Shaping up to divide: Coordinating actin and microtubule cytoskeletal remodelling during mitosis

Seminars in Cell and Developmental Biology

Volumn 34, Issue , 2014, Pages 109-115

  Lancaster, Oscar M ^a   Baum, Buzz ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Actin; Cell shape; Cortex; Mitosis; Spindle; Spindle formation; Spindle positioning

Indexed keywords

ACTIN;

ACTIN FILAMENT; CELL FUNCTION; CELL SEPARATION; CELL SHAPE; CENTROSOME; CHROMOSOME SEGREGATION; MEIOTIC SPINDLE; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; MORPHOGENESIS; NONHUMAN; PROTEIN FUNCTION; REVIEW; SPINDLE POSITIONING; ANIMAL; CELL DIVISION; HUMAN; METABOLISM; PROTEIN MULTIMERIZATION; SPINDLE APPARATUS;

ACTIN CYTOSKELETON; ANIMALS; CELL DIVISION; CELL SHAPE; CHROMOSOME SEGREGATION; HUMANS; MICROTUBULES; MITOSIS; PROTEIN MULTIMERIZATION; SPINDLE APPARATUS;

EID: 84914167004     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2014.02.015     Document Type: Review

References (101)

1. Niethammer P, Kronja I, Kandels-Lewis S, Rybina S, Bastiaens P, Karsenti E. Discrete states of a protein interaction network govern interphase and mitotic microtubule dynamics. PLoS Biology 2007, 5(2):e29.
2. Walczak C.E., Heald R. Mechanisms of mitotic spindle assembly and function. International Review of Cytology 2008, 265:111-158.
3. Vladimirou E., McHedlishvili N., Gasic I., Armond J.W., Samora C.P., Meraldi P., et al. Nonautonomous movement of chromosomes in mitosis. Developmental Cell 2013, 27(1):60-71.
4. Lara-Gonzalez P., Westhorpe F.G., Taylor S.S. The spindle assembly checkpoint. Current Biology 2012, 22(22):R966-R980.
5. Heald R., Tournebize R., Blank T., Sandaltzopoulos R., Becker P., Hyman A., et al. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 1996, 382(6590):420-425.
6. Fededa J.P., Gerlich D.W. Molecular control of animal cell cytokinesis. Nature Cell Biology 2012, 14(5):440-447.
7. Sedzinski J., Biro M., Oswald A., Tinevez J.Y., Salbreux G., Paluch E. Polar actomyosin contractility destabilizes the position of the cytokinetic furrow. Nature 2011, 476(7361):462-466.
8. Kunda P., Rodrigues N.T., Moeendarbary E., Liu T., Ivetic A., Charras G., et al. PP1-mediated moesin dephosphorylation couples polar relaxation to mitotic exit. Current Biology 2012, 22(3):231-236.
9. Kiyomitsu T., Cheeseman I.M. Cortical dynein and asymmetric membrane elongation coordinately position the spindle in anaphase. Cell 2013, 154(2):391-402.
10. Simon G.C., Prekeris R. The role of FIP3-dependent endosome transport during cytokinesis. Communicative and Integrative Biology 2008, 1(2):132-133.
11. Guizetti J., Gerlich D.W. Cytokinetic abscission in animal cells. Seminars in Cell and Developmental Biology 2010, 21(9):909-916.
12. Kunda P., Baum B. The actin cytoskeleton in spindle assembly and positioning. Trends in Cell Biology 2009, 19(4):174-179.
13. Wheeler R.J., Gluenz E., Gull K. The cell cycle of Leishmania: morphogenetic events and their implications for parasite biology. Molecular Microbiology 2011, 79(3):647-662.
14. Luxenburg C., Pasolli H.A., Williams S.E., Fuchs E. Developmental roles for Srf: cortical cytoskeleton and cell shape in epidermal spindle orientation. Nature Cell Biology 2011, 13(3):203-214.
15. Gibson W.T., Veldhuis J.H., Rubinstein B., Cartwright H.N., Perrimon N., Brodland G.W., et al. Control of the mitotic cleavage plane by local epithelial topology. Cell 2011, 144(3):427-438.
16. Matthews H.K., Baum B. The metastatic cancer cell cortex: an adaptation to enhance robust cell division in novel environments?. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 2012, 34(12):1017-1020.
17. Stewart M.P., Helenius J., Toyoda Y., Ramanathan S.P., Muller D.J., Hyman A.A. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 2011, 469(7329):226-230.
18. Matthews H.K., Delabre U., Rohn J.L., Guck J., Kunda P., Baum B. Changes in Ect2 localization couple actomyosin-dependent cell shape changes to mitotic progression. Developmental Cell 2012, 23(2):371-383.
19. Lancaster O.M., Le Berre M., Dimitracopoulos A., Bonazzi D., Zlotek-Zlotkiewicz E., Picone R., et al. Mitotic rounding alters cell geometry to ensure efficient bipolar spindle formation. Developmental Cell 2013, 25(3):270-283.
20. Atilla-Gokcumen G.E., Castoreno A.B., Sasse S., Eggert U.S. Making the cut: the chemical biology of cytokinesis. ACS Chemical Biology 2010, 5(1):79-90.
21. Cramer L.P., Mitchison T.J. Investigation of the mechanism of retraction of the cell margin and rearward flow of nodules during mitotic cell rounding. Molecular Biology of the Cell 1997, 8(1):109-119.
22. Maddox A.S., Burridge K. RhoA is required for cortical retraction and rigidity during mitotic cell rounding. Journal of Cell Biology 2003, 160(2):255-265.
23. Mitchison T.J. Actin based motility on retraction fibers in mitotic PtK2 cells. Cell Motility and the Cytoskeleton 1992, 22(2):135-151.
24. Dao V.T., Dupuy A.G., Gavet O., Caron E., de Gunzburg J. Dynamic changes in Rap1 activity are required for cell retraction and spreading during mitosis. Journal of Cell Science 2009, 122(Pt 16):2996-3004.
25. Harris A. Location of cellular adhesions to solid substrata. Developmental Biology 1973, 35(1):97-114.
26. Thery M., Racine V., Pepin A., Piel M., Chen Y., Sibarita J.B., et al. The extracellular matrix guides the orientation of the cell division axis. Nature Cell Biology 2005, 7(10):947-953.
27. Kunda P., Pelling A.E., Liu T., Baum B. Moesin controls cortical rigidity: cell rounding, and spindle morphogenesis during mitosis. Current Biology 2008, 18(2):91-101.
28. Fehon R.G., McClatchey A.I., Bretscher A. Organizing the cell cortex: the role of ERM proteins. Nature Reviews Molecular Cell Biology 2010, 11(4):276-287.
29. Thery M., Jimenez-Dalmaroni A., Racine V., Bornens M., Julicher F. Experimental and theoretical study of mitotic spindle orientation. Nature 2007, 447(7143):493-496.
30. Fujibuchi T., Abe Y., Takeuchi T., Imai Y., Kamei Y., Murase R., et al. AIP1/WDR1 supports mitotic cell rounding. Biochemical and Biophysical Research Communications 2005, 327(1):268-275.
31. Kaji N., Muramoto A., Mizuno K. LIM kinase-mediated cofilin phosphorylation during mitosis is required for precise spindle positioning. Journal of Biological Chemistry 2008, 283(8):4983-4992.
32. Clark A.G., Dierkes K., Paluch E.K. Monitoring actin cortex thickness in live cells. Biophysical Journal 2013, 105(3):570-580.
33. Carreno S., Kouranti I., Glusman E.S., Fuller M.T., Echard A., Payre F. Moesin and its activating kinase Slik are required for cortical stability and microtubule organization in mitotic cells. Journal of Cell Biology 2008, 180(4):739-746.
34. Kondo T., Hayashi S. Mitotic cell rounding accelerates epithelial invagination. Nature 2013, 494(7435):125-129.
35. Sandquist J.C., Kita A.M., Bement W.M. And the dead shall rise: actin and myosin return to the spindle. Developmental Cell 2011, 21(3):410-419.
36. Moulding D.A., Blundell M.P., Spiller D.G., White M.R., Cory G.O., Calle Y., et al. Unregulated actin polymerization by WASp causes defects of mitosis and cytokinesis in X-linked neutropenia. Journal of Experimental Medicine 2007, 204(9):2213-2224.
37. Moulding D.A., Moeendarbary E., Valon L., Record J., Charras G.T., Thrasher A.J. Excess F-actin mechanically impedes mitosis leading to cytokinesis failure in X-linked neutropenia by exceeding Aurora B kinase error correction capacity. Blood 2012, 120(18):3803-3811.
38. Robinson R.W., Snyder J.A. Localization of myosin II to chromosome arms and spindle fibers in PtK1 cells: a possible role for an actomyosin system in mitosis. Protoplasma 2005, 225(1/2):113-122.
39. Fabian L., Forer A. Redundant mechanisms for anaphase chromosome movements: crane-fly spermatocyte spindles normally use actin filaments but also can function without them. Protoplasma 2005, 225(3/4):169-184.
40. Woolner S., O'Brien L.L., Wiese C., Bement W.M. Myosin-10 and actin filaments are essential for mitotic spindle function. Journal of Cell Biology 2008, 182(1):77-88.
41. Vilmos P., Jankovics F., Szathmari M., Lukacsovich T., Henn L., Erdelyi M. Live imaging reveals that the Drosophila actin-binding ERM protein: moesin, co-localizes with the mitotic spindle. European Journal of Cell Biology 2009, 88(10):609-619.
42. Tse H.T., Weaver W.M., Di Carlo D. Increased asymmetric and multi-daughter cell division in mechanically confined microenvironments. PLoS ONE 2012, 7(6):e38986.
43. Dumont S., Mitchison T.J. Compression regulates mitotic spindle length by a mechanochemical switch at the poles. Current Biology 2009, 19(13):1086-1095.
44. Dinarina A., Pugieux C., Corral M.M., Loose M., Spatz J., Karsenti E., et al. Chromatin shapes the mitotic spindle. Cell 2009, 138(3):502-513.
45. Toyoshima F., Nishida E. Integrin-mediated adhesion orients the spindle parallel to the substratum in an EB1- and myosin X-dependent manner. EMBO Journal 2007, 26(6):1487-1498.
46. Morin X., Bellaiche Y. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Developmental Cell 2011, 21(1):102-119.
47. Whitehead C.M., Winkfein R.J., Rattner J.B. The relationship of HsEg5 and the actin cytoskeleton to centrosome separation. Cell Motility and the Cytoskeleton 1996, 35(4):298-308.
48. Whitehead C.M., Rattner J.B. Expanding the role of HsEg5 within the mitotic and post-mitotic phases of the cell cycle. Journal of Cell Science 1998, 111(Pt 17):2551-2561.
49. Tanenbaum M.E., Macurek L., Galjart N., Medema R.H. Dynein: Lis1 and CLIP-170 counteract Eg5-dependent centrosome separation during bipolar spindle assembly. EMBO Journal 2008, 27(24):3235-3245.
50. Raaijmakers J.A., van Heesbeen R.G., Meaders J.L., Geers E.F., Fernandez-Garcia B., Medema R.H., et al. Nuclear envelope-associated dynein drives prophase centrosome separation and enables Eg5-independent bipolar spindle formation. EMBO Journal 2012, 31(21):4179-4190.
51. Toso A., Winter J.R., Garrod A.J., Amaro A.C., Meraldi P., McAinsh A.D. Kinetochore-generated pushing forces separate centrosomes during bipolar spindle assembly. Journal of Cell Biology 2009, 184(3):365-372.
52. McHedlishvili N., Wieser S., Holtackers R., Mouysset J., Belwal M., Amaro A.C., et al. Kinetochores accelerate centrosome separation to ensure faithful chromosome segregation. Journal of Cell Science 2012, 125(Pt 4):906-918.
53. Tanenbaum M.E., Medema R.H. Mechanisms of centrosome separation and bipolar spindle assembly. Developmental Cell 2010, 19(6):797-806.
54. Rosenblatt J., Cramer L.P., Baum B., McGee K.M. Myosin II-dependent cortical movement is required for centrosome separation and positioning during mitotic spindle assembly. Cell 2004, 117(3):361-372.
55. Uzbekov R., Kireyev I., Prigent C. Centrosome separation: respective role of microtubules and actin filaments. Biology of the Cell 2002, 94(4/5):275-288.
56. Wang W, Chen L, Ding Y, Jin J, Liao K. Centrosome separation driven by actin-microfilaments during mitosis is mediated by centrosome-associated tyrosine-phosphorylated cortactin. Journal of Cell Science 2008, 121(Pt 8):1334-1343.
57. Silkworth W.T., Nardi I.K., Paul R., Mogilner A., Cimini D. Timing of centrosome separation is important for accurate chromosome segregation. Molecular Biology of the Cell 2012, 23(3):401-411.
58. Kaseda K., McAinsh A.D., Cross R.A. Dual pathway spindle assembly increases both the speed and the fidelity of mitosis. Biology Open 2012, 1(1):12-18.
59. Cao J., Crest J., Fasulo B., Sullivan W. Cortical actin dynamics facilitate early-stage centrosome separation. Current Biology 2010, 20(8):770-776.
60. Basto R., Lau J., Vinogradova T., Gardiol A., Woods C.G., Khodjakov A., et al. Flies without centrioles. Cell 2006, 125(7):1375-1386.
61. Khodjakov A., Cole R.W., Oakley B.R., Rieder C.L. Centrosome-independent mitotic spindle formation in vertebrates. Current Biology 2000, 10(2):59-67.
62. Rappaport R., Rappaport B.N. Establishment of cleavage furrows by the mitotic spindle. Journal of Experimental Zoology 1974, 189(2):189-196.
63. Siller K.H., Doe C.Q. Spindle orientation during asymmetric cell division. Nature Cell Biology 2009, 11(4):365-374.
64. Lu M.S., Johnston C.A. Molecular pathways regulating mitotic spindle orientation in animal cells. Development 2013, 140(9):1843-1856.
65. Kiyomitsu T., Cheeseman I.M. Chromosome- and spindle-pole-derived signals generate an intrinsic code for spindle position and orientation. Nature Cell Biology 2012, 14(3):311-317.
66. Woodard G.E., Huang N.N., Cho H., Miki T., Tall G.G., Kehrl J.H. Ric-8A and Gi alpha recruit LGN: NuMA, and dynein to the cell cortex to help orient the mitotic spindle. Molecular and Cellular Biology 2010, 30(14):3519-3530.
67. Kotak S., Busso C., Gonczy P. Cortical dynein is critical for proper spindle positioning in human cells. Journal of Cell Biology 2012, 199(1):97-110.
68. Dunsch A.K., Hammond D., Lloyd J., Schermelleh L., Gruneberg U., Barr F.A. Dynein light chain 1 and a spindle-associated adaptor promote dynein asymmetry and spindle orientation. Journal of Cell Biology 2012, 198(6):1039-1054.
69. Chaigne A., Verlhac M.H., Terret M.E. Spindle positioning in mammalian oocytes. Experimental Cell Research 2012, 318(12):1442-1447.
70. Longo F.J., Chen D.Y. Development of cortical polarity in mouse eggs: involvement of the meiotic apparatus. Developmental Biology 1985, 107(2):382-394.
71. Dumont J., Million K., Sunderland K., Rassinier P., Lim H., Leader B., et al. Formin-2 is required for spindle migration and for the late steps of cytokinesis in mouse oocytes. Developmental Biology 2007, 301(1):254-265.
72. Pfender S., Kuznetsov V., Pleiser S., Kerkhoff E., Schuh M. Spire-type actin nucleators cooperate with Formin-2 to drive asymmetric oocyte division. Current Biology 2011, 21(11):955-960.
73. Sun S.C., Wang Z.B., Xu Y.N., Lee S.E., Cui X.S., Kim N.H. Arp2/3 complex regulates asymmetric division and cytokinesis in mouse oocytes. PLoS ONE 2011, 6(4):e18392.
74. Schuh M., Ellenberg J. A new model for asymmetric spindle positioning in mouse oocytes. Current Biology 2008, 18(24):1986-1992.
75. Holubcova Z., Howard G., Schuh M. Vesicles modulate an actin network for asymmetric spindle positioning. Nature Cell Biology 2013, 15(8):937-947.
76. Chaigne A., Campillo C., Gov N.S., Voituriez R., Azoury J., Umana-Diaz C., et al. A soft cortex is essential for asymmetric spindle positioning in mouse oocytes. Nature Cell Biology 2013, 15(8):958-966.
77. Yi K., Rubinstein B., Unruh J.R., Guo F., Slaughter B.D., Li R. Sequential actin-based pushing forces drive meiosis I chromosome migration and symmetry breaking in oocytes. Journal of Cell Biology 2013, 200(5):567-576.
78. Field C.M., Lenart P. Bulk cytoplasmic actin and its functions in meiosis and mitosis. Current Biology 2011, 21(19):R825-R830.
79. Lenart P., Bacher C.P., Daigle N., Hand A.R., Eils R., Terasaki M., et al. A contractile nuclear actin network drives chromosome congression in oocytes. Nature 2005, 436(7052):812-818.
80. Zheng Z., Wan Q., Liu J., Zhu H., Chu X., Du Q. Evidence for dynein and astral microtubule-mediated cortical release and transport of Galphai/LGN/NuMA complex in mitotic cells. Molecular Biology of the Cell 2013, 24(7):901-913.
81. Heng Y.W., Lim H.H., Mina T., Utomo P., Zhong S., Lim C.T., et al. TPPP acts downstream of RhoA-ROCK-LIMK2 to regulate astral microtubule organization and spindle orientation. Journal of Cell Science 2012, 125(Pt 6):1579-1590.
82. Mitsushima M., Toyoshima F., Nishida E. Dual role of Cdc42 in spindle orientation control of adherent cells. Molecular and Cellular Biology 2009, 29(10):2816-2827.
83. Matsumura S., Hamasaki M., Yamamoto T., Ebisuya M., Sato M., Nishida E., et al. ABL1 regulates spindle orientation in adherent cells and mammalian skin. Nature Communications 2012, 3:626.
84. Toyoshima F., Matsumura S., Morimoto H., Mitsushima M., Nishida E. PtdIns(3,4,5)P3 regulates spindle orientation in adherent cells. Developmental Cell 2007, 13(6):796-811.
85. Maier B., Kirsch M., Anderhub S., Zentgraf H., Kramer A. The novel actin/focal adhesion-associated protein MISP is involved in mitotic spindle positioning in human cells. Cell Cycle 2013, 12(9):1457-1471.
86. Fink J., Carpi N., Betz T., Betard A., Chebah M., Azioune A., et al. External forces control mitotic spindle positioning. Nature Cell Biology 2011, 13(7):771-778.
87. Minc N., Burgess D., Chang F. Influence of cell geometry on division-plane positioning. Cell 2011, 144(3):414-426.
88. Mitsushima M., Aoki K., Ebisuya M., Matsumura S., Yamamoto T., Matsuda M., et al. Revolving movement of a dynamic cluster of actin filaments during mitosis. Journal of Cell Biology 2010, 191(3):453-462.
89. Gonczy P. Mechanisms of asymmetric cell division: flies and worms pave the way. Nature Reviews Molecular cell biology 2008, 9(5):355-366.
90. den Elzen N., Buttery C.V., Maddugoda M.P., Ren G., Yap A.S. Cadherin adhesion receptors orient the mitotic spindle during symmetric cell division in mammalian epithelia. Molecular Biology of the Cell 2009, 20(16):3740-3750.
91. Lu B., Roegiers F., Jan L.Y., Jan Y.N. Adherens junctions inhibit asymmetric division in the Drosophila epithelium. Nature 2001, 409(6819):522-525.
92. Fernandez-Minan A., Martin-Bermudo M.D., Gonzalez-Reyes A. Integrin signaling regulates spindle orientation in Drosophila to preserve the follicular-epithelium monolayer. Current Biology 2007, 17(8):683-688.
93. Nakajima Y., Meyer E.J., Kroesen A., McKinney S.A., Gibson M.C. Epithelial junctions maintain tissue architecture by directing planar spindle orientation. Nature 2013, 500(7462):359-362.
94. Woolner S., Papalopulu N. Spindle position in symmetric cell divisions during epiboly is controlled by opposing and dynamic apicobasal forces. Developmental Cell 2012, 22(4):775-787.
95. Meyer E.J., Ikmi A., Gibson M.C. Interkinetic nuclear migration is a broadly conserved feature of cell division in pseudostratified epithelia. Current Biology 2011, 21(6):485-491.
96. Rujano M.A., Sanchez-Pulido L., Pennetier C., le Dez G., Basto R. The microcephaly protein Asp regulates neuroepithelium morphogenesis by controlling the spatial distribution of myosin II. Nature Cell Biology 2013, 15(11):1294-1306.
97. Baena-Lopez L.A., Baonza A., Garcia-Bellido A. The orientation of cell divisions determines the shape of Drosophila organs. Current Biology 2005, 15(18):1640-1644.
98. Mao Y., Tournier A.L., Bates P.A., Gale J.E., Tapon N., Thompson B.J. Planar polarization of the atypical myosin Dachs orients cell divisions in Drosophila. Genes and Development 2011, 25(2):131-136.
99. Mao Y., Tournier A.L., Hoppe A., Kester L., Thompson B.J., Tapon N. Differential proliferation rates generate patterns of mechanical tension that orient tissue growth. EMBO Journal 2013, 32(21):2790-2803.
100. Kondylis V., van Nispen tot Pannerden H.E., Herpers B., Friggi-Grelin F., Rabouille C. The Golgi comprises a paired stack that is separated at G2 by modulation of the actin cytoskeleton through Abi and Scar/WAVE. Developmental Cell 2007, 12(6):901-915.
101. Fielding A.B., Royle S.J. Mitotic inhibition of clathrin-mediated endocytosis. Cellular and Molecular Life Sciences 2013, 70(18):3423-3433.