EB1 and EB3 control CLIP dissociation from the ends of growing microtubules

Molecular Biology of the Cell

Volumn 16, Issue 11, 2005, Pages 5334-5345

  Komarova, Yulia ^a   Lansbergen, Gideon ^b   Galjart, Niels ^b   Grosveld, Frank ^b   Borisy, Gary G ^a   Akhmanova, Anna ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MUTANT PROTEIN; PROTEIN CLIP; PROTEIN CLIP 115; PROTEIN CLIP 170; PROTEIN EB1; PROTEIN EB2; PROTEIN EB3; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; DISSOCIATION; GENE OVEREXPRESSION; GENETIC CONSERVATION; MICROTUBULE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE;

AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; CHO CELLS; COS CELLS; CRICETINAE; CRICETULUS; CYTOSKELETAL PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NEOPLASM PROTEINS; NERVE TISSUE PROTEINS; TRANSFECTION;

ANIMALIA; MAMMALIA;

EID: 27644487562     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-07-0614     Document Type: Article

References (37)

1. Akhmanova, A., and Hoogenraad, C. C. (2005). Microtubule plus-end-tracking proteins: mechanisms and functions. Curr. Opin. Cell Biol. 17, 47-54.
2. Arnal, I., Heichette, C., Diamantopoulos, G. S., and Chretien, D. (2004). CLIP-170/tubulin-curved oligomers coassemble at microtubule ends and promote rescues. Curr. Biol. 14, 2086-2095.
3. Askham, J. M., Vaughan, K. T., Goodson, H. V., and Morrison, E. E. (2002). 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 13, 3627-3645.
4. Badin-Larcon, A. C., Boscheron, C., Soleilhac, J. M., Piel, M., Mann, C., Denarier, E., Fourest-Lieuvin, A., Lafanechere, L., Bornens, M., and Job, D. (2004). Suppression of nuclear oscillations in Saccharomyces cerevisiae expressing Glu tubulin. Proc. Natl. Acad. Sci. USA 101, 5577-5582.
5. Berrueta, L., Kraeft, S. K., Tirnauer, J. S., Schuyler, S. C., Chen, L. B., Hill, D. E., Pellman, D., and Bierer, B. E. (1998). The adenomatous polyposis coli-binding protein EB1 is associated with cytoplasmic and spindle microtubules. Proc. Natl. Acad. Sci. USA 95, 10596-10601.
6. Brummelkamp, T. R., Bernards, R., and Agami, R. (2002). A system for stable expression of short interfering RNAs in mammalian cells. Science 296, 550-553.
7. Bu, W., and Su, L. K. (2003). Characterization of functional domains of human EB1 family proteins. J. Biol. Chem. 278, 49721-49731.
8. Busch, K. E., and Brunner, D. (2004). The microtubule plus end-tracking proteins mal3p and tip1p cooperate for cell-end targeting of interphase microtubules. Curr. Biol. 14, 548-559.
9. Busch, K. E., Hayles, J., Nurse, P., and Brunner, D. (2004). Tea2p kinesin is involved in spatial microtubule organization by transporting tip1p on microtubules. Dev. Cell 6, 831-843.
10. Carvalho, P., Gupta, M. L., Jr., Hoyt, M. A., and Pellman, D. (2004). Cell cycle control of kinesin-mediated transport of Bik1 (CLIP-170) regulates microtubule stability and dynein activation. Dev. Cell 6, 815-829.
11. Carvalho, P., Tirnauer, J. S., and Pellman, D. (2003). Surfing on microtubule ends. Trends Cell Biol. 13, 229-237.
12. Coquelle, F. M. et al. (2002). LIS1, CLIP-170's key to the dynein/dynactin pathway. Mol. Cell. Biol. 22, 3089-3102.
13. Diamantopoulos, G. S., Perez, F., Goodson, H. V., Batelier, G., Melki, R., Kreis, T. E., and Rickard, J. E. (1999). Dynamic localization of CLIP-170 to microtubule plus ends is coupled to microtubule assembly. J. Cell Biol. 144, 99-112.
14. Erck, C. et al. (2005). A vital role of tubulin-tyrosine-ligase for neuronal organization. Proc. Natl. Acad. Sci. USA 102, 7853-7858.
15. Galjart, N., and Perez, F. (2003). A plus-end raft to control microtubule dynamics and function. Curr. Opin. Cell Biol. 25, 48-53.
16. Goodson, H. V., Skube, S. B., Stalder, R., Valetti, C., Kreis, T. E., Morrison, E. E., and Schroer, T. A. (2003). CLIP-170 interacts with dynactin complex and the APC-binding protein EB1 by different mechanisms. Cell Motil. Cytoskelet. 55, 156-173.
17. Hayashi, I., and Ikura, M. (2003). Crystal structure of the amino-terminal microtubule-binding domain of end-binding protein 1 (EB1). J. Biol. Chem. 278, 36430-36434.
18. Honnappa, S., John, C. M., Kostrewa, D., Winkler, F. K., and Steinmetz, M. O. (2005). Structural insights into the EB1-APC interaction. EMBO J. 24, 261-269.
19. Hoogenraad, C. C., Akhmanova, A., Grosveld, F., De Zeeuw, C. I., and Galjart, N. (2000). Functional analysis of CLIP-115 and its binding to microtubules. J. Cell Sci. 113, 2285-2297.
20. Howard, J., and Hyman, A. A. (2003). Dynamics and mechanics of the microtubule plus end. Nature 422, 753-758.
21. Juwana, J. P., Henderikx, P., Mischo, A., Wadle, A., Fadle, N., Gerlach, K., Arends, J. W., Hoogenboom, H., Pfreundschuh, M., and Renner, C. (1999). EB/RP gene family encodes tubulin binding proteins. Int. J. Cancer 81, 275-284.
22. Kodama, A., Karakesisoglou, I., Wong, E., Vaezi, A., and Fuchs, E. (2003). ACF7: an essential integrator of microtubule dynamics. Cell 115, 343-354.
23. Komarova, Y. A., Akhmanova, A. S., Kojima, S., Galjart, N., and Borisy, G. G. (2002). Cytoplasmic linker proteins promote microtubule rescue in vivo. J. Cell Biol. 159, 589-599.
24. Lansbergen, G. et al. (2004). Conformational changes in CLIP-170 regulate its binding to microtubules and dynactin localisation. J. Cell Biol. 166, 1003-1014.
25. Ligon, L. A., Shelly, S. S., Tokito, M., and Holzbaur, E. L. (2003). The microtubule plus-end proteins EB1 and dynactin have differential effects on microtubule polymerization. Mol. Biol. Cell 14, 1405-1417.
26. Mennella, V., Rogers, G. C., Rogers, S. L., Buster, D. W., Vale, R. D., and Sharp, D. J. (2005). Functionally distinct kinesin-13 family members cooperate to regulate microtubule dynamics during interphase. Nat. Cell Biol. 7, 235-245.
27. Mimori-Kiyosue, Y. et al. (2005). CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J. Cell Biol. 168, 141-153.
28. Perez, F., Diamantopoulos, G. S., Stalder, R., and Kreis, T. E. (1999). CLIP-170 highlights growing microtubule ends in vivo. Cell 96, 517-527.
29. Pierre, P., Scheel, J., Rickard, J. E., and Kreis, T. E. (1992). CLIP-170 links endocytic vesicles to microtubules. Cell 70, 887-900.
30. Rogers, S. L., Wiedemann, U., Hacker, U., Turck, C., and Vale, R. D. (2004). Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr. Biol. 14, 1827-1833.
31. Schuyler, S. C., and Pellman, D. (2001). Microtubule "plus-end- tracking proteins": the end is just the beginning. Cell 105, 421-424.
32. Slep, K. C., Rogers, S. L., Elliott, S. L., Ohkura, H., Kolodziej, P. A., and Vale, R. D. (2005). Structural determinants for EB1-mediated recruitment of APC and spectraplakins to the microtubule plus end. J. Cell Biol. 168, 587-598.
33. Stepanova, T., Slemmer, J., Hoogenraad, C. C., Lansbergen, G., Dortland, B., De Zeeuw, C. I., Grosveld, F., van Cappellen, G., Akhmanova, A., and Galjart, N. (2003). Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23, 2655-2664.
34. Su, L. K., and Qi, Y. (2001). Characterization of human MAPRE genes and their proteins. Genomics 71, 142-149.
35. Tirnauer, J. S., and Bierer, B. E. (2000). EB1 proteins regulate microtubule dynamics, cell polarity, and chromosome stability. J. Cell Biol. 149, 761-766.
36. Tirnauer, J. S., Grego, S., Salmon, E. D., and Mitchison, T. J. (2002). EB1-microtubule interactions in Xenopus egg extracts: role of EB1 in microtubule stabilization and mechanisms of targeting to microtubules. Mol. Biol. Cell 13, 3614-3626.
37. Wen, Y., Eng, C. H., Schmoranzer, J., Cabrera-Poch, N., Morris, E. J., Chen, M., Wallar, B. J., Alberts, A. S., and Gundersen, G. G. (2004). EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat. Cell Biol. 6, 820-830.