+TIPs: SxIPping along microtubule ends

Trends in Cell Biology

Volumn 22, Issue 8, 2012, Pages 418-428

  Kumar, Praveen ^a   Wittmann, Torsten ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

+TIPs; EB1; Microtubule; Microtubule dynamics; Plus end tracking

Indexed keywords

APC PROTEIN; MICROTUBULE PROTEIN; PROTEIN TIP; UNCLASSIFIED DRUG;

HUMAN; HYDROPHOBICITY; IMMUNOFLUORESCENCE; MICROTUBULE; MICROTUBULE ASSEMBLY; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW;

AMINO ACID MOTIFS; ANIMALS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; PROTEIN BINDING;

EID: 84864319735     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2012.05.005     Document Type: Review

References (104)

1. Perez F., et al. CLIP-170 highlights growing microtubule ends in vivo. Cell 1999, 96:517-527.
2. 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.
3. Galjart N. Plus-end-tracking proteins and their interactions at microtubule ends. Curr. Biol. 2010, 20:R528-R537.
4. Akhmanova A., Steinmetz M.O. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 2008, 9:309-322.
5. Brouhard G.J., et al. XMAP215 is a processive microtubule polymerase. Cell 2008, 132:79-88.
6. Howard J., Hyman A.A. Microtubule polymerases and depolymerases. Curr. Opin. Cell Biol. 2007, 19:31-35.
7. Bieling P., et al. Reconstitution of a microtubule plus-end tracking system in vitro. Nature 2007, 450:1100-1105.
8. 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.
9. Komarova Y., et al. Mammalian end binding proteins control persistent microtubule growth. J. Cell Biol. 2009, 184:691-706.
10. Dixit R., et al. Microtubule plus-end tracking by CLIP-170 requires EB1. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:492-497.
11. Howard J., Hyman A.A. Growth, fluctuation and switching at microtubule plus ends. Nat. Rev. Mol. Cell Biol. 2009, 10:569-574.
12. Dimitrov A., et al. Detection of GTP-tubulin conformation in vivo reveals a role for GTP remnants in microtubule rescues. Science 2008, 322:1353-1356.
13. Zanic M., et al. EB1 recognizes the nucleotide state of tubulin in the microtubule lattice. PLoS ONE 2009, 4:e7585.
14. 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.
15. Maurer S.P., et al. EBs recognize a nucleotide-dependent structural cap at growing microtubule ends. Cell 2012, 149:371-382.
16. Wade R.H. On and around microtubules: an overview. Mol. Biotechnol. 2009, 43:177-191.
17. McIntosh J.R., et al. Lattice structure of cytoplasmic microtubules in a cultured Mammalian cell. J. Mol. Biol. 2009, 394:177-182.
18. Sandblad L., et al. The Schizosaccharomyces pombe EB1 homolog Mal3p binds and stabilizes the microtubule lattice seam. Cell 2006, 127:1415-1424.
19. 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.
20. des Georges A., et al. Mal3, the Schizosaccharomyces pombe homolog of EB1, changes the microtubule lattice. Nat. Struct. Mol. Biol. 2008, 15:1102-1108.
21. Fourniol F.J., et al. Template-free 13-protofilament microtubule-MAP assembly visualized at 8 A resolution. J. Cell Biol. 2010, 191:463-470.
22. Bechstedt, S. and Brouhard, G.J. (2012) Doublecortin recognizes the 13-protofilament microtubule cooperatively and tracks microtubule ends. Dev. Cell, doi:10.1016/j.devcel.2012.05.006.
23. Chretien D., et al. Structure of growing microtubule ends: two-dimensional sheets close into tubes at variable rates. J. Cell Biol. 1995, 129:1311-1328.
24. Tirnauer J.S., et al. EB1-microtubule interactions in Xenopus egg extracts: role of EB1 in microtubule stabilization and mechanisms of targeting to microtubules. Mol. Biol. Cell 2002, 13:3614-3626.
25. Buey R.M., et al. Insights into EB1 structure and the role of its C-terminal domain for discriminating microtubule tips from the lattice. Mol. Biol. Cell 2011, 22:2912-2923.
26. Vitre B., et al. EB1 regulates microtubule dynamics and tubulin sheet closure in vitro. Nat. Cell Biol. 2008, 10:415-421.
27. 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.
28. Gierke S., Wittmann T. EB1-recruited microtubule +TIP complexes coordinate protrusion dynamics during 3D epithelial remodeling. Curr. Biol. 2012, 22:753-762.
29. Montenegro G.S., et al. In vitro reconstitution of the functional interplay between MCAK and EB3 at microtubule plus ends. Curr. Biol. 2010, 20:1717-1722.
30. Honnappa S., et al. An EB1-binding motif acts as a microtubule tip localization signal. Cell 2009, 138:366-376.
31. Kumar P., et al. Multisite phosphorylation disrupts arginine-glutamate salt bridge networks required for binding of the cytoplasmic linker-associated protein 2 (CLASP2) to end-binding protein 1 (EB1). J. Biol. Chem 2012, 287:17050-17064.
32. Honnappa S., et al. Structural insights into the EB1-APC interaction. EMBO J. 2005, 24:261-269.
33. 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.
34. 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.
35. Neduva V., Russell R.B. DILIMOT: discovery of linear motifs in proteins. Nucleic Acids Res. 2006, 34:W350-W355.
36. Zimniak T., et al. Spatiotemporal regulation of ipl1/aurora activity by direct cdk1 phosphorylation. Curr. Biol. 2012, 22:787-793.
37. Browning H., et al. Targeted movement of cell end factors in fission yeast. Nat. Cell Biol. 2003, 5:812-818.
38. 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.
39. Mandell D.J., et al. Strengths of hydrogen bonds involving phosphorylated amino acid side chains. J. Am. Chem. Soc. 2007, 129:820-827.
40. Kumar P., et al. GSK3beta phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J. Cell Biol. 2009, 184:895-908.
41. Watanabe T., et al. Phosphorylation of CLASP2 by GSK-3beta regulates its interaction with IQGAP1, EB1 and microtubules. J. Cell Sci. 2009, 122:2969-2979.
42. Moore A.T., et al. MCAK associates with the tips of polymerizing microtubules. J. Cell Biol. 2005, 169:391-397.
43. Meireles A.M., et al. Kebab: kinetochore and EB1 associated basic protein that dynamically changes its localisation during Drosophila mitosis. PLoS ONE 2011, 6:e24174.
44. Wu X., et al. Skin stem cells orchestrate directional migration by regulating microtubule-ACF7 connections through GSK3beta. Cell 2011, 144:341-352.
45. Steinmetz M.O., Akhmanova A. Capturing protein tails by CAP-Gly domains. Trends Biochem. Sci. 2008, 33:535-545.
46. Slep K.C. Structural and mechanistic insights into microtubule end-binding proteins. Curr. Opin. Cell Biol. 2010, 22:88-95.
47. Mishima M., et al. Structural basis for tubulin recognition by cytoplasmic linker protein 170 and its autoinhibition. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:10346-10351.
48. Honnappa S., et al. Key interaction modes of dynamic +TIP networks. Mol. Cell 2006, 23:663-671.
49. Gupta K.K., et al. Minimal plus-end tracking unit of the cytoplasmic linker protein CLIP-170. J. Biol. Chem. 2009, 284:6735-6742.
50. Komarova Y., et al. EB1 and EB3 control CLIP dissociation from the ends of growing microtubules. Mol. Biol. Cell 2005, 16:5334-5345.
51. Weisbrich A., et al. Structure-function relationship of CAP-Gly domains. Nat. Struct. Mol. Biol. 2007, 14:959-967.
52. 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.
53. Lansbergen G., et al. Conformational changes in CLIP-170 regulate its binding to microtubules and dynactin localization. J. Cell Biol. 2004, 166:1003-1014.
54. Bjelic S., et al. Interaction of mammalian end binding proteins with CAP-Gly domains of CLIP-170 and p150(glued). J. Struct. Biol. 2012, 177:160-167.
55. Wollman R., et al. Efficient chromosome capture requires a bias in the 'search-and-capture' process during mitotic-spindle assembly. Curr. Biol. 2005, 15:828-832.
56. Wu X., et al. ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 2008, 135:137-148.
57. Lansbergen G., et al. CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5beta. Dev. Cell 2006, 11:21-32.
58. Mimori-Kiyosue Y., 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.
59. Kodama A., et al. ACF7: an essential integrator of microtubule dynamics. Cell 2003, 115:343-354.
60. Applewhite D.A., et al. The spectraplakin Short stop is an actin-microtubule cross-linker that contributes to organization of the microtubule network. Mol. Biol. Cell 2010, 21:1714-1724.
61. Drabek K., et al. Role of CLASP2 in microtubule stabilization and the regulation of persistent motility. Curr. Biol. 2006, 16:2259-2264.
62. Wittmann T., Waterman-Storer C.M. Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3beta in migrating epithelial cells. J. Cell Biol. 2005, 169:929-939.
63. Barth A.I., et al. Role of adenomatous polyposis coli (APC) and microtubules in directional cell migration and neuronal polarization. Semin. Cell Dev. Biol. 2008, 19:245-251.
64. Kita K., et al. Adenomatous polyposis coli on microtubule plus ends in cell extensions can promote microtubule net growth with or without EB1. Mol. Biol. Cell 2006, 17:2331-2345.
65. Etienne-Manneville S. APC in cell migration. Adv. Exp. Med. Biol. 2009, 656:30-40.
66. Caro-Gonzalez H.Y., et al. Mitogen-activated protein kinase (MAPK/ERK) regulates adenomatous polyposis coli during growth-factor-induced cell extension. J. Cell Sci. 2012, 125:1247-1258.
67. Bahmanyar S., et al. Role of APC and its binding partners in regulating microtubules in mitosis. Adv. Exp. Med. Biol. 2009, 656:65-74.
68. Maffini S., et al. Motor-independent targeting of CLASPs to kinetochores by CENP-E promotes microtubule turnover and poleward flux. Curr. Biol. 2009, 19:1566-1572.
69. Efimov A., et al. Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev. Cell 2007, 12:917-930.
70. Miller P.M., et al. Golgi-derived CLASP-dependent microtubules control Golgi organization and polarized trafficking in motile cells. Nat. Cell Biol. 2009, 11:1069-1080.
71. Grigoriev I., et al. STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr. Biol. 2008, 18:177-182.
72. Wu X.S., et al. Melanophilin and myosin Va track the microtubule plus end on EB1. J. Cell Biol. 2005, 171:201-207.
73. Jaworski J., et al. Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 2009, 61:85-100.
74. Mennella V., et al. Functionally distinct kinesin-13 family members cooperate to regulate microtubule dynamics during interphase. Nat. Cell Biol. 2005, 7:235-245.
75. Jiang K., et al. TIP150 interacts with and targets MCAK at the microtubule plus ends. EMBO Rep. 2009, 10:857-865.
76. Stout J.R., et al. Kif18B interacts with EB1 and controls astral microtubule length during mitosis. Mol. Biol. Cell 2011, 22:3070-3080.
77. Tanenbaum M.E., et al. A complex of Kif18b and MCAK promotes microtubule depolymerization and is negatively regulated by Aurora kinases. Curr. Biol. 2011, 21:1356-1365.
78. Currie J.D., et al. The microtubule lattice and plus-end association of Drosophila Mini spindles is spatially regulated to fine-tune microtubule dynamics. Mol. Biol. Cell 2011, 22:4343-4361.
79. Li W., et al. EB1 promotes microtubule dynamics by recruiting Sentin in Drosophila cells. J. Cell Biol. 2011, 193:973-983.
80. Al-Bassam J., et al. CLASP promotes microtubule rescue by recruiting tubulin dimers to the microtubule. Dev. Cell 2010, 19:245-258.
81. Al-Bassam J., Chang F. Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol. 2011, 21:604-614.
82. Lewis A., et al. The C-terminus of Apc does not influence intestinal adenoma development or progression. J. Pathol. 2012, 226:73-83.
83. Hume A.N., et al. Rab27a and MyoVa are the primary Mlph interactors regulating melanosome transport in melanocytes. J. Cell Sci. 2007, 120:3111-3122.
84. Zaoui K., et al. ErbB2 receptor controls microtubule capture by recruiting ACF7 to the plasma membrane of migrating cells. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:18517-18522.
85. Etienne-Manneville S., et al. Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J. Cell Biol. 2005, 170:895-901.
86. Reilein A., Nelson W.J. APC is a component of an organizing template for cortical microtubule networks. Nat. Cell Biol. 2005, 7:463-473.
87. Nathke I.S. The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu. Rev. Cell Dev. Biol. 2004, 20:337-366.
88. Smyth J.T., et al. Phosphorylation of STIM1 underlies suppression of store-operated calcium entry during mitosis. Nat. Cell Biol. 2009, 11:1465-1472.
89. Feske S., et al. Immunodeficiency due to mutations in ORAI1 and STIM1. Clin. Immunol. 2010, 135:169-182.
90. Andrews P.D., et al. Aurora B regulates MCAK at the mitotic centromere. Dev. Cell 2004, 6:253-268.
91. Goshima G., et al. Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J. Cell Biol. 2008, 181:421-429.
92. Fong K.W., et al. Interaction of CDK5RAP2 with EB1 to track growing microtubule tips and to regulate microtubule dynamics. Mol. Biol. Cell 2009, 20:3660-3670.
93. Megraw T.L., et al. Cdk5rap2 exposes the centrosomal root of microcephaly syndromes. Trends Cell Biol. 2011, 21:470-480.
94. van Gele M., et al. Griscelli syndrome: a model system to study vesicular trafficking. Pigment Cell Melanoma Res. 2009, 22:268-282.
95. Yan X., et al. A complex of two centrosomal proteins, CAP350 and FOP, cooperates with EB1 in microtubule anchoring. Mol. Biol. Cell 2006, 17:634-644.
96. Popovici C., et al. The t(6;8)(q27;p11) translocation in a stem cell myeloproliferative disorder fuses a novel gene, FOP, to fibroblast growth factor receptor 1. Blood 1999, 93:1381-1389.
97. Martinez-Lopez M.J., et al. Mouse neuron navigator 1, a novel microtubule-associated protein involved in neuronal migration. Mol. Cell. Neurosci. 2005, 28:599-612.
98. van Haren J., et al. Mammalian Navigators are microtubule plus-end tracking proteins that can reorganize the cytoskeleton to induce neurite-like extensions. Cell Motil. Cytoskeleton 2009, 66:824-838.
99. Rogers S.L., et al. Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr. Biol. 2004, 14:1827-1833.
100. Hsieh P.C., et al. p53 downstream target DDA3 is a novel microtubule-associated protein that interacts with end-binding protein EB3 and activates beta-catenin pathway. Oncogene 2007, 26:4928-4940.
101. Jang C.Y., et al. DDA3 recruits microtubule depolymerase Kif2a to spindle poles and controls spindle dynamics and mitotic chromosome movement. J. Cell Biol. 2008, 181:255-267.
102. Laht P., et al. Plexin-B3 interacts with EB-family proteins through a conserved motif. Biochim. Biophys. Acta 2012, 1820:888-893.
103. De Groot C.O., et al. Molecular insights into mammalian end-binding protein heterodimerization. J. Biol. Chem. 2010, 285:5802-5814.
104. 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.