1932

Abstract

The assembly of the mitotic spindle and the subsequent segregation of sister chromatids are based on the self-organized action of microtubule filaments, motor proteins, and other microtubule-associated proteins, which constitute the fundamental force-generating elements in the system. Many of the components in the spindle have been identified, but until recently it remained unclear how their collective behaviors resulted in such a robust bipolar structure. Here, we review the current understanding of the physics of the metaphase spindle that is only now starting to emerge.

[Erratum, Closure]

An erratum has been published for this article:
Erratum: The Physics of the Metaphase Spindle
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-060414-034107
2018-05-20
2024-10-04
Loading full text...

Full text loading...

/deliver/fulltext/biophys/47/1/annurev-biophys-060414-034107.html?itemId=/content/journals/10.1146/annurev-biophys-060414-034107&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Al-Obaidi N, Mitchison TJ, Crews CM, Mayer TU 2016. Identification of MAC1: a small molecule that rescues spindle bipolarity in monastrol-treated cells. ACS Chem. Biol. 11:1544–51
    [Google Scholar]
  2. 2.  Alexander SP, Rieder CL 1991. Chromosome motion during attachment to the vertebrate spindle: initial saltatory-like behaviour of chromosomes and quantitative analysis of force production by nascent kinetochore fibers. J. Cell Biol. 113:805–15
    [Google Scholar]
  3. 3.  Alvarado J, Sheinman M, Sharma A, MacKintosh FC, Koenderink GH 2013. Molecular motors robustly drive active gels to a critically connected state. Nat. Phys. 9:591–97
    [Google Scholar]
  4. 4.  Ault JG, Nicklas RB 1989. Tension, microtubule rearrangements, and the proper distribution of chromosomes in mitosis. Chromosoma 98:33–39
    [Google Scholar]
  5. 5.  Belmont LD, Hyman AA, Sawin KE, Mitchison TJ 1990. Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell 62:579–89
    [Google Scholar]
  6. 6.  Bendix PM, Koenderink GH, Cuvelier D, Dogic Z, Koeleman BN et al. 2008. A quantitative analysis of contractility in active cytoskeletal protein networks. Biophys. J. 94:3126–36
    [Google Scholar]
  7. 7.  Blangy A, Lane HA, d'Hérin P, Harper M, Kress M, Nigg EA 1995. Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo. Cell 83:1159–69
    [Google Scholar]
  8. 8.  Borisy GG, Taylor EW 1967. The mechanism of action of colchicine. J. Cell Biol. 34:525–33
    [Google Scholar]
  9. 9.  Brugués J, Needleman DJ 2014. Physical basis of spindle self-organization. PNAS 111:18496–500
    [Google Scholar]
  10. 10.  Brugués J, Nuzzo V, Mazur E, Needleman DJ 2012. Nucleation and transport organize microtubules in metaphase spindles. Cell 149:554–64
    [Google Scholar]
  11. 11.  Burbank KS, Mitchison TJ, Fisher DS 2007. Slide-and-cluster models for spindle assembly. Curr. Biol. 17:1373–83
    [Google Scholar]
  12. 12.  Carpenter AT. 1991. Distributive segregation: motors in the polar wind. ? Cell 64:885–90
    [Google Scholar]
  13. 13.  Caudron M, Bunt G, Bastiaens P, Karsenti E 2005. Spatial coordination of spindle assembly by chromosome-mediated signaling gradients. Science 309:1373–76
    [Google Scholar]
  14. 14.  Clarke PR, Zhang C 2008. Spatial and temporal coordination of mitosis by Ran GTPase. Nat. Rev. Mol. Cell Biol. 9:464–77
    [Google Scholar]
  15. 15.  Conde C, Cáceres A 2009. Microtubule assembly, organization and dynamics in axons and dendrites. Nat. Rev. Neurosci. 10:319–32
    [Google Scholar]
  16. 16.  Creus GJ. 1986. Viscoelasticity: Basic Theory and Applications to Concrete Structures Berlin: Springer-Verlag
    [Google Scholar]
  17. 17.  Cross RA, McAinsh A 2014. Prime movers: the mechanochemistry of mitotic kinesins. Nat. Rev. Mol. Cell Biol. 15:257–71
    [Google Scholar]
  18. 18.  Crowder ME, Strzelecka M, Wilbur JD, Good MC, von Dassow G, Heald R 2015. A comparative analysis of spindle morphometrics across metazoans. Curr. Biol. 25:1542–50
    [Google Scholar]
  19. 19.  de Gennes PG, Prost J 1974. The Physics of Liquid Crystals Oxford, UK: Clarendon Press
    [Google Scholar]
  20. 20.  Decker F, Oriola D, Dalton B, Brugués J 2018. Autocatalytic microtubule nucleation determines the mass and size of spindles. eLife 7:e31149
    [Google Scholar]
  21. 21.  Desai A, Murray A, Mitchison TJ, Walczak CE 1998. The use of Xenopus egg extracts to study mitotic spindle assembly and function in vitro. Meth. Cell Biol. 61:385–412
    [Google Scholar]
  22. 22.  Dinarina A, Pugieux C, Corral MM, Loose M, Spatz J et al. 2009. Chromatin shapes the mitotic spindle. Cell 138:502–13
    [Google Scholar]
  23. 23.  Dogterom M, Yurke B 1997. Measurement of the force-velocity relation for growing microtubules. Science 278:856–60
    [Google Scholar]
  24. 24.  Dumont S, Mitchison TJ 2009. Force and length in the mitotic spindle. Curr. Biol. 19:R749–61
    [Google Scholar]
  25. 25.  Elting MW, Prakash M, Udy DB, Dumont S 2017. Mapping load-bearing in the mammalian spindle reveals local kinetochore fiber anchorage that provides mechanical isolation and redundancy. Curr. Biol. 27:2112–22
    [Google Scholar]
  26. 26.  Enos AP, Morris NR 1990. Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans. Cell 60:1019–27
    [Google Scholar]
  27. 27.  Fink G, Schuchardt I, Colombelli J, Stelzer E, Steinberg G 2006. Dynein-mediated pulling forces drive rapid mitotic spindle elongation in Ustilago maydis. EMBO J 25:4897–908
    [Google Scholar]
  28. 28.  Flemming W. 1882. Zellsubstanz, Kern und Zelltheilung Leipzig, Ger.: FCW Vogel
    [Google Scholar]
  29. 29.  Forth S, Hsia KC, Shimamoto Y, Kapoor TM 2014. Asymmetric friction of nonmotor maps can lead to their directional motion in active microtubule networks. Cell 157:420–32
    [Google Scholar]
  30. 30.  Forth S, Kapoor TM 2017. The mechanics of microtubule networks in cell division. J. Cell Biol. 216:1525–31
    [Google Scholar]
  31. 31.  Foster PJ, Fürthauer S, Shelley MJ, Needleman DJ 2015. Active contraction of microtubule networks. eLife 4:e10837
    [Google Scholar]
  32. 32.  Gao T, Betterton MD, Jhang AS, Shelley MJ 2017. Analytical structure, dynamics, and coarse graining of a kinetic model of an active fluid. Phys. Rev. Fluids 2:093302
    [Google Scholar]
  33. 33.  Gao T, Blackwell R, Glaser MA, Betterton MD, Shelley MJ 2015. Multiscale polar theory of microtubule and motor-protein assemblies. Phys. Rev. Lett. 114:048101
    [Google Scholar]
  34. 34.  Gardner MK, Zanic M, Howard J 2013. Microtubule catastrophe and rescue. Curr. Opin. Cell Biol. 25:14–22
    [Google Scholar]
  35. 35.  Garzon-Coral C, Fantana HA, Howard J 2016. A force-generating machinery maintains the spindle at the cell center during mitosis. Science 352:1124–27
    [Google Scholar]
  36. 36.  Gatlin JC, Matov A, Groen AC, Needleman DJ, Maresca TJ et al. 2009. Spindle fusion requires dynein-mediated sliding of oppositely oriented microtubules. Curr. Biol. 19:287–96
    [Google Scholar]
  37. 37.  Gennerich A, Carter AP, Reck-Peterson SL, Vale RD 2007. Force-induced bidirectional stepping of cytoplasmic dynein. Cell 131:952–65
    [Google Scholar]
  38. 38.  Good MC, Vahey MD, Skandarajah A, Fletcher DA, Heald R 2013. Cytoplasmic volume modulates spindle size during embryogenesis. Science 342:856–60
    [Google Scholar]
  39. 39.  Goshima G, Vale RD 2003. The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J. Cell Biol. 162:1003–16
    [Google Scholar]
  40. 40.  Grill SW, Gönczy P, Stelzer EHK, Hyman AA 2001. Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409:630–33
    [Google Scholar]
  41. 41.  Grill SW, Howard J, Schäffer E, Stelzer EHK, Hyman AA 2003. The distribution of active force generators controls mitotic spindle position. Science 301:518–21
    [Google Scholar]
  42. 42.  Grill SW, Hyman AA 2005. Spindle positioning by cortical pulling forces. Dev. Cell 8:461–65
    [Google Scholar]
  43. 43.  Guillamat P, Ignés-Mullol J, Sagués F 2016. Control of active liquid crystals with a magnetic field. PNAS 113:5498–502
    [Google Scholar]
  44. 44.  Hannak E, Heald R 2006. Investigating mitotic spindle assembly and function in vitro using Xenopus laevis egg extracts. Nat. Protoc. 1:2305–14
    [Google Scholar]
  45. 45.  Hazel J, Krutkramelis K, Mooney P, Tomschik M, Gerow K et al. 2013. Changes in cytoplasmic volume are sufficient to drive spindle scaling. Science 342:853–56
    [Google Scholar]
  46. 46.  Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P et al. 1996. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382:420–25
    [Google Scholar]
  47. 47.  Hepler PK, Jackson WT 1968. Microtubules and early stages of cell-plate formation in the endosperm of Haemanthus katherinae baker. J. Cell Biol. 38:437–46
    [Google Scholar]
  48. 48.  Howard J. 2001. Mechanics of Motor Proteins and the Cytoskeleton Sunderland, MA: Sinauer Assoc
    [Google Scholar]
  49. 49.  Huxley H, Hanson J 1954. Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173:973–76
    [Google Scholar]
  50. 50.  Inoué S. 1953. Polarization optical studies of the mitotic spindle. I. The demonstration of spindle fibers in living cells. Chromosoma 5:487–500
    [Google Scholar]
  51. 51.  Inoué S, Sato H 1967. Cell motility by labile association of molecules: the nature of the mitotic spindle fibers and their role in chromosome movement. J. Gen. Physiol. 50:259–92
    [Google Scholar]
  52. 52.  Ishihara K, Korolev KS, Mitchison TJ 2016. Physical basis of large microtubule aster growth. eLife 5:e19145
    [Google Scholar]
  53. 53.  Ishihara K, Nguyen PA, Groen AC, Field CM, Mitchison TJ 2014. Microtubule nucleation remote from centrosomes may explain how asters span large cells. PNAS 111:17715–22
    [Google Scholar]
  54. 54.  Itabashi T, Takagi J, Shimamoto Y, Onoe H, Kuwana K et al. 2009. Probing the mechanical architecture of the vertebrate meiotic spindle. Nat. Meth. 6:167–72
    [Google Scholar]
  55. 55.  Jannasch A, Bormuth V, Storch M, Howard J, Schäffer E 2013. Kinesin-8 is a low-force motor protein with a weakly bound slip state. Biophys. J. 104:2456–64
    [Google Scholar]
  56. 56.  Joanny JF, Jülicher F, Kruse K, Prost J 2007. Hydrodynamic theory for multicomponent active gels. New J. Phys. 9:422
    [Google Scholar]
  57. 57.  Jülicher F, Kruse K, Prost J, Joanny JF 2007. Active behaviour of the cytoskeleton. Phys. Rep. 449:3–28
    [Google Scholar]
  58. 58.  Kálab P, Pralle A, Isacoff EY, Heald R, Weis K 2006. Analysis of a RanGTP-regulated gradient in mitotic somatic cells. Nature 440:697–701
    [Google Scholar]
  59. 59.  Karsenti E. 2008. Self-organization in cell biology: a brief history. Nat. Rev. Mol. Cell Biol. 9:255–62
    [Google Scholar]
  60. 60.  Kashina AS, Baskin RJ, Cole DG, Wedaman KP, Saxton WM, Scholey JM 1996. A bipolar kinesin. Nature 379:270–72
    [Google Scholar]
  61. 61.  Kimura K, Kimura A 2011. Intracellular organelles mediate cytoplasmic pulling force for centrosome centration in the Caenorhabditis elegans early embryo. PNAS 108:137–42
    [Google Scholar]
  62. 62.  Kittler R, Pelletier L, Heninger AK, Slabicki M, Theis M et al. 2007. Genome-scale RNAi profiling of cell division in human tissue culture cells. Nat. Cell Biol. 9:1401–12
    [Google Scholar]
  63. 63.  Kiyomitsu T, Cheeseman IM 2013. Cortical dynein and asymmetric membrane elongation coordinately position the spindle in anaphase. Cell 154:391–402
    [Google Scholar]
  64. 64.  Laan L, Husson J, Munteanu EL, Kerssemakers JWJ, Dogterom M 2008. Force-generation and dynamic instability of microtubule bundles. PNAS 105:8920–25
    [Google Scholar]
  65. 65.  Lansky Z, Braun M, Lüdecke A, Schlierf M, ten Wolde PR et al. 2015. Diffusible crosslinkers generate directed forces in microtubule networks. Cell 160:1159–68
    [Google Scholar]
  66. 66.  Liverpool TB, Marchetti MC 2006. Rheology of active filament solutions. Phys. Rev. Lett. 97:268101
    [Google Scholar]
  67. 67.  Loughlin R, Heald R, Nédélec F 2010. A computational model predicts Xenopus meiotic spindle organization. J. Cell Biol. 191:1239–49
    [Google Scholar]
  68. 68.  Maddox P, Desai A, Oegema K, Mitchison TJ, Salmon ED 2002. Poleward microtubule flux is a major component of spindle dynamics and anaphase A in mitotic Drosophila embryos. Curr. Biol. 12:1670–74
    [Google Scholar]
  69. 69.  Marchetti MC, Joanny JF, Ramaswamy S, Liverpool TB, Prost J et al. 2013. Hydrodynamics of soft active matter. Rev. Mod. Phys. 85:1143–89
    [Google Scholar]
  70. 70.  Mayer TU, Kapoor TM, Haggarty SJ, King RW, Schreiber SL, Mitchison TJ 1999. Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286:971–74
    [Google Scholar]
  71. 71.  McDonald KL, O'Toole ET, Mastronade DN, McIntosh JR 1992. Kinetochore microtubules in PTK cells. J. Cell Biol. 118:369–83
    [Google Scholar]
  72. 72.  McIntosh JR, Hepler PK, Van Wie DG 1969. Model for mitosis. Nature 224:659–63
    [Google Scholar]
  73. 73.  Meluh PB, Rose MD 1990. KAR3, a kinesin-related gene required for yeast nuclear fusion. Cell 60:1029–41
    [Google Scholar]
  74. 74.  Merdes A, Heald R, Samejima K, Earnshaw WC, Cleveland DW 2000. Formation of spindle poles by dynein/dynactin-dependent transport of Numa. J. Cell Biol. 149:851–62
    [Google Scholar]
  75. 75.  Merdes A, Ramyar K, Vechio JD, Cleveland DW 1996. A complex of Numa and cytoplasmic dynein is essential for mitotic spindle assembly. Cell 87:447–58
    [Google Scholar]
  76. 76.  Mirny L, Needleman DJ 2010. Quantitative characterization of filament dynamics by single-molecule lifetime measurements. Meth. Cell Biol. 95:583–600
    [Google Scholar]
  77. 77.  Mitchison T, Kirschner MW 1984. Dynamic instability of microtubule growth. Nature 312:237–42
    [Google Scholar]
  78. 78.  Mitchison TJ. 2005. Mechanism and function of poleward flux in Xenopus extract meiotic spindles. Philos. Trans. R. Soc. B Biol. Sci. 360:623–29
    [Google Scholar]
  79. 79.  Mitchison TJ, Ishihara K, Nguyen P, Wühr M 2015. Size scaling of microtubule assemblies in early Xenopus embryos. Cold Spring Harb. Perspect. Biol. 7:a019182
    [Google Scholar]
  80. 80.  Mitchison TJ, Maddox P, Gaetz J, Groen A, Shirasu M et al. 2005. Roles of polymerization dynamics, opposed motors, and a tensile element in governing the length of Xenopus extract meiotic spindles. Mol. Biol. Cell 16:3064–76
    [Google Scholar]
  81. 81.  Miyamoto DT, Perlman ZE, Burbank KS, Groen AC, Mitchison TJ 2004. The kinesin Eg5 drives poleward microtubule flux in Xenopus laevis egg extract spindles. J. Cell Biol. 167:813–18
    [Google Scholar]
  82. 82.  Mogilner A, Craig E 2010. Towards a quantitative understanding of mitotic spindle assembly and mechanics. J. Cell Sci. 123:3435–45
    [Google Scholar]
  83. 83.  Morales-Mulia S, Scholey JM 2005. Spindle pole organization in Drosophila S2 cells by dynein, Abnormal Spindle protein (Asp), and KLP10A. Mol. Biol. Cell 16:3176–86
    [Google Scholar]
  84. 84.  Murrel MP, Gardel ML 2012. F-actin buckling coordinates contractility and severing in a biomimetic actomyosin cortex. PNAS 109:20820–25
    [Google Scholar]
  85. 85.  Nédélec F. 2002. Computer simulations reveal motor properties generating stable antiparallel microtubule interactions. J. Cell Biol. 158:1005–15
    [Google Scholar]
  86. 86.  Nédélec F, Surrey T, Karsenti E 2003. Self-organisation and force in the microtubule cytoskeleton. Curr. Opin. Cell Biol. 15:118–24
    [Google Scholar]
  87. 87.  Needleman D, Dogic Z 2017. Active matter at the interface between materials science and cell biology. Nat. Rev. Mater. 2:17048
    [Google Scholar]
  88. 88.  Needleman DJ, Groen AC, Ohi R, Maresca T, Mirny L, Mitchison TJ 2010. Fast microtubule dynamics in meiotic spindles measured by single molecule imaging: evidence that the spindle environment does not stabilize microtubules. Mol. Biol. Cell 21:323–33
    [Google Scholar]
  89. 89.  Nicklas RB. 1983. Measurements of the force produced by the mitotic spindle in anaphase. J. Cell Biol. 97:542–48
    [Google Scholar]
  90. 90.  Nicklas RB. 1988. The forces that move chromosomes in mitosis. Annu. Rev. Biophys. Biophys. Chem. 17:431–49
    [Google Scholar]
  91. 91.  Oh D, Yu CH, Needleman DJ 2016. Spatial organization of the Ran pathway by microtubules in mitosis. PNAS 113:8729–34
    [Google Scholar]
  92. 92.  Oriola D, Alert R, Casademunt J 2017. Fluidization and active thinning by molecular kinetics in active gels. Phys. Rev. Lett. 118:088002
    [Google Scholar]
  93. 93.  Peterman EJG, Scholey JM 2009. Mitotic microtubule crosslinkers: insights from mechanistic studies. Curr. Biol. 19:R1089–94
    [Google Scholar]
  94. 94.  Petry S, Groen AC, Ishihara K, Mitchison TJ, Vale RD 2013. Branching microtubule nucleation in Xenopus egg extracts mediated by Augmin and TPX2. Cell 152:768–77
    [Google Scholar]
  95. 95.  Prost J, Jülicher F, Joanny JF 2015. Active gel physics. Nat. Phys. 11:111–17
    [Google Scholar]
  96. 96.  Rath O, Kozielski F 2012. Kinesins and cancer. Nat. Rev. Cancer 12:527–39
    [Google Scholar]
  97. 97.  Reber SB, Baumgart J, Widlund PO, Pozniakovsky A, Howard J et al. 2013. XMAP215 activity sets spindle length by controlling the total mass of spindle microtubules. Nat. Cell Biol. 15:1116–22
    [Google Scholar]
  98. 98.  Redemann S, Baumgart J, Lindow N, Shelley MJ, Nazockdast E et al. 2017. C. elegans chromosomes connect to centrosomes by anchoring into the spindle network. Nat. Commun. 8:15288
    [Google Scholar]
  99. 99.  Rieder CL, Davison EA, Jensen LCW, 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. 103:581–91
    [Google Scholar]
  100. 100.  Roof DM, Meluh PB, Rose MD 1992. Kinesin-related proteins required for assembly of the mitotic spindle. J. Cell Biol. 118:95–108
    [Google Scholar]
  101. 101.  Sanchez T, Chen DTN, DeCamp SJ, Heymann M, Dogic Z 2012. Spontaneous motion in hierarchically assembled active matter. Nature 491:431–34
    [Google Scholar]
  102. 102.  Sauer G, Körner R, Hanisch A, Ries A, Nigg EA, Silljé HH 2005. Proteome analysis of the human mitotic spindle. Mol. Cell. Proteom. 4:35–43
    [Google Scholar]
  103. 103.  Sawin KE, LeGuellec K, Philippe M, Mitchison TJ 1992. Mitotic spindle organization by a plus end–directed microtubule motor. Nature 359:540–43
    [Google Scholar]
  104. 104.  Sawin KE, Mitchison TJ 1991. Poleward microtubule flux mitotic spindles assembled in vitro. J. Cell Biol. 112:941–54
    [Google Scholar]
  105. 105.  Schermelleh L, Heintzmann R, Leonhardt H 2010. A guide to super-resolution fluorescence microscopy. J. Cell Biol. 190:165–75
    [Google Scholar]
  106. 106.  Sharp DJ, Yu KR, Sisson JC, Sullivan W, Schoely JM 1999. Antagonistic microtubule-sliding motors position mitotic centrosomes in Drosophila early embryos. Nat. Cell Biol. 1:51–54
    [Google Scholar]
  107. 107.  Shelley MJ. 2016. The dynamics of microtubule/motor-protein assemblies in biology and physics. Annu. Rev. Fluid Mech. 48:487–506
    [Google Scholar]
  108. 108.  Shimamoto Y, Maeda YT, Ishiwata S, Libchaber AJ, Kapoor TM 2011. Insights into the micromechanical properties of the metaphase spindle. Cell 145:1062–74
    [Google Scholar]
  109. 109.  Shinar T, Mana M, Piano F, Shelley MJ 2011. A model of cytoplasmically driven microtubule-based motion in the single-celled Caenorhabditis elegans embryo. PNAS 108:10508–13
    [Google Scholar]
  110. 110.  Simha RA, Ramaswamy S 2002. Hydrodynamic fluctuations and instabilities in ordered suspensions of self-propelled particles. Phys. Rev. Lett. 89:058101
    [Google Scholar]
  111. 111.  Skoufias DA, DeBonis S, Saoudi Y, Lebeau L, Crevel I et al. 2006. S-Trityl-l-cysteine is a reversible, tight binding inhibitor of the human kinesin Eg5 that specifically blocks mitotic progression. J. Biol. Chem. 281:17559–69
    [Google Scholar]
  112. 112.  Surrey T, Nédélec F, Leibler S, Karsenti E 2001. Physical properties determining self-organization of motors and microtubules. Science 292:1167–71
    [Google Scholar]
  113. 113.  Szent-Györgyi A. 1943. Observations on actomyosin. Stud. Inst. Med. Chem. Univ. Szeged 3:86–92
    [Google Scholar]
  114. 114.  Takagi J, Itabashi T, Suzuki K, Shimamoto Y, Kapoor TM, Ishiwata S 2014. Micromechanics of the vertebrate meiotic spindle examined by stretching along the pole-to-pole axis. Biophys. J. 106:735–40
    [Google Scholar]
  115. 115.  Tanaka F, Edwards SF 1992. Viscoelastic properties of physically cross-linked networks. 1. Transient network theory. Macromolecules 25:1516–23
    [Google Scholar]
  116. 116.  Tirnauer JS, Salmon ED, Mitchison TJ 2004. Microtubule plus-end dynamics in Xenopus egg extract spindles. Mol. Biol. Cell 15:1776–84
    [Google Scholar]
  117. 117.  Tólic-Nørrelykke IM. 2008. Push-me-pull-you: how microtubules organize the cell interior. Eur. Biophys. J. 37:1271–78
    [Google Scholar]
  118. 118.  Tólic-Nørrelykke IM, Sacconi L, Thon G, Pavone FS 2004. Positioning and elongation of the fission yeast spindle by microtubule-based pushing. Curr. Biol. 14:1181–86
    [Google Scholar]
  119. 119.  Uteng M, Hentrich C, Miura K, Bieling P, Surrey T 2008. Poleward transport of Eg5 by dynein-dynactin in Xenopus laevis egg extract spindles. J. Cell Biol. 182:715–26
    [Google Scholar]
  120. 120.  Valentine MT, Fordyce PM, Krzysiak TC, Gilbert SP, Block SM 2006. Individual dimers of the mitotic kinesin motor Eg5 step processively and support substantial loads in vitro. Nat. Cell Biol. 8:470–76
    [Google Scholar]
  121. 121.  Valentine MT, Perlman ZE, Mitchison TJ, Weitz DA 2005. Mechanical properties of Xenopus egg extract cytoplasmic extracts. Biophys. J. 88:680–89
    [Google Scholar]
  122. 122.  Verde F, Berrez JM, Antony C, Karsenti E 1991. Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein. J. Cell Biol. 112:1177–87
    [Google Scholar]
  123. 123.  Verde F, Dogterom M, Stelzer E, Karsenti E, Leibler S 1992. Control of microtubule dynamics and length by cyclin A– and cyclin B–dependent kinases in Xenopus egg extracts. J. Cell Biol. 118:1097–108
    [Google Scholar]
  124. 124.  Walczak CE, Cai S, Khodjakov A 2010. Mechanisms of chromosome behaviour during mitosis. Nat. Rev. Mol. Cell Biol. 11:91–102
    [Google Scholar]
  125. 125.  Waterman-Storer C, Desai A, Salmon ED 1999. Fluorescent speckle microscopy of spindle microtubule assembly and motility in living cells. Meth. Cell Biol. 61:155–73
    [Google Scholar]
  126. 126.  Weisenberg R, Cianci C 1984. ATP-induced gelation-contraction of microtubules assembled in vitro. J. Cell Biol. 99:1527–33
    [Google Scholar]
  127. 127.  Wu HY, Nazockdast E, Shelley MJ, Needleman JD 2016. Forces positioning the mitotic spindle: theories, and now experiments. BioEssays 39:1600212
    [Google Scholar]
  128. 128.  Wühr M, Dumont S, Groen AC, Needleman DJ, Mitchison TJ 2009. How does a millimiter-sized cell find its center. ? Cell Cycle 8:1115–21
    [Google Scholar]
  129. 129.  Wühr M, Freeman RMJ, Presler M, Horb ME, Peshkin L et al. 2014. Deep proteomics of the Xenopus laevis egg using an mRNA-derived reference database. Curr. Biol. 24:1467–75
    [Google Scholar]
  130. 130.  Yu CH, Langowitz N, Wu HY, Farhadifar R, Brugués J et al. 2014. Measuring microtubule polarity in spindles with second-harmonic generation. Biophys. J. 106:1578–87
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-060414-034107
Loading
/content/journals/10.1146/annurev-biophys-060414-034107
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error