Building Complexity: Insights into Self-Organized Assembly of Microtubule-Based Architectures

Developmental Cell

Volumn 23, Issue 5, 2012, Pages 874-885

  Subramanian, Radhika ^a   Kapoor, Tarun M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASE1 PROTEIN; KINESIN; KINESIN 1; KINESIN 14; KINESIN 8; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MOLECULAR MOTOR; PRC1 PROTEIN; STATHMIN; TUBULIN; UNCLASSIFIED DRUG;

BINDING AFFINITY; CELL DIVISION; CELL GROWTH; CELL STRUCTURE; CELL TYPE; COMPLEX FORMATION; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; CYTOSKELETON; DEPOLYMERIZATION; EUKARYOTE; HUMAN; MICROTUBULE; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; REVIEW;

ANIMALS; CYTOSKELETON; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MODELS, BIOLOGICAL; MOLECULAR MOTOR PROTEINS; PROTEIN MULTIMERIZATION;

EID: 84869050723     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.10.011     Document Type: Review

References (112)

1. Adams D.W., Errington J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat. Rev. Microbiol. 2009, 7:642-653.
2. Akhmanova A., Hoogenraad C.C., Drabek K., Stepanova T., Dortland B., Verkerk T., Vermeulen W., Burgering B.M., De Zeeuw C.I., Grosveld F., Galjart N. Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 2001, 104:923-935.
3. Al-Bassam J., Chang F. Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol. 2011, 21:604-614.
4. Al-Bassam J., Kim H., Brouhard G., van Oijen A., Harrison S.C., Chang F. CLASP promotes microtubule rescue by recruiting tubulin dimers to the microtubule. Dev. Cell 2010, 19:245-258.
5. Ayaz P., Ye X., Huddleston P., Brautigam C.A., Rice L.M. A TOG:αβ-tubulin complex structure reveals conformation-based mechanisms for a microtubule polymerase. Science 2012, 337:857-860.
6. Belmont L., Mitchison T., Deacon H.W. Catastrophic revelations about Op18/stathmin. Trends Biochem. Sci. 1996, 21:197-198.
7. Bieling P., Telley I.A., Surrey T. A minimal midzone protein module controls formation and length of antiparallel microtubule overlaps. Cell 2010, 142:420-432.
8. Bormuth V., Varga V., Howard J., Schäffer E. Protein friction limits diffusive and directed movements of kinesin motors on microtubules. Science 2009, 325:870-873.
9. Bratman S.V., Chang F. Mechanisms for maintaining microtubule bundles. Trends Cell Biol. 2008, 18:580-586.
10. 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.
11. Braun M., Lansky Z., Fink G., Ruhnow F., Diez S., Janson M.E. Adaptive braking by Ase1 prevents overlapping microtubules from sliding completely apart. Nat. Cell Biol. 2011, 13:1259-1264.
12. Brouhard G.J., Stear J.H., Noetzel T.L., Al-Bassam J., Kinoshita K., Harrison S.C., Howard J., Hyman A.A. XMAP215 is a processive microtubule polymerase. Cell 2008, 132:79-88.
13. Cabeen M.T., Jacobs-Wagner C. The bacterial cytoskeleton. Annu. Rev. Genet. 2010, 44:365-392.
14. Carazo-Salas R.E., Nurse P. Self-organization of interphase microtubule arrays in fission yeast. Nat. Cell Biol. 2006, 8:1102-1107.
15. Cassimeris L. The oncoprotein 18/stathmin family of microtubule destabilizers. Curr. Opin. Cell Biol. 2002, 14:18-24.
16. Chen J., Kanai Y., Cowan N.J., Hirokawa N. Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 1992, 360:674-677.
17. Civelekoglu-Scholey G., Tao L., Brust-Mascher I., Wollman R., Scholey J.M. Prometaphase spindle maintenance by an antagonistic motor-dependent force balance made robust by a disassembling lamin-B envelope. J. Cell Biol. 2010, 188:49-68.
18. Conde C., Cáceres A. Microtubule assembly, organization and dynamics in axons and dendrites. Nat. Rev. Neurosci. 2009, 10:319-332.
19. Davis L., Chin J.W. Designer proteins: applications of genetic code expansion in cell biology. Nat. Rev. Mol. Cell Biol. 2012, 13:168-182.
20. Desai A., Mitchison T.J. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 1997, 13:83-117.
21. Desai A., Verma S., Mitchison T.J., Walczak C.E. Kin I kinesins are microtubule-destabilizing enzymes. Cell 1999, 96:69-78.
22. Drummond D.R., Kain S., Newcombe A., Hoey C., Katsuki M., Cross R.A. Purification of tubulin from the fission yeast Schizosaccharomyces pombe. Methods Mol. Biol. 2011, 777:29-55.
23. Erickson H.P., Anderson D.E., Osawa M. FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol. Mol. Biol. Rev. 2010, 74:504-528.
24. 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.
25. Foley T.L., Burkart M.D. Site-specific protein modification: advances and applications. Curr. Opin. Chem. Biol. 2007, 11:12-19.
26. Fu C., Ward J.J., Loiodice I., Velve-Casquillas G., Nedelec F.J., Tran P.T. Phospho-regulated interaction between kinesin-6 Klp9p and microtubule bundler Ase1p promotes spindle elongation. Dev. Cell 2009, 17:257-267.
27. Fukata Y., Itoh T.J., Kimura T., Ménager C., Nishimura T., Shiromizu T., Watanabe H., Inagaki N., Iwamatsu A., Hotani H., Kaibuchi K. CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 2002, 4:583-591.
28. Gaglio T., Saredi A., Compton D.A. NuMA is required for the organization of microtubules into aster-like mitotic arrays. J. Cell Biol. 1995, 131:693-708.
29. Gaglio T., Saredi A., Bingham J.B., Hasbani M.J., Gill S.R., Schroer T.A., Compton D.A. Opposing motor activities are required for the organization of the mammalian mitotic spindle pole. J. Cell Biol. 1996, 135:399-414.
30. Gaillard J., Neumann E., Van Damme D., Stoppin-Mellet V., Ebel C., Barbier E., Geelen D., Vantard M. Two microtubule-associated proteins of Arabidopsis MAP65s promote antiparallel microtubule bundling. Mol. Biol. Cell 2008, 19:4534-4544.
31. Gardner M.K., Odde D.J., Bloom K. Kinesin-8 molecular motors: putting the brakes on chromosome oscillations. Trends Cell Biol. 2008, 18:307-310.
32. Gardner M.K., Zanic M., Gell C., Bormuth V., Howard J. Depolymerizing kinesins Kip3 and MCAK shape cellular microtubule architecture by differential control of catastrophe. Cell 2011, 147:1092-1103.
33. Garner E.C., Campbell C.S., Mullins R.D. Dynamic instability in a DNA-segregating prokaryotic actin homolog. Science 2004, 306:1021-1025.
34. Garner E.C., Campbell C.S., Weibel D.B., Mullins R.D. Reconstitution of DNA segregation driven by assembly of a prokaryotic actin homolog. Science 2007, 315:1270-1274.
35. Gerdes K., Howard M., Szardenings F. Pushing and pulling in prokaryotic DNA segregation. Cell 2010, 141:927-942.
36. Gigant B., Curmi P.A., Martin-Barbey C., Charbaut E., Lachkar S., Lebeau L., Siavoshian S., Sobel A., Knossow M. The 4 å X-ray structure of a tubulin:stathmin-like domain complex. Cell 2000, 102:809-816.
37. Gittes F., Mickey B., Nettleton J., Howard J. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 1993, 120:923-934.
38. Glotzer M. The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat. Rev. Mol. Cell Biol. 2009, 10:9-20.
39. Goodwin S.S., Vale R.D. Patronin regulates the microtubule network by protecting microtubule minus ends. Cell 2010, 143:263-274.
40. Gruneberg U., Neef R., Li X., Chan E.H., Chalamalasetty R.B., Nigg E.A., Barr F.A. KIF14 and citron kinase act together to promote efficient cytokinesis. J. Cell Biol. 2006, 172:363-372.
41. Gueiros-Filho F.J., Losick R. A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev. 2002, 16:2544-2556.
42. Gupta M.L., Carvalho P., Roof D.M., Pellman D. Plus end-specific depolymerase activity of Kip3, a kinesin-8 protein, explains its role in positioning the yeast mitotic spindle. Nat. Cell Biol. 2006, 8:913-923.
43. Helenius J., Brouhard G., Kalaidzidis Y., Diez S., Howard J. The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends. Nature 2006, 441:115-119.
44. Hentrich C., Surrey T. Microtubule organization by the antagonistic mitotic motors kinesin-5 and kinesin-14. J. Cell Biol. 2010, 189:465-480.
45. Howard J., Hyman A.A. Growth, fluctuation and switching at microtubule plus ends. Nat. Rev. Mol. Cell Biol. 2009, 10:569-574.
46. Hu C.K., Coughlin M., Field C.M., Mitchison T.J. KIF4 regulates midzone length during cytokinesis. Curr. Biol. 2011, 21:815-824.
47. Hu C.K., Ozlü N., Coughlin M., Steen J.J., Mitchison T.J. Plk1 negatively regulates PRC1 to prevent premature midzone formation before cytokinesis. Mol. Biol. Cell 2012, 23:2702-2711.
48. Hunter A.W., Caplow M., Coy D.L., Hancock W.O., Diez S., Wordeman L., Howard J. The kinesin-related protein MCAK is a microtubule depolymerase that forms an ATP-hydrolyzing complex at microtubule ends. Mol. Cell 2003, 11:445-457.
49. Hyman A.A., Chrétien D., Arnal I., Wade R.H. Structural changes accompanying GTP hydrolysis in microtubules: information from a slowly hydrolyzable analogue guanylyl-(α,β)-methylene-diphosphonate. J. Cell Biol. 1995, 128:117-125.
50. Ishikawa H., Marshall W.F. Ciliogenesis: building the cell's antenna. Nat. Rev. Mol. Cell Biol. 2011, 12:222-234.
51. Janke C., Bulinski J.C. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 2011, 12:773-786.
52. Janson M.E., Loughlin R., Loïodice I., Fu C., Brunner D., Nédélec F.J., Tran P.T. Crosslinkers and motors organize dynamic microtubules to form stable bipolar arrays in fission yeast. Cell 2007, 128:357-368.
53. Johnson V., Ayaz P., Huddleston P., Rice L.M. Design, overexpression, and purification of polymerization-blocked yeast αβ-tubulin mutants. Biochemistry 2011, 50:8636-8644.
54. Kapitein L.C., Peterman E.J., 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.
55. Kapitein L.C., Janson M.E., van den Wildenberg S.M., Hoogenraad C.C., Schmidt C.F., Peterman E.J. Microtubule-driven multimerization recruits ase1p onto overlapping microtubules. Curr. Biol. 2008, 18:1713-1717.
56. 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.
57. Kaverina I., Straube A. Regulation of cell migration by dynamic microtubules. Semin. Cell Dev. Biol. 2011, 22:968-974.
58. Khmelinskii A., Roostalu J., Roque H., Antony C., Schiebel E. Phosphorylation-dependent protein interactions at the spindle midzone mediate cell cycle regulation of spindle elongation. Dev. Cell 2009, 17:244-256.
59. Kimura T., Watanabe H., Iwamatsu A., Kaibuchi K. Tubulin and CRMP-2 complex is transported via Kinesin-1. J. Neurochem. 2005, 93:1371-1382.
60. Kinoshita K., Arnal I., Desai A., Drechsel D.N., Hyman A.A. Reconstitution of physiological microtubule dynamics using purified components. Science 2001, 294:1340-1343.
61. Kirkpatrick C.L., Viollier P.H. New(s) to the (Z-)ring. Curr. Opin. Microbiol. 2011, 14:691-697.
62. Kollman J.M., Merdes A., Mourey L., Agard D.A. Microtubule nucleation by γ-tubulin complexes. Nat. Rev. Mol. Cell Biol. 2011, 12:709-721.
63. Kurasawa Y., Earnshaw W.C., Mochizuki Y., Dohmae N., Todokoro K. Essential roles of KIF4 and its binding partner PRC1 in organized central spindle midzone formation. EMBO J. 2004, 23:3237-3248.
64. Low H.H., Moncrieffe M.C., Löwe J. The crystal structure of ZapA and its modulation of FtsZ polymerisation. J. Mol. Biol. 2004, 341:839-852.
65. Löwe J., Li H., Downing K.H., Nogales E. Refined structure of αβ-tubulin at 3.5 å resolution. J. Mol. Biol. 2001, 313:1045-1057.
66. Lüders J., Stearns T. Microtubule-organizing centres: a re-evaluation. Nat. Rev. Mol. Cell Biol. 2007, 8:161-167.
67. Margolin W. Sculpting the bacterial cell. Curr. Biol. 2009, 19:R812-R822.
68. Matsubara I., Goldman Y.E., Simmons R.M. Changes in the lateral filament spacing of skinned muscle fibres when cross-bridges attach. J. Mol. Biol. 1984, 173:15-33.
69. Merdes A., Ramyar K., Vechio J.D., Cleveland D.W. A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell 1996, 87:447-458.
70. Merdes A., Heald R., Samejima K., Earnshaw W.C., Cleveland D.W. Formation of spindle poles by dynein/dynactin-dependent transport of NuMA. J. Cell Biol. 2000, 149:851-862.
71. Meunier S., Vernos I. K-fibre minus ends are stabilized by a RanGTP-dependent mechanism essential for functional spindle assembly. Nat. Cell Biol. 2011, 13:1406-1414.
72. Mimori-Kiyosue Y., Grigoriev I., Lansbergen G., Sasaki H., Matsui C., Severin F., Galjart N., Grosveld F., Vorobjev I., Tsukita S., Akhmanova A. CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J. Cell Biol. 2005, 168:141-153.
73. Mitchison T.J. Self-organization of polymer-motor systems in the cytoskeleton. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1992, 336:99-106.
74. Moores C.A., Yu M., Guo J., Beraud C., Sakowicz R., Milligan R.A. A mechanism for microtubule depolymerization by KinI kinesins. Mol. Cell 2002, 9:903-909.
75. Morris N.R. Nuclear positioning: the means is at the ends. Curr. Opin. Cell Biol. 2003, 15:54-59.
76. Nédélec F.J., Surrey T., Maggs A.C., Leibler S. Self-organization of microtubules and motors. Nature 1997, 389:305-308.
77. Nédélec F., Surrey T., Karsenti E. Self-organisation and forces in the microtubule cytoskeleton. Curr. Opin. Cell Biol. 2003, 15:118-124.
78. Neef R., Gruneberg U., Kopajtich R., Li X., Nigg E.A., Sillje H., Barr F.A. Choice of Plk1 docking partners during mitosis and cytokinesis is controlled by the activation state of Cdk1. Nat. Cell Biol. 2007, 9:436-444.
79. Peters C., Brejc K., Belmont L., Bodey A.J., Lee Y., Yu M., Guo J., Sakowicz R., Hartman J., Moores C.A. Insight into the molecular mechanism of the multitasking kinesin-8 motor. EMBO J. 2010, 29:3437-3447.
80. Peris L., Wagenbach M., Lafanechère L., Brocard J., Moore A.T., Kozielski F., Job D., Wordeman L., Andrieux A. Motor-dependent microtubule disassembly driven by tubulin tyrosination. J. Cell Biol. 2009, 185:1159-1166.
81. Peterman E.J., Scholey J.M. Mitotic microtubule crosslinkers: insights from mechanistic studies. Curr. Biol. 2009, 19:R1089-R1094.
82. Ravelli R.B., Gigant B., Curmi P.A., Jourdain I., Lachkar S., Sobel A., Knossow M. Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain. Nature 2004, 428:198-202.
83. Rey M., Sanchez-Madrid F., Valenzuela-Fernandez A. The role of actomyosin and the microtubular network in both the immunological synapse and T cell activation. Front. Biosci. 2007, 12:437-447.
84. Roll-Mecak A., McNally F.J. Microtubule-severing enzymes. Curr. Opin. Cell Biol. 2010, 22:96-103.
85. Salje J., Gayathri P., Löwe J. The ParMRC system: molecular mechanisms of plasmid segregation by actin-like filaments. Nat. Rev. Microbiol. 2010, 8:683-692.
86. Sekine Y., Okada Y., Noda Y., Kondo S., Aizawa H., Takemura R., Hirokawa N. A novel microtubule-based motor protein (KIF4) for organelle transports, whose expression is regulated developmentally. J. Cell Biol. 1994, 127:187-201.
87. Shaevitz J.W., Gitai Z. The structure and function of bacterial actin homologs. Cold Spring Harb. Perspect. Biol. 2010, 2:a000364.
88. Sharp D.J., Ross J.L. Microtubule-severing enzymes at the cutting edge. J. Cell Sci. 2012, 125:2561-2569.
89. Slep K.C., Vale R.D. Structural basis of microtubule plus end tracking by XMAP215, CLIP-170, and EB1. Mol. Cell 2007, 27:976-991.
90. Stenmark P., Ogg D., Flodin S., Flores A., Kotenyova T., Nyman T., Nordlund P., Kursula P. The structure of human collapsin response mediator protein 2, a regulator of axonal growth. J. Neurochem. 2007, 101:906-917.
91. Stiess M., Bradke F. Neuronal polarization: the cytoskeleton leads the way. Dev. Neurobiol. 2011, 71:430-444.
92. Su X., Qiu W., Gupta M.L., Pereira-Leal J.B., Reck-Peterson S.L., Pellman D. Mechanisms underlying the dual-mode regulation of microtubule dynamics by Kip3/kinesin-8. Mol. Cell 2011, 43:751-763.
93. Subramanian R., Wilson-Kubalek E.M., Arthur C.P., Bick M.J., Campbell E.A., Darst S.A., Milligan R.A., Kapoor T.M. Insights into antiparallel microtubule crosslinking by PRC1, a conserved nonmotor microtubule binding protein. Cell 2010, 142:433-443.
94. Surrey T., Nedelec F., Leibler S., Karsenti E. Physical properties determining self-organization of motors and microtubules. Science 2001, 292:1167-1171.
95. Svoboda K., Block S.M. Force and velocity measured for single kinesin molecules. Cell 1994, 77:773-784.
96. Tanenbaum M.E., Medema R.H. Mechanisms of centrosome separation and bipolar spindle assembly. Dev. Cell 2010, 19:797-806.
97. Tao L., Mogilner A., Civelekoglu-Scholey G., Wollman R., Evans J., Stahlberg H., Scholey J.M. A homotetrameric kinesin-5, KLP61F, bundles microtubules and antagonizes Ncd in motility assays. Curr. Biol. 2006, 16:2293-2302.
98. Tørring T., Voigt N.V., Nangreave J., Yan H., Gothelf K.V. DNA origami: a quantum leap for self-assembly of complex structures. Chem. Soc. Rev. 2011, 40:5636-5646.
99. Vale R.D. The molecular motor toolbox for intracellular transport. Cell 2003, 112:467-480.
100. Vale R.D., Malik F., Brown D. Directional instability of microtubule transport in the presence of kinesin and dynein, two opposite polarity motor proteins. J. Cell Biol. 1992, 119:1589-1596.
101. Valentine M.T., Fordyce P.M., Krzysiak T.C., Gilbert S.P., Block S.M. Individual dimers of the mitotic kinesin motor Eg5 step processively and support substantial loads in vitro. Nat. Cell Biol. 2006, 8:470-476.
102. Varga V., Helenius J., Tanaka K., Hyman A.A., Tanaka T.U., Howard J. Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner. Nat. Cell Biol. 2006, 8:957-962.
103. Varga V., Leduc C., Bormuth V., Diez S., Howard J. Kinesin-8 motors act cooperatively to mediate length-dependent microtubule depolymerization. Cell 2009, 138:1174-1183.
104. Verhey K.J., Gaertig J. The tubulin code. Cell Cycle 2007, 6:2152-2160.
105. Vila-Perelló M., Muir T.W. Biological applications of protein splicing. Cell 2010, 143:191-200.
106. Wasteneys G.O., Ambrose J.C. Spatial organization of plant cortical microtubules: close encounters of the 2D kind. Trends Cell Biol. 2009, 19:62-71.
107. Watanabe T., Noritake J., Kaibuchi K. Regulation of microtubules in cell migration. Trends Cell Biol. 2005, 15:76-83.
108. Widlund P.O., Stear J.H., Pozniakovsky A., Zanic M., Reber S., Brouhard G.J., Hyman A.A., Howard J. XMAP215 polymerase activity is built by combining multiple tubulin-binding TOG domains and a basic lattice-binding region. Proc. Natl. Acad. Sci. USA 2011, 108:2741-2746.
109. Wittmann T., Hyman A., Desai A. The spindle: a dynamic assembly of microtubules and motors. Nat. Cell Biol. 2001, 3:E28-E34.
110. Wordeman L. Microtubule-depolymerizing kinesins. Curr. Opin. Cell Biol. 2005, 17:82-88.
111. Wühr M., Dumont S., Groen A.C., Needleman D.J., Mitchison T.J. How does a millimeter-sized cell find its center?. Cell Cycle 2009, 8:1115-1121.
112. Zhu C., Jiang W. Cell cycle-dependent translocation of PRC1 on the spindle by Kif4 is essential for midzone formation and cytokinesis. Proc. Natl. Acad. Sci. USA 2005, 102:343-348.