Insights into the micromechanical properties of the metaphase spindle

Cell

Volumn 145, Issue 7, 2011, Pages 1062-1074

  Shimamoto, Yuta ^a   Maeda, Yusuke T ^a   Ishiwata, Shin'Ichi ^b   Libchaber, Albert J ^a   Kapoor, Tarun M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b WASEDA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASMIC DYNEIN; KINESIN 5;

ARTICLE; CELL FUNCTION; CELL STRUCTURE; CENTROMERE; CONTROLLED STUDY; CYTOARCHITECTURE; DENSITY; ELASTICITY; MECHANICS; METAPHASE; MICROSCOPY; MICROTUBULE; NEEDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; SPINDLE CELL; SPINDLE POLE BODY; VISCOELASTICITY; VISCOSITY;

VERTEBRATA;

EID: 79959644058     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.05.038     Document Type: Article

References (63)

1. S.P. Alexander, and C.L. Rieder Chromosome motion during attachment to the vertebrate spindle: initial saltatory-like behavior of chromosomes and quantitative analysis of force production by nascent kinetochore fibers J. Cell Biol. 113 1991 805 815 (Pubitemid 21909716)
2. L.D. Belmont, and T.J. Mitchison Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules Cell 84 1996 623 631 (Pubitemid 26071742)
3. K.S. Burbank, A.C. Groen, Z.E. Perlman, D.S. Fisher, and T.J. Mitchison A new method reveals microtubule minus ends throughout the meiotic spindle J. Cell Biol. 175 2006 369 375 (Pubitemid 44708061)
4. A. Chakravarty, L. Howard, and D.A. Compton A mechanistic model for the organization of microtubule asters by motor and non-motor proteins in a mammalian mitotic extract Mol. Biol. Cell 15 2004 2116 2132 (Pubitemid 38580632)
5. C.R. Cowan, and A.A. Hyman Asymmetric cell division in C. elegans: cortical polarity and spindle positioning Annu. Rev. Cell Dev. Biol. 20 2004 427 453 (Pubitemid 39488645)
6. A. Desai, A. Murray, T.J. Mitchison, and C.E. Walczak The use of Xenopus egg extracts to study mitotic spindle assembly and function in vitro Methods Cell Biol. 61 1999 385 412
7. M. Dogterom, and B. Yurke Measurement of the force-velocity relation for growing microtubules Science 278 1997 856 860 (Pubitemid 27467922)
8. S. Dumont, and T.J. Mitchison Compression regulates mitotic spindle length by a mechanochemical switch at the poles Curr. Biol. 19 2009 1086 1095
9. R.M. Evans, M. Tassieri, D. Auhl, and T.A. Waigh Direct conversion of rheological compliance measurements into storage and loss moduli Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 80 2009 012501
10. D.A. Fletcher, and R.D. Mullins Cell mechanics and the cytoskeleton Nature 463 2010 485 492
11. J. Gaetz, and T.M. Kapoor Dynein/dynactin regulate metaphase spindle length by targeting depolymerizing activities to spindle poles J. Cell Biol. 166 2004 465 471 (Pubitemid 39097165)
12. M.L. Gardel, K.E. Kasza, C.P. Brangwynne, J. Liu, and D.A. Weitz Chapter 19: Mechanical response of cytoskeletal networks Methods Cell Biol. 89 2008 487 519
13. J.C. Gatlin, A. Matov, G. Danuser, T.J. Mitchison, and E.D. Salmon Directly probing the mechanical properties of the spindle and its matrix J. Cell Biol. 188 2010 481 489
14. A. Gennerich, A.P. Carter, S.L. Reck-Peterson, and R.D. Vale Force-induced bidirectional stepping of cytoplasmic dynein Cell 131 2007 952 965 (Pubitemid 350138087)
15. F. Gittes, B. Mickey, J. Nettleton, and J. Howard Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape J. Cell Biol. 120 1993 923 934 (Pubitemid 23056298)
16. G. Goshima, and J.M. Scholey Control of mitotic spindle length Annu. Rev. Cell Dev. Biol. 26 2010 21 57
17. N. Hirokawa Kinesin and dynein superfamily proteins and the mechanism of organelle transport Science 279 1998 519 526 (Pubitemid 28067273)
18. B.R. Houghtaling, G. Yang, A. Matov, G. Danuser, and T.M. Kapoor Op18 reveals the contribution of nonkinetochore microtubules to the dynamic organization of the vertebrate meiotic spindle Proc. Natl. Acad. Sci. USA 106 2009 15338 15343
19. J. Howard Mechanics of Motor Proteins and the Cytoskeleton 2001 Sinauer Associates Massachusetts
20. S.E. Hughes, W.D. Gilliland, J.L. Cotitta, S. Takeo, K.A. Collins, and R.S. Hawley Heterochromatic threads connect oscillating chromosomes during prometaphase I in Drosophila oocytes PLoS Genet. 5 2009 e1000348
21. S. Inoué, and E.D. Salmon Force generation by microtubule assembly/disassembly in mitosis and related movements Mol. Biol. Cell 6 1995 1619 1640
22. T. Itabashi, J. Takagi, Y. Shimamoto, H. Onoe, K. Kuwana, I. Shimoyama, J. Gaetz, T.M. Kapoor, and S. Ishiwata Probing the mechanical architecture of the vertebrate meiotic spindle Nat. Methods 6 2009 167 172
23. P.A. Janmey, P.C. Georges, and S. Hvidt Basic rheology for biologists Methods Cell Biol. 83 2007 3 27
24. T.M. Kapoor, M.A. Lampson, P. Hergert, L. Cameron, D. Cimini, E.D. Salmon, B.F. McEwen, and A. Khodjakov Chromosomes can congress to the metaphase plate before biorientation Science 311 2006 388 391 (Pubitemid 43132665)
25. S. Karki, and E.L. Holzbaur Cytoplasmic dynein and dynactin in cell division and intracellular transport Curr. Opin. Cell Biol. 11 1999 45 53 (Pubitemid 29084131)
26. A. Kishino, and T. Yanagida Force measurements by micromanipulation of a single actin filament by glass needles Nature 334 1988 74 76
27. B.H. Kwok, and T.M. Kapoor Microtubule flux: drivers wanted Curr. Opin. Cell Biol. 19 2007 36 42 (Pubitemid 46123969)
28. R.J. Leslie, and J.D. Pickett-Heaps Spindle microtubule dynamics following ultraviolet-microbeam irradiations of mitotic diatoms Cell 36 1984 717 727
29. Y. Lin, G.H. Koenderink, F.C. MacKintosh, and D.A. Weitz Viscoelastic properties of microtubule networks Macromolecules 40 2007 771407720
30. J.R. McIntosh, and S.C. Landis The distribution of spindle microtubules during mitosis in cultured human cells J. Cell Biol. 49 1971 468 497
31. J.R. McIntosh, W.Z. Cande, and J.A. Snyder Structure and physiology of the mammalian mitotic spindle Soc. Gen. Physiol. Ser. 30 1975 31 76
32. T. Mitchison, and M. Kirschner Dynamic instability of microtubule growth Nature 312 1984 237 242 (Pubitemid 15201998)
33. T.J. Mitchison, P. Maddox, J. Gaetz, A. Groen, M. Shirasu, A. Desai, E.D. Salmon, and T.M. Kapoor Roles of polymerization dynamics, opposed motors, and a tensile element in governing the length of Xenopus extract meiotic spindles Mol. Biol. Cell 16 2005 3064 3076 (Pubitemid 40741248)
34. A. Mogilner, and E. Craig Towards a quantitative understanding of mitotic spindle assembly and mechanics J. Cell Sci. 123 2010 3435 3445
35. F. Nédélec, and T. Surrey Assaying spatial organization of microtubules by kinesin motors Methods Mol. Biol. 164 2001 213 222
36. B. Neumann, T. Walter, J.K. Hériché, J. Bulkescher, H. Erfle, C. Conrad, P. Rogers, I. Poser, M. Held, and U. Liebel Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes Nature 464 2010 721 727
37. R.B. Nicklas Chromosome velocity during mitosis as a function of chromosome size and position J. Cell Biol. 25 1965 119 135
38. R.B. Nicklas Measurements of the force produced by the mitotic spindle in anaphase J. Cell Biol. 97 1983 542 548 (Pubitemid 13041017)
39. R. Ohi, K. Burbank, Q. Liu, and T.J. Mitchison Nonredundant functions of Kinesin-13s during meiotic spindle assembly Curr. Biol. 17 2007 953 959 (Pubitemid 46829840)
40. E.D. Salmon, R.J. Leslie, W.M. Saxton, M.L. Karow, and J.R. McIntosh Spindle microtubule dynamics in sea urchin embryos: analysis using a fluorescein-labeled tubulin and measurements of fluorescence redistribution after laser photobleaching J. Cell Biol. 99 1984 2165 2174 (Pubitemid 15181880)
41. M. Sato, W.H. Schwartz, S.C. Selden, and T.D. Pollard Mechanical properties of brain tubulin and microtubules J. Cell Biol. 106 1988 1205 1211
42. K.E. Sawin, and T.J. Mitchison Poleward microtubule flux mitotic spindles assembled in vitro J. Cell Biol. 112 1991 941 954 (Pubitemid 21909640)
43. K. Tawada, and K. Sekimoto Protein friction exerted by motor enzymes through a weak-binding interaction J. Theor. Biol. 150 1991 193 200
44. J.S. Tirnauer, E.D. Salmon, and T.J. Mitchison Microtubule plus-end dynamics in Xenopus egg extract spindles Mol. Biol. Cell 15 2004 1776 1784 (Pubitemid 38401826)
45. M.T. Valentine, Z.E. Perlman, M.L. Gardel, J.H. Shin, P. Matsudaira, T.J. Mitchison, and D.A. Weitz Colloid surface chemistry critically affects multiple particle tracking measurements of biomaterials Biophys. J. 86 2004 4004 4014 (Pubitemid 38780276)
46. M.T. Valentine, P.M. Fordyce, T.C. Krzysiak, S.P. Gilbert, and S.M. Block Individual dimers of the mitotic kinesin motor Eg5 step processively and support substantial loads in vitro Nat. Cell Biol. 8 2006 470 476
47. C.E. Walczak, and R. Heald Mechanisms of mitotic spindle assembly and function Int. Rev. Cytol. 265 2008 111 158 (Pubitemid 351215987)
48. J.C. Waters, R.V. Skibbens, and E.D. Salmon Oscillating mitotic newt lung cell kinetochores are, on average, under tension and rarely push J. Cell Sci. 109 1996 2823 2831 (Pubitemid 27029253)
49. T. Wittmann, and T. Hyman Recombinant p50/dynamitin as a tool to examine the role of dynactin in intracellular processes Methods Cell Biol. 61 1999 137 143
50. G. Yang, B.R. Houghtaling, J. Gaetz, J.Z. Liu, G. Danuser, and T.M. Kapoor Architectural dynamics of the meiotic spindle revealed by single-fluorophore imaging Nat. Cell Biol. 9 2007 1233 1242 (Pubitemid 350042355)
51. Y. Zhai, P.J. Kronebusch, and G.G. Borisy Kinetochore microtubule dynamics and the metaphase-anaphase transition J. Cell Biol. 131 1995 721 734
52. Burbank, K.S., Groen, A.C., Perlman, Z.E., Fisher, D.S., and Mitchison, T.J. (2006). A new method reveals microtubule minus ends throughout the meiotic spindle. J. Cell Biol. 175, 369-375. (Pubitemid 44708061)
53. Claessens, M.M., Bathe, M., Frey, E., and Bausch, A.R. (2006). Actin-binding proteins sensitively mediate F-actin bundle stiffness. Nat. Mater. 5, 748-753. (Pubitemid 44320328)
54. Evans, R.M., Tassieri, M., Auhl, D., and Waigh, T.A. (2009). Direct conversion of rheological compliance measurements into storage and loss moduli. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 80, 012501.
55. Ferry, J.D. (1980). Viscoelastic Properties of Polymers, Third Edition (New York: John Wiley & Sons).
56. Gittes, F., Mickey, B., Nettleton, J., and Howard, J. (1993). Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120, 923-934. (Pubitemid 23056298)
57. Howard, J. (2001). Mechanics of Motor Proteins and the Cytoskeleton (Massachusetts: Sinauer Associates).
58. Losada, A., and Hirano, T. (2001). Shaping the metaphase chromosome: coordination of cohesion and condensation. Bioessays 23, 924-935. (Pubitemid 32972692)
59. Maiato, H., DeLuca, J., Salmon, E.D., and Earnshaw, W.C. (2004). The dynamic kinetochore-microtubule interface. J. Cell Sci. 117, 5461-5477. (Pubitemid 40012194)
60. Mickey, B., and Howard, J. (1995). Rigidity of microtubules is increased by stabilizing agents. J. Cell Biol. 130, 909-917.
61. Ohi, R., Burbank, K., Liu, Q., and Mitchison, T.J. (2007). Nonredundant functions of Kinesin-13s during meiotic spindle assembly. Curr. Biol. 17, 953-959. (Pubitemid 46829840)
62. Sawin, K.E., and Mitchison, T.J. (1991). Poleward microtubule flux mitotic spindles assembled in vitro. J. Cell Biol. 112, 941-954. (Pubitemid 21909640)
63. Yang, G., Houghtaling, B.R., Gaetz, J., Liu, J.Z., Danuser, G., and Kapoor, T.M. (2007). Architectural dynamics of the meiotic spindle revealed by single-fluorophore imaging. Nat. Cell Biol. 9, 1233-1242. (Pubitemid 350042355)