The coupling between sister kinetochore directional instability and oscillations in centromere stretch in metaphase PtK1 cells

Molecular Biology of the Cell

Volumn 23, Issue 6, 2012, Pages 1035-1046

  Wan, Xiaohu ^a   Cimini, Daniela ^a,b   Cameron, Lisa A ^a,c   Salmon, E D ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CENTROMERE; CHROMOSOME; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DEPOLYMERIZATION; GENE SWITCHING; METAPHASE; MICROSATELLITE INSTABILITY; MICROTUBULE; NEWT; NONHUMAN; OSCILLATION; POLYMERIZATION; PRIORITY JOURNAL; SPINDLE CELL;

ANIMALS; CELL LINE; CENTROMERE; CHROMOSOMES; DIPODOMYS; KINETOCHORES; METAPHASE; MITOTIC SPINDLE APPARATUS;

MAMMALIA; VERTEBRATA;

EID: 84858387979     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-09-0767     Document Type: Article

References (54)

1. Akiyoshi B, Sarangapani KK, Powers AF, Nelson CR, Reichow SL, Arellano-Santoyo H, Gonen T, Ranish JA, Asbury CL, Biggins S (2010). Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468, 576-579.
2. Amaro AC, Samora CP, Holtackers R, Wang E, Kingston IJ, Alonso M, Lampson M, McAinsh AD, Meraldi P (2010). Molecular control of kinetochore-microtubule dynamics and chromosome oscillations. Nat Cell Biol 12, 319-329.
3. Cai S, O'Connell CB, Khodjakov A, Walczak CE (2009). Chromosome congression in the absence of kinetochore fibres. Nat Cell Biol 11, 832-838.
4. Cameron LA, Yang G, Cimini D, Canman JC, Kisurina-Evgenieva O, Khodjakov A, Danuser G, Salmon ED (2006). Kinesin 5-independent poleward flux of kinetochore microtubules in PtK1 cells. J Cell Biol 173, 173-179.
5. Cassimeris L, Rieder CL, Rupp G, Salmon ED (1990). Stability of microtubule attachment to metaphase kinetochores in PtK1 cells. J Cell Sci 96, 9-15.
6. Cassimeris L, Rieder CL, Salmon ED (1994). Microtubule assembly and kinetochore directional instability in vertebrate monopolar spindles: implications for the mechanism of chromosome congression. J Cell Sci 107, 285-297. (Pubitemid 24039054)
7. Cimini D, Cameron LA, Salmon ED (2004). Anaphase spindle mechanics prevent mis-segregation of merotelically oriented chromosomes. Curr Biol 14, 2149-2155. (Pubitemid 39623198)
8. Cimini D, Wan X, Hirel CB, Salmon ED (2006). Aurora kinase promotes turnover of kinetochore microtubules to reduce chromosome segregation errors. Curr Biol 16, 1711-1718. (Pubitemid 44691779)
9. DeLuca JG, Gall WE, Ciferri C, Cimini D, Musacchio A, Salmon ED (2006). Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127, 969-982. (Pubitemid 44792254)
10. Du Y, English CA, Ohi R (2010). The kinesin-8 Kif18A dampens microtubule plus-end dynamics. Curr Biol 20, 374-380.
11. Dumont S, Mitchison TJ (2009). Compression regulates mitotic spindle length by a mechanochemical switch at the poles. Curr Biol 19, 1086-1095.
12. Gardner MK et al. (2008). Chromosome congression by kinesin-5 motor-mediated disassembly of longer kinetochore microtubules. Cell 135, 894-906.
13. Hays TS, Salmon ED (1990). Poleward force at the kinetochore in metaphase depends on the number of kinetochore microtubules. J Cell Biol 110, 391-404.
14. Hoffman DB, Pearson CG, Yen TJ, Howell BJ, Salmon ED (2001). Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. Mol Biol Cell 12, 1995-2009. (Pubitemid 33049694)
15. Inoué S, Salmon ED (1995). Force generation by microtubule assembly/disassembly in mitosis and related movements. Mol Biol Cell 6, 1619-1640.
16. Jaqaman K et al. (2010). Kinetochore alignment within the metaphase plate is regulated by centromere stiffness and microtubule depolymerases. J Cell Biol 188, 665-679.
17. Joglekar AP, Hunt AJ (2002). A simple, mechanistic model for directional instability during mitotic chromosome movements. Biophys J 83, 42-58. (Pubitemid 34694719)
18. Kapoor TM, Lampson MA, Hergert P, Cameron L, Cimini D, Salmon ED, McEwen BF, Khodjakov A (2006). Chromosomes can congress to the metaphase plate before biorientation. Science 311, 388-391. (Pubitemid 43132665)
19. Ke K, Cheng J, Hunt AJ (2009). The distribution of polar ejection forces determines the amplitude of chromosome directional instability. Curr Biol 19, 807-815.
20. Khodjakov A, Cole RW, McEwen BF, Buttle KF, Rieder CL (1997). Chromosome fragments possessing only one kinetochore can congress to the spindle equator. J Cell Biol 136, 229-240. (Pubitemid 27063077)
21. Khodjakov A, Rieder CL (1996). Kinetochores moving away from their associated pole do not exert a significant pushing force on the chromosome. J Cell Biol 135, 315-327. (Pubitemid 26359328)
22. LaFountain JR Jr (1972). Spindle shape changes as an indicator of force production in crane-fly spermatocytes. J Cell Sci 10, 79-93.
23. Levesque AA, Compton DA (2001). The chromokinesin Kid is necessary for chromosome arm orientation and oscillation, but not congression, on mitotic spindles. J Cell Biol 154, 1135-1146. (Pubitemid 34286192)
24. Liu J, Desai A, Onuchic JN, Hwa T (2008). An integrated mechanobiochemical feedback mechanism describes chromosome motility from prometaphase to anaphase in mitosis. Proc Natl Acad Sci USA 105, 13752-13757.
25. Maddox P, Straight A, Coughlin P, Mitchison TJ, Salmon ED (2003). Direct observation of microtubule dynamics at kinetochores in Xenopus extract spindles: implications for spindle mechanics. J Cell Biol 162, 377-382. (Pubitemid 36988547)
26. Magidson V, O'Connell CB, Lonèarek J, Paul R, Mogilner A, Khodjakov A (2011). The spatial arrangement of chromosomes during prometaphase facilitates spindle assembly. Cell 146, 555-567.
27. Maiato H, DeLuca J, Salmon ED, Earnshaw WC (2004). The dynamic kinetochore-microtubule interface. J Cell Sci 117, 5461-5477. (Pubitemid 40012194)
28. Maiato H, Hergert PJ, Moutinho-Pereira S, Dong Y, Vandenbeldt KJ, Rieder CL, McEwen BF (2006). The ultrastructure of the kinetochore and kinetochore fiber in Drosophila somatic cells. Chromosoma 115, 469-480. (Pubitemid 44642639)
29. Maiato H, Rieder CL, Khodjakov A (2004). Kinetochore-driven formation of kinetochore fibers contributes to spindle assembly during animal mitosis. J Cell Biol 167, 831-840. (Pubitemid 39628106)
30. Maresca TJ, Salmon ED (2010). Welcome to a new kind of tension: translating kinetochore mechanics into a wait-anaphase signal. J Cell Sci 123, 825-835.
31. Mayr MI, Hummer S, Bormann J, Gruner T, Adio S, Woehlke G, Mayer TU (2007). The human kinesin Kif18A is a motile microtubule depolymerase essential for chromosome congression. Curr Biol 17, 488-498. (Pubitemid 46401386)
32. McEwen BF, Ding Y, Heagle AB (1998). Relevance of kinetochore size and microtubule-binding capacity for stable chromosome attachment during mitosis in PtK1 cells. Chromosome Res 6, 123-132. (Pubitemid 28121896)
33. McEwen BF, Heagle AB, Cassels GO, Buttle KF, Rieder CL (1997). Kinetochore fiber maturation in PtK1 cells and its implications for the mechanisms of chromosome congression and anaphase onset. J Cell Biol 137, 1567-1580. (Pubitemid 27282237)
34. Mitchison TJ (1989). Polewards microtubule flux in the mitotic spindle: evidence from photoactivation of fluorescence. J Cell Biol 109, 637-652.
35. Mitchison TJ, Salmon ED (1992). Poleward kinetochore fiber movement occurs during both metaphase and anaphase-A in newt lung cell mitosis. J Cell Biol 119, 569-582.
36. Nicklas RB, Campbell MS, Ward SC, Gorbsky GJ (1998). Tension-sensitive kinetochore phosphorylation in vitro. J Cell Sci 111, 3189-3196. (Pubitemid 28532429)
37. Rieder CL (1981). The structure of the cold-stable kinetochore fiber in metaphase PtK1 cells. Chromosoma 84, 145-158.
38. Rieder CL, Davison EA, Jensen LC, Cassimeris L, Salmon ED (1986). 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 103, 581-591. (Pubitemid 16055053)
39. Rieder CL, Salmon ED (1994). Motile kinetochores and polar ejection forces dictate chromosome position on the vertebrate mitotic spindle. J Cell Biol 124, 223-233. (Pubitemid 24050342)
40. Rieder CL, Salmon ED (1998). The vertebrate cell kinetochore and its roles during mitosis. Trends Cell Biol 8, 310-318. (Pubitemid 28362588)
41. Santaguida S, Musacchio A (2009). The life and miracles of kinetochores. EMBO J 28, 2511-2531.
42. Skibbens RV, Rieder CL, Salmon ED (1995). Kinetochore motility after severing between sister centromeres using laser microsurgery: evidence that kinetochore directional instability and position is regulated by tension. J Cell Sci 108, 2537-2548.
43. Skibbens RV, Salmon ED (1997). Micromanipulation of chromosomes in mitotic vertebrate tissue cells: tension controls the state of kinetochore movement. Exp Cell Res 235, 314-324. (Pubitemid 27398389)
44. Skibbens RV, Skeen VP, Salmon ED (1993). Directional instability of kinetochore motility during chromosome congression and segregation in mitotic newt lung cells: a push-pull mechanism. J Cell Biol 122, 859-875. (Pubitemid 23241095)
45. Stumpff J, von Dassow G, Wagenbach M, Asbury C, Wordeman L (2008). The kinesin-8 motor Kif18A suppresses kinetochore movements to control mitotic chromosome alignment. Dev Cell 14, 252-262. (Pubitemid 351189173)
46. Tirnauer JS, Canman JC, Salmon ED, Mitchison TJ (2002). EB1 targets to kinetochores with attached, polymerizing microtubules. Mol Biol Cell 13, 4308-4316. (Pubitemid 35471187)
47. VandenBeldt KJ, Barnard RM, Hergert PJ, Meng X, Maiato H, McEwen BF (2006). Kinetochores use a novel mechanism for coordinating the dynamics of individual microtubules. Curr Biol 16, 1217-1223. (Pubitemid 43867295)
48. Varga V, Helenius J, Tanaka K, Hyman AA, Tanaka TU, Howard J (2006). Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner. Nat Cell Biol 8, 957-962. (Pubitemid 44314726)
49. Vladimirou E, Harry E, Burroughs N, McAinsh AD (2011). Springs, clutches and motors: driving forward kinetochore mechanism by modelling. Chromosome Res 19, 409-421.
50. Wan X et al. (2009). Protein architecture of the human kinetochore microtubule attachment site. Cell 137, 672-684.
51. Waters JC, Mitchison TJ, Rieder CL, Salmon ED (1996a). The kinetochore microtubule minus-end disassembly associated with poleward flux produces a force that can do work. Mol Biol Cell 7, 1547-1558. (Pubitemid 26339728)
52. Waters JC, Skibbens RV, Salmon ED (1996b). Oscillating mitotic newt lung cell kinetochores are, on average, under tension and rarely push. J Cell Sci 109, 2823-2831. (Pubitemid 27029253)
53. Wordeman L, Wagenbach M, von Dassow G (2007). MCAK facilitates chromosome movement by promoting kinetochore microtubule turnover. J Cell Biol 179, 869-879. (Pubitemid 350223485)
54. Zhai Y, Kronebusch PJ, Borisy GG (1995). Kinetochore microtubule dynamics and the metaphase-anaphase transition. J Cell Biol 131, 721-734.