistic mitotic motors kinesin-5 and kinesin-14. J.Cell Biol. 2010, 189:465-480.
21. Jaqaman K., King E.M., Amaro A.C., Winter J.R., Dorn J.F., Elliott H.L., Mchedlishvili N., McClelland S.E., Porter I.M., Posch M., et al. Kinetochore alignment within the metaphase plate is regulated by centromere stiffness and microtubule depolymerases. J.Cell Biol. 2010, 188:665-679.
22. Joglekar A.P., Hunt A.J. A simple, mechanistic model for directional instability during mitotic chromosome movements. Biophys. J. 2002, 83:42-58.
23. Kapitein L.C., Peterman E.J.G., Kwok B.H., Kim J.H., Kapoor T.M., Schmidt C.F. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature 2005, 435:114-118.
24. Kapoor T.M., Mitchison T.J. Eg5 is static in bipolar spindles relative to tubulin: evidence for a static spindle matrix. J.Cell Biol. 2001, 154:1125-1133.
25. Kashina A.S., Baskin R.J., Cole D.G., Wedaman K.P., Saxton W.M., Scholey J.M. A bipolar kinesin. Nature 1996, 379:270-272.
26. Kitajima T.S., Ohsugi M., Ellenberg J. Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 2011, 146:568-581.
27. Ma N., Titus J., Gable A., Ross J.L., Wadsworth P. TPX2 regulates the localization and activity of Eg5 in the mammalian mitotic spindle. J.Cell Biol. 2011, 195:87-98.
28. Magidson V., O'Connell C.B., Lončarek J., Paul R., Mogilner A., Khodjakov A.L. The spatial arrangement of chromosomes during prometaphase facilitates spindle assembly. Cell 2011, 146:555-567.
29. Maiato H., Rieder C.L., Khodjakov A.L. Kinetochore-driven formation of kinetochore fibers contributes to spindle assembly during animal mitosis. J.Cell Biol. 2004, 167:831-840.
30. Matos I., Pereira A.J., Lince-Faria M., Cameron L.A., Salmon E.D., Maiato H. Synchronizing chromosome segregation by flux-dependent force equalization at kinetochores. J.Cell Biol. 2009, 186:11-26.
31. Mayer T.U., Kapoor T.M., Haggarty S.J., King R.W., Schreiber S.L., Mitchison T.J. Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 1999, 286:971-974.
32. Mchedlishvili N., Wieser S., Holtackers R., Mouysset J., Belwal M., Amaro A.C., Meraldi P. Kinetochores accelerate centrosome separation to ensure faithful chromosome segregation. J.Cell Sci. 2012, 125:906-918.
33. McIntosh J.R., Molodtsov M.I., Ataullakhanov F.I. Biophysics of mitosis. Q.Rev. Biophys. 2012, 45:147-207.
34. Mountain V., Simerly C., Howard L., Ando A., Schatten G., Compton D.A. The kinesin-related protein, HSET, opposes the activity of Eg5 and cross-links microtubules in the mammalian mitotic spindle. J.Cell Biol. 1999, 147:351-366.
35. Nicklas R.B., Arana P. Evolution and the meaning of metaphase. J.Cell Sci. 1992, 102:681-690.
36. Nicklas R.B., Kubai D.F., Hays T.S. Spindle microtubules and their mechanical associations after micromanipulation in anaphase. J.Cell Biol. 1982, 95:91-104.
37. Press W.H., Teukolsky S.A., Vetterling W.T., Flannery B.P. The Art of Scientific Computing 2007, Cambridge University Press, New York. Third Edition.
38. Qi H., Rath U., Wang D., Xu Y.-Z., Ding Y., Zhang W., Blacketer M.J., Paddy M.R., Girton J., Johansen J., Johansen K.M. Megator, an essential coiled-coil protein that localizes to the putative spindle matrix during mitosis in Drosophila. Mol. Biol. Cell 2004, 15:4854-4865.
39. Rieder C.L., Davison E.A., Jensen L.C., Cassimeris L., Salmon E.D. Oscillatory movements of monooriented chromosomes and their position relative to the spindle pole result from the ejection properties of the aster and half-spindle. J.Cell Biol. 1986, 103:581-591.
40. Samora C.P., Mogessie B., Conway L., Ross J.L., Straube A., McAinsh A.D. MAP4 and CLASP1 operate as a safety mechanism to maintain a stable spindle position in mitosis. Nat. Cell Biol. 2011, 13:1040-1050.
41. Sawin K.E., LeGuellec K., Philippe M., Mitchison T.J. Mitotic spindle organization by a plus-end-directed microtubule motor. Nature 1992, 359:540-543.
42. Shimamoto Y., Maeda Y.T., Ishiwata S., Libchaber A.J., Kapoor T.M. Insights into the micromechanical properties of the metaphase spindle. Cell 2011, 145:1062-1074.
43. Skibbens R.V., Skeen V.P., Salmon E.D. Directional instability of kinetochore motility during chromosome congression and segregation in mitotic newt lung cells: a push-pull mechanism. J.Cell Biol. 1993, 122:859-875.
44. Stumpff J., Wagenbach M., Franck A.D., Asbury C.L., Wordeman L. Kif18A and chromokinesins confine centromere movements via microtubule growth suppression and spatial control of kinetochore tension. Dev. Cell 2012, 22:1017-1029.
45. Sturgill E.G., Ohi R. Kinesin-12 differentially affects spindle assembly depending on its microtubule substrate. Curr. Biol. 2013, 23:1280-1290.
46. Tanenbaum M.E., Macůrek L., Janssen A., Geers E.F., Alvarez-Fernández M., Medema R.H. Kif15 cooperates with eg5 to promote bipolar spindle assembly. Curr. Biol. 2009, 19:1703-1711.
47. Tsai M.-Y., Wang S., Heidinger J.M., Shumaker D.K., Adam S.A., Goldman R.D., Zheng Y. A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 2006, 311:1887-1893.
48. Vanneste D., Takagi M., Imamoto N., Vernos I. The role of Hklp2 in the stabilization and maintenance of spindle bipolarity. Curr. Biol. 2009, 19:1712-1717.
49. Wandke C., Barisic M., Sigl R., Rauch V., Wolf F., Amaro A.C., Tan C.H., Pereira A.J., Kutay U., Maiato H., et al. Human chromokinesins promote chromosome congression and spindle microtubule dynamics during mitosis. J.Cell Biol. 2012, 198:847-863.
50. Waters J.C., Mitchison T.J., Rieder C.L., Salmon E.D. The kinetochore microtubule minus-end disassembly associated with poleward flux produces a force that can do work. Mol. Biol. Cell 1996, 7:1547-1558.
51. Yamamoto A., West R.R., McIntosh J.R., Hiraoka Y. A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast. J.Cell Biol. 1999, 145:1233-1249.