End-binding proteins and Ase1/PRC1 define local functionality of structurally distinct parts of the microtubule cytoskeleton

Trends in Cell Biology

Volumn 23, Issue 2, 2013, Pages 54-63

  Duellberg, Christian ^a   Fourniol, Franck J ^a   Maurer, Sebastian P ^a   Roostalu, Johanna ^a   Surrey, Thomas ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Antiparallel microtubules; EB1; Microtubule organization; Microtubule plus end tracking; Mitotic spindle

Indexed keywords

BINDING PROTEIN; MICROTUBULE PROTEIN; PRC1 PROTEIN; SPECTRIN; UNCLASSIFIED DRUG;

CYTOSKELETON; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; YEAST;

ANIMALS; CARRIER PROTEINS; CATHEPSIN A; CELL MOVEMENT; CELL POLARITY; CYTOSKELETON; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES POMBE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; YEASTS;

EUKARYOTA;

EID: 84872831129     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2012.10.003     Document Type: Review

References (124)

1. Mardin B.R., Schiebel E. Breaking the ties that bind: new advances in centrosome biology. J. Cell Biol. 2012, 197:11-18.
2. DeLuca J.G., Musacchio A. Structural organization of the kinetochore-microtubule interface. Curr. Opin. Cell Biol. 2012, 24:48-56.
3. Akhmanova A., Steinmetz M.O. Microtubule +TIPs at a glance. J. Cell Sci. 2010, 123:3415-3419.
4. Mata J., Nurse P. tea1 and the microtubular cytoskeleton are important for generating global spatial order within the fission yeast cell. Cell 1997, 89:939-949.
5. Carvalho P., et al. Surfing on microtubule ends. Trends Cell Biol. 2003, 13:229-237.
6. Galjart N. Plus-end-tracking proteins and their interactions at microtubule ends. Curr. Biol. 2010, 20:R528-R537.
7. Kumar P., Wittmann T. +TIPs: SxIPping along microtubule ends. Trends Cell Biol. 2012, 22:418-428.
8. Mimori-Kiyosue Y., et al. The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr. Biol. 2000, 10:865-868.
9. Glotzer M. The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat. Rev. Mol. Cell Biol. 2009, 10:9-20.
10. Bratman S.V., Chang F. Mechanisms for maintaining microtubule bundles. Trends Cell Biol. 2008, 18:580-586.
11. Su L.K., et al. APC binds to the novel protein EB1. Cancer Res. 1995, 55:2972-2977.
12. Tirnauer J.S., et al. Yeast Bim1p promotes the G1-specific dynamics of microtubules. J. Cell Biol. 1999, 145:993-1007.
13. Busch K.E., Brunner D. The microtubule plus end-tracking proteins mal3p and tip1p cooperate for cell-end targeting of interphase microtubules. Curr. Biol. 2004, 14:548-559.
14. Gierke S., Wittmann T. EB1-recruited microtubule +TIP complexes coordinate protrusion dynamics during 3D epithelial remodeling. Curr. Biol. 2012, 22:753-762.
15. Hale C.M., et al. SMRT analysis of MTOC and nuclear positioning reveals the role of EB1 and LIC1 in single-cell polarization. J. Cell Sci. 2011, 124:4267-4285.
16. Moughamian A.J., Holzbaur E.L. Dynactin is required for transport initiation from the distal axon. Neuron 2012, 74:331-343.
17. Mathur J., et al. A novel localization pattern for an EB1-like protein links microtubule dynamics to endomembrane organization. Curr. Biol. 2003, 13:1991-1997.
18. Nakagawa H., et al. EB3, a novel member of the EB1 family preferentially expressed in the central nervous system, binds to a CNS-specific APC homologue. Oncogene 2000, 19:210-216.
19. Bieling P., et al. CLIP-170 tracks growing microtubule ends by dynamically recognizing composite EB1/tubulin-binding sites. J. Cell Biol. 2008, 183:1223-1233.
20. Bieling P., et al. Reconstitution of a microtubule plus-end tracking system in vitro. Nature 2007, 450:1100-1105.
21. Dixit R., et al. Microtubule plus-end tracking by CLIP-170 requires EB1. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:492-497.
22. Zimniak T., et al. Phosphoregulation of the budding yeast EB1 homologue Bim1p by Aurora/Ipl1p. J. Cell Biol. 2009, 186:379-391.
23. Montenegro Gouveia S., et al. In vitro reconstitution of the functional interplay between MCAK and EB3 at microtubule plus ends. Curr. Biol. 2010, 20:1717-1722.
24. Hayashi I., Ikura M. Crystal structure of the amino-terminal microtubule-binding domain of end-binding protein 1 (EB1). J. Biol. Chem. 2003, 278:36430-36434.
25. Slep K.C., et al. Structural determinants for EB1-mediated recruitment of APC and spectraplakins to the microtubule plus end. J. Cell Biol. 2005, 168:587-598.
26. Honnappa S., et al. Structural insights into the EB1-APC interaction. EMBO J. 2005, 24:261-269.
27. Honnappa S., et al. An EB1-binding motif acts as a microtubule tip localization signal. Cell 2009, 138:366-376.
28. Askham J.M., et al. Evidence that an interaction between EB1 and p150(Glued) is required for the formation and maintenance of a radial microtubule array anchored at the centrosome. Mol. Biol. Cell 2002, 13:3627-3645.
29. Sjoblom B., et al. Novel structural insights into F-actin-binding and novel functions of calponin homology domains. Curr. Opin. Struct. Biol. 2008, 18:702-708.
30. Alushin G.M., et al. The Ndc80 kinetochore complex forms oligomeric arrays along microtubules. Nature 2010, 467:805-810.
31. Maurer S.P., et al. EBs recognize a nucleotide-dependent structural cap at growing microtubule ends. Cell 2012, 149:371-382.
32. des Georges, et al. Mal3, the Schizosaccharomyces pombe homolog of EB1, changes the microtubule lattice. Nat. Struct. Mol. Biol. 2008, 15:1102-1108.
33. Sandblad L., et al. The Schizosaccharomyces pombe EB1 homolog Mal3p binds and stabilizes the microtubule lattice seam. Cell 2006, 127:1415-1424.
34. Mizuno N., et al. Dynein and kinesin share an overlapping microtubule-binding site. EMBO J. 2004, 23:2459-2467.
35. Zanic M., et al. EB1 recognizes the nucleotide state of tubulin in the microtubule lattice. PLoS ONE 2009, 4:e7585.
36. Maurer S.P., et al. GTPgammaS microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs). Proc. Natl. Acad. Sci. U.S.A. 2011, 108:3988-3993.
37. Tirnauer J.S., et al. EB1 targets to kinetochores with attached, polymerizing microtubules. Mol. Biol. Cell 2002, 13:4308-4316.
38. Seetapun D., et al. Estimating the microtubule GTP cap size in vivo. Curr. Biol. 2012, 22:1681-1687.
39. Komarova Y., et al. Mammalian end binding proteins control persistent microtubule growth. J. Cell Biol. 2009, 184:691-706.
40. Vitre B., et al. EB1 regulates microtubule dynamics and tubulin sheet closure in vitro. Nat. Cell Biol. 2008, 10:415-421.
41. Katsuki M., et al. Mal3 masks catastrophe events in Schizosaccharomyces pombe microtubules by inhibiting shrinkage and promoting rescue. J. Biol. Chem. 2009, 284:29246-29250.
42. Kronja I., et al. XMAP215-EB1 interaction is required for proper spindle assembly and chromosome segregation in Xenopus egg extract. Mol. Biol. Cell 2009, 20:2684-2696.
43. Buey R.M., et al. Sequence determinants of a microtubule tip localization signal (MtLS). J. Biol. Chem. 2012, 287:28227-28242.
44. Steinmetz M.O., Akhmanova A. Capturing protein tails by CAP-Gly domains. Trends Biochem. Sci. 2008, 33:535-545.
45. Honnappa S., et al. Key interaction modes of dynamic +TIP networks. Mol. Cell 2006, 23:663-671.
46. Jaulin F., Kreitzer G. KIF17 stabilizes microtubules and contributes to epithelial morphogenesis by acting at MT plus ends with EB1 and APC. J. Cell Biol. 2010, 190:443-460.
47. Mattie F.J., et al. Directed microtubule growth, +TIPs, and kinesin-2 are required for uniform microtubule polarity in dendrites. Curr. Biol. 2010, 20:2169-2177.
48. Zhang J., et al. The microtubule plus-end localization of Aspergillus dynein is important for dynein-early-endosome interaction but not for dynein ATPase activation. J. Cell Sci. 2010, 123:3596-3604.
49. Browning H., et al. Tea2p is a kinesin-like protein required to generate polarized growth in fission yeast. J. Cell Biol. 2000, 151:15-28.
50. Dragestein K.A., et al. Dynamic behavior of GFP-CLIP-170 reveals fast protein turnover on microtubule plus ends. J. Cell Biol. 2008, 180:729-737.
51. Lansbergen G., et al. Conformational changes in CLIP-170 regulate its binding to microtubules and dynactin localization. J. Cell Biol. 2004, 166:1003-1014.
52. Wu X., et al. ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 2008, 135:137-148.
53. Fukata M., et al. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 2002, 109:873-885.
54. Watanabe T., et al. Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev. Cell 2004, 7:871-883.
55. Leung C.L., et al. Microtubule actin cross-linking factor (MACF): a hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons. J. Cell Biol. 1999, 147:1275-1286.
56. Lansbergen G., et al. CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5beta. Dev. Cell 2006, 11:21-32.
57. Mimori-Kiyosue, et al. CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J. Cell Biol. 2005, 168:141-153.
58. Ridley A.J., et al. Cell migration: integrating signals from front to back. Science 2003, 302:1704-1709.
59. Hayles J., Nurse P. A journey into space. Nat. Rev. Mol. Cell Biol. 2001, 2:647-656.
60. Moore J.K., Cooper J.A. Coordinating mitosis with cell polarity: molecular motors at the cell cortex. Semin. Cell Dev. Biol. 2010, 21:283-289.
61. Lomakin A.J., et al. CLIP-170-dependent capture of membrane organelles by microtubules initiates minus-end directed transport. Dev. Cell 2009, 17:323-333.
62. Pierre P., et al. CLIP-170 links endocytic vesicles to microtubules. Cell 1992, 70:887-900.
63. Watson P., et al. Coupling of ER exit to microtubules through direct interaction of COPII with dynactin. Nat. Cell Biol. 2005, 7:48-55.
64. Lloyd T.E., et al. The p150(Glued) CAP-Gly domain regulates initiation of retrograde transport at synaptic termini. Neuron 2012, 74:344-360.
65. Ban R., et al. Mitotic regulation of the stability of microtubule plus-end tracking protein EB3 by ubiquitin ligase SIAH-1 and Aurora mitotic kinases. J. Biol. Chem. 2009, 284:28367-28381.
66. Peth A., et al. Ubiquitin-dependent proteolysis of the microtubule end-binding protein 1, EB1, is controlled by the COP9 signalosome: possible consequences for microtubule filament stability. J. Mol. Biol. 2007, 368:550-563.
67. Schwartz K., et al. BIM1 encodes a microtubule-binding protein in yeast. Mol. Biol. Cell 1997, 8:2677-2691.
68. Rogers S.L., et al. Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J. Cell Biol. 2002, 158:873-884.
69. Lee H.S., et al. Phosphorylation controls autoinhibition of cytoplasmic linker protein-170. Mol. Biol. Cell 2010, 21:2661-2673.
70. Peris L., et al. Tubulin tyrosination is a major factor affecting the recruitment of CAP-Gly proteins at microtubule plus ends. J. Cell Biol. 2006, 174:839-849.
71. Jiang W., et al. PRC1: a human mitotic spindle-associated CDK substrate protein required for cytokinesis. Mol. Cell 1998, 2:877-885.
72. Smertenko A., et al. A new class of microtubule-associated proteins in plants. Nat. Cell Biol. 2000, 2:750-753.
73. Bieling P., et al. A minimal midzone protein module controls formation and length of antiparallel microtubule overlaps. Cell 2010, 142:420-432.
74. Gaillard J., et al. Two microtubule-associated proteins of Arabidopsis MAP65s promote antiparallel microtubule bundling. Mol. Biol. Cell 2008, 19:4534-4544.
75. Janson M.E., et al. Crosslinkers and motors organize dynamic microtubules to form stable bipolar arrays in fission yeast. Cell 2007, 128:357-368.
76. Kapitein L.C., et al. Microtubule-driven multimerization recruits ase1p onto overlapping microtubules. Curr. Biol. 2008, 18:1713-1717.
77. Pellman D., et al. Two microtubule-associated proteins required for anaphase spindle movement in Saccharomyces cerevisiae. J. Cell Biol. 1995, 130:1373-1385.
78. Subramanian R., et al. Insights into antiparallel microtubule crosslinking by PRC1, a conserved nonmotor microtubule binding protein. Cell 2010, 142:433-443.
79. Tulin A., et al. Single-molecule analysis of the microtubule cross-linking protein MAP65-1 reveals a molecular mechanism for contact-angle-dependent microtubule bundling. Biophys. J. 2012, 102:802-809.
80. Verbrugghe K.J., White J.G. SPD-1 is required for the formation of the spindle midzone but is not essential for the completion of cytokinesis in C. elegans embryos. Curr. Biol. 2004, 14:1755-1760.
81. Verni F., et al. Feo, the Drosophila homolog of PRC1, is required for central-spindle formation and cytokinesis. Curr. Biol. 2004, 14:1569-1575.
82. Roostalu J., et al. Cell cycle control of spindle elongation. Cell Cycle 2010, 9:1084-1090.
83. Kurasawa Y., et al. Essential roles of KIF4 and its binding partner PRC1 in organized central spindle midzone formation. EMBO J. 2004, 23:3237-3248.
84. Mollinari C., et al. PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J. Cell Biol. 2002, 157:1175-1186.
85. Schuyler S.C., et al. The molecular function of Ase1p: evidence for a MAP-dependent midzone-specific spindle matrix. Microtubule-associated proteins. J. Cell Biol. 2003, 160:517-528.
86. Sawin K.E., Tran T.P. Cytoplasmic microtubule organization in fission yeast. Yeast 2006, 23:1001-1014.
87. Van Damme D., et al. In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiol. 2004, 136:3956-3967.
88. Djinovic-Carugo K., et al. The spectrin repeat: a structural platform for cytoskeletal protein assemblies. FEBS Lett. 2002, 513:119-123.
89. Loiodice I., et al. Ase1p organizes antiparallel microtubule arrays during interphase and mitosis in fission yeast. Mol. Biol. Cell 2005, 16:1756-1768.
90. Smertenko A.P., et al. Control of the AtMAP65-1 interaction with microtubules through the cell cycle. J. Cell Sci. 2006, 119:3227-3237.
91. Ding R., et al. Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J. Cell Biol. 1993, 120:141-151.
92. Winey M., et al. Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle. J. Cell Biol. 1995, 129:1601-1615.
93. Mastronarde D.N., et al. Interpolar spindle microtubules in PTK cells. J. Cell Biol. 1993, 123:1475-1489.
94. McIntosh J.R., Landis S.C. The distribution of spindle microtubules during mitosis in cultured human cells. J. Cell Biol. 1971, 49:468-497.
95. Srayko M., et al. Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis. Curr. Biol. 2006, 16:1944-1949.
96. Kieserman E.K., et al. Developmental regulation of central spindle assembly and cytokinesis during vertebrate embryogenesis. Curr. Biol. 2008, 18:116-123.
97. Juang Y.L., et al. APC-mediated proteolysis of Ase1 and the morphogenesis of the mitotic spindle. Science 1997, 275:1311-1314.
98. Yamashita A., et al. The roles of fission yeast ase1 in mitotic cell division, meiotic nuclear oscillation, and cytokinesis checkpoint signaling. Mol. Biol. Cell 2005, 16:1378-1395.
99. Sullivan M., et al. Studies on substrate recognition by the budding yeast separase. J. Biol. Chem. 2004, 279:1191-1196.
100. Loog M., Morgan D.O. Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature 2005, 434:104-108.
101. Hu C.K., et al. Plk1 negatively regulates PRC1 to prevent premature midzone formation before cytokinesis. Mol. Biol. Cell 2012, 23:2702-2711.
102. Neef R., et al. Choice of Plk1 docking partners during mitosis and cytokinesis is controlled by the activation state of Cdk1. Nat. Cell Biol. 2007, 9:436-444.
103. Kotwaliwale C.V., et al. A pathway containing the Ipl1/aurora protein kinase and the spindle midzone protein Ase1 regulates yeast spindle assembly. Dev. Cell 2007, 13:433-445.
104. Khmelinskii A., et al. Phosphorylation-dependent protein interactions at the spindle midzone mediate cell cycle regulation of spindle elongation. Dev. Cell 2009, 17:244-256.
105. Fu C., Ward, et al. Phospho-regulated interaction between kinesin-6 Klp9p and microtubule bundler Ase1p promotes spindle elongation. Dev. Cell 2009, 17:257-267.
106. Sasabe M., et al. Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells. Genes Dev. 2006, 20:1004-1014.
107. Zhu C., et al. Spatiotemporal control of spindle midzone formation by PRC1 in human cells. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:6196-6201.
108. 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. U.S.A. 2005, 102:343-348.
109. Braun M., et al. Adaptive braking by Ase1 prevents overlapping microtubules from sliding completely apart. Nat. Cell Biol. 2011, 13:1259-1264.
110. Gruneberg U., et al. KIF14 and citron kinase act together to promote efficient cytokinesis. J. Cell Biol. 2006, 172:363-372.
111. Hu C.K., et al. KIF4 regulates midzone length during cytokinesis. Curr. Biol. 2011, 21:815-824.
112. Ho C.M., et al. Interaction of antiparallel microtubules in the phragmoplast is mediated by the microtubule-associated protein MAP65-3 in Arabidopsis. Plant Cell 2011, 23:2909-2923.
113. Dhonukshe P., et al. A PLETHORA-auxin transcription module controls cell division plane rotation through MAP65 and CLASP. Cell 2012, 149:383-396.
114. Khmelinskii A., et al. Cdc14-regulated midzone assembly controls anaphase B. J. Cell Biol. 2007, 177:981-993.
115. 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.
116. Friedman J.R., Voeltz G.K. The ER in 3D: a multifunctional dynamic membrane network. Trends Cell Biol. 2011, 21:709-717.
117. Paredez A.R., et al. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 2006, 312:1491-1495.
118. van der Vaart B., et al. SLAIN2 links microtubule plus end-tracking proteins and controls microtubule growth in interphase. J. Cell Biol. 2011, 193:1083-1099.
119. Akhmanova A., et al. Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 2001, 104:923-935.
120. Goshima G., et al. Mechanisms for focusing mitotic spindle poles by minus end-directed motor proteins. J. Cell Biol. 2005, 171:229-240.
121. Bratman S.V., Chang F. Stabilization of overlapping microtubules by fission yeast CLASP. Dev. Cell 2007, 13:812-827.
122. Kumar P., et al. GSK3beta phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J. Cell Biol. 2009, 184:895-908.
123. Andrews P.D., et al. Aurora B regulates MCAK at the mitotic centromere. Dev. Cell 2004, 6:253-268.
124. Weisbrich A., et al. Structure-function relationship of CAP-Gly domains. Nat. Struct. Mol. Biol. 2007, 14:959-967.