CLASP2 has two distinct TOG domains that contribute differently to microtubule dynamics

Journal of Molecular Biology

Volumn 427, Issue 14, 2015, Pages 2379-2395

  Maki, Takahisa ^a   Grimaldi, Ashley D ^b   Fuchigami, Sotaro ^a   Kaverina, Irina ^b   Hayashi, Ikuko ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

+TIPs; Crystal structure; Microtubule; Microtubule associated protein (map); Molecular modeling

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN; CLIP ASSOCIATED PROTEIN 2; GREEN FLUORESCENT PROTEIN; PROTEIN; RED FLUORESCENT PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG; CLASP2 PROTEIN, HUMAN; CLASP2 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DISSOCIATION CONSTANT; GEL PERMEATION CHROMATOGRAPHY; GENE INSERTION SEQUENCE; HYDROGEN BOND; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; ISOTHERMAL TITRATION CALORIMETRY; MICROTUBULE; MOLECULAR MODEL; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; STOICHIOMETRY; WESTERN BLOTTING; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CELL CULTURE; CHEMICAL STRUCTURE; CHEMISTRY; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELLS, CULTURED; CRYSTALLOGRAPHY, X-RAY; HEK293 CELLS; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84934987503     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.05.012     Document Type: Article

References (53)

1. Mitchison T, Kirschner M. Dynamic instability of microtubule growth. Nature 1984;312:237-42.
2. Desai A, Mitchison TJ. Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 1997;13:83-117.
3. Akhmanova A, Steinmetz MO. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol 2008;9:309-22.
4. Maiato H, Fairley EA, Rieder CL, Swedlow JR, Sunkel CE, Earnshaw WC. Human CLASP1 is an outer kinetochore component that regulates spindle microtubule dynamics. Cell 2003;113:891-904.
5. Bratman SV, Chang F. Stabilization of overlapping microtubules by fission yeast CLASP. Dev Cell 2007;13:812-27.
6. Efimov A, Kharitonov A, Efimova N, Loncarek J, Miller PM, Andreyeva N, et al. Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev Cell 2007;12:917-30.
7. Akhmanova A, Hoogenraad CC, Drabek K, Stepanova T, Dortland B, Verkerk T, et al. Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 2001;104:923-35.
8. Charrasse S, Schroeder M, Gauthier-Rouviere C, Ango F, Cassimeris L, Gard DL, et al. The TOGp protein is a new human microtubule-associated protein homologous to the Xenopus XMAP215. J Cell Sci 1998;111:1371-83.
9. Brouhard GJ, Stear JH, Noetzel TL, Al-Bassam J, Kinoshita K, Harrison SC, et al. XMAP215 is a processive microtubule polymerase. Cell 2008;132:79-88.
10. Al-Bassam J, Larsen NA, Hyman AA, Harrison SC. Crystal structure of a TOG domain: conserved features of XMAP215/Dis1-family TOG domains and implications for tubulin binding. Structure 2007;15:355-62.
11. Slep KC, Vale RD. Structural basis of microtubule plus end tracking by XMAP215, CLIP-170, and EB1. Mol Cell 2007;27:976-91.
12. Al-Bassam J, Chang F. Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol 2011;21:604-14.
13. Ayaz P, Ye X, Huddleston P, Brautigam CA, Rice LM. A TOG:αβ-tubulin complex structure reveals conformation-based mechanisms for a microtubule polymerase. Science 2012;337:857-60.
14. Slep KC. The role of TOG domains in microtubule plus end dynamics. Biochem Soc Trans 2009;37:1002-6.
15. Leano JB, Rogers SL, Slep KC. A cryptic TOG domain with a distinct architecture underlies CLASP-dependent bipolar spindle formation. Structure 2013;21:939-50.
16. Wittmann T, Waterman-Storer CM. Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3beta in migrating epithelial cells. J Cell Biol 2005;169:929-39.
17. Tournebize R, Popov A, Kinoshita K, Ashford AJ, Rybina S, Pozniakovsky A, et al. Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nat Cell Biol 2000;2:13-9.
18. Widlund PO, Stear JH, Pozniakovsky A, Zanic M, Reber S, Brouhard GJ, et al. XMAP215 polymerase activity is built by combining multiple tubulin-binding TOG domains and a basic lattice-binding region. Proc Natl Acad Sci U S A 2011;108:2741-6.
19. Al-Bassam J, Kim H, Brouhard G, van Oijen A, Harrison SC, Chang F. CLASP promotes microtubule rescue by recruiting tubulin dimers to the microtubule. Dev Cell 2010;19:245-58.
20. Mimori-Kiyosue Y, Grigoriev I, Lansbergen G, Sasaki H, Matsui C, Severin F, et al. CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J Cell Biol 2005;168:141-53.
21. Inoue YH, do Carmo Avides M, Shiraki M, Deak P, Yamaguchi M, Nishimoto Y, et al. Orbit, a novel microtubule-associated protein essential for mitosis in Drosophila melanogaster. J Cell Biol 2000;149:153-66.
22. Lemos CL, Sampaio P, Maiato H, Costa M, Omel'yanchuk LV, Liberal V, et al. Mast, a conserved microtubule-associated protein required for bipolar mitotic spindle organization. EMBO J 2000;19:3668-82.
23. Kumar P, Lyle KS, Gierke S, Matov A, Danuser G, Wittmann T. GSK3beta phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J Cell Biol 2009;184:895-908.
24. Watanabe T, Noritake J, Kakeno M, Matsui T, Harada T, Wang S, et al. Phosphorylation of CLASP2 by GSK-3beta regulates its interaction with IQGAP1, EB1 and microtubules. J Cell Sci 2009;122:2969-79.
25. Hoogenraad CC, Akhmanova A, Grosveld F, De Zeeuw CI, Galjart N. Functional analysis of CLIP-115 and its binding to microtubules. J Cell Sci 2000;113:2285-97.
26. Kumar P, Chimenti MS, Pemble H, Schonichen A, Thompson O, Jacobson MP, et al. Multisite phosphorylation disrupts arginine-glutamate salt bridge networks required for binding of cytoplasmic linker-associated protein 2 (CLASP2) to end-binding protein 1 (EB1). J Biol Chem 2012;287:17050-64.
27. Buey RM, Sen I, Kortt O, Mohan R, Gfeller D, Veprintsev D, et al. Sequence determinants of a microtubule tip localization signal (MtLS). J Biol Chem 2012;287:28227-42.
28. Podolski M, Mahamdeh M, Howard J. Stu2, the budding yeast XMAP215/Dis1 homolog, promotes assembly of yeast microtubules by increasing growth rate and decreasing catastrophe frequency. J Biol Chem 2014;289:28087-93.
29. Löwe J, Li H, Downing KH, Nogales E. Refined structure of αβ-tubulin at 3.5 Å resolution. J Mol Biol 2001;313:1045-57.
30. Ravelli RB, Gigant B, Curmi PA, Jourdain I, Lachkar S, Sobel A, et al. Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain. Nature 2004;428:198-202.
31. Asenjo AB, Chatterjee C, Tan D, DePaoli V, Rice WJ, Diaz-Avalos R, et al. Structural model for tubulin recognition and deformation by kinesin-13 microtubule depolymerases. Cell Rep 2013;3:759-68.
32. Jordan MA, Margolis RL, Himes RH, Wilson L. Identification of a distinct class of vinblastine binding sites on microtubules. J Mol Biol 1986;187:61-73.
33. Gigant B, Wang C, Ravelli RB, Roussi F, Steinmetz MO, Curmi PA, et al. Structural basis for the regulation of tubulin by vinblastine. Nature 2005;435:519-22.
34. Moores CA, Milligan RA. Visualisation of a kinesin-13 motor on microtubule end mimics. J Mol Biol 2008;377:647-54.
35. Cormier A, Marchand M, Ravelli RB, Knossow M, Gigant B. Structural insight into the inhibition of tubulin by vinca domain peptide ligands. EMBO Rep 2008;9:1101-6.
36. Honnappa S, Gouveia SM, Weisbrich A, Damberger FF, Bhavesh NS, Jawhari H, et al. An EB1-binding motif acts as a microtubule tip localization signal. Cell 2009;138:366-76.
37. Patel K, Nogales E, Heald R. Multiple domains of human CLASP contribute to microtubule dynamics and organization in vitro and in Xenopus egg extracts. Cytoskeleton (Hoboken) 2012;69:155-65.
38. Grimaldi AD, Maki T, Fitton BP, Roth D, Yampolsky D, Davidson MW, et al. CLASPs are required for proper microtubule localization of end-binding proteins. Dev Cell 2014;30:343-52.
39. Nogales E, Wang HW. Structural intermediates in microtubule assembly and disassembly: how and why? Curr Opin Struct Biol 2006;18:179-84.
40. Ayaz P, Munyoki S, Geyer EA, Piedra FA, Vu ES, Bromberg R, et al. A tethered delivery mechanism explains the catalytic action of a microtubule polymerase. eLife 2014;3:03069.
41. Blommel PG, Fox BG. A combined approach to improving large-scale production of tobacco etch virus protease. Protein Expr Purif 2007;55:53-68.
42. Van Duyne GD, Standaert RF, Karplus PA, Schreiber SL, Clardy J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J Mol Biol 1993;229:105-24.
43. Hayashi I, Wilde A, Mal TK, Ikura M. Structural basis for the activation of microtubule assembly by the EB1 and p150Glued complex. Mol Cell 2005;19:449-60.
44. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276:307-26.
45. Terwilliger TC, Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 1999;55:849-61.
46. Terwilliger TC. Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr 2000;56:965-72.
47. Perrakis A, Morris R, Lamzin VS. Automated protein model building combined with iterative structure refinement. Nat Struct Biol 1999;6:458-63.
48. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004;60:2126-32.
49. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 1998;54:905-21.
50. DeLano WL. The PyMOL Molecular Graphics System, Version 1.2b2. Schrödinger, LLC; 2002.
51. Hyman A, Drechsel D, Kellogg D, Salser S, Sawin K, Steffen P, et al. Preparation of modified tubulins. Methods Enzymol 1991;196:478-85.
52. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 2001;98:10037-41.
53. Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983;22:2577-637.