Asymmetric CLASP-Dependent Nucleation of Noncentrosomal Microtubules at the trans-Golgi Network

Developmental Cell

Volumn 12, Issue 6, 2007, Pages 917-930

  Efimov, Andrey ^a   Kharitonov, Alexey ^b   Efimova, Nadia ^a   Loncarek, Jadranka ^c   Miller, Paul M ^a   Andreyeva, Natalia ^b   Gleeson, Paul ^d   Galjart, Niels ^e   Maia, Ana R R ^f   McLeod, Ian X ^g   Yates III, John R ^g   Maiato, Helder ^f   Khodjakov, Alexey ^c   Akhmanova, Anna ^e   Kaverina, Irina ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

^c WADSWORTH CENTER   (United States)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF PORTO   (Portugal)

^g SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

CELLBIO

Indexed keywords

BINDING PROTEIN; GAMMA TUBULIN; MEMBRANE PROTEIN; PROTEIN CLASP; UNCLASSIFIED DRUG;

ARTICLE; CELL MOTILITY; CELL NUCLEUS; CELL POLARITY; CELL TRANSPORT; CENTROSOME; CONTROLLED STUDY; GOLGI COMPLEX; HUMAN; HUMAN CELL; MICROTUBULE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SOMATIC CELL; TRANS GOLGI NETWORK; VERTEBRATE;

CELLS, CULTURED; CENTROSOME; GOLGI APPARATUS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULE-ORGANIZING CENTER; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PIGMENT EPITHELIUM OF EYE; TRANS-GOLGI NETWORK; TUBULIN;

VERTEBRATA;

EID: 34249305474     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2007.04.002     Document Type: Article

References (39)

1. Akhmanova A., Hoogenraad C.C., Drabek K., Stepanova T., Dortland B., Verkerk T., Vermeulen W., Burgering B.M., De Zeeuw C.I., Grosveld F., and Galjart N. CLASPs are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104 (2001) 923-935
2. Bacallao R., Antony C., Dotti C., Karsenti E., Stelzer E.H., and Simons K. The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J. Cell Biol. 109 (1989) 2817-2832
3. Bartolini F., and Gundersen G.G. Generation of noncentrosomal microtubule arrays. J. Cell Sci. 119 (2006) 4155-4163
4. Bergen L.G., Kuriyama R., and Borisy G.G. Polarity of microtubules nucleated by centrosomes and chromosomes of Chinese hamster ovary cells in vitro. J. Cell Biol. 84 (1980) 151-159
5. Bugnard E., Zaal K.J., and Ralston E. Reorganization of microtubule nucleation during muscle differentiation. Cell Motil. Cytoskeleton 60 (2005) 1-13
6. Chabin-Brion K., Marceiller J., Perez F., Settegrana C., Drechou A., Durand G., and Pous C. The Golgi complex is a microtubule-organizing organelle. Mol. Biol. Cell 12 (2001) 2047-2060
7. Cheeseman I.M., and Desai A. A combined approach for the localization and tandem affinity purification of protein complexes from metazoans. Sci. STKE 2005 (2005) pl1
8. Coquelle F.M., Caspi M., Cordelieres F.P., Dompierre J.P., Dujardin D.L., Koifman C., Martin P., Hoogenraad C.C., Akhmanova A., Galjart N., et al. LIS1, CLIP-170's key to the dynein/dynactin pathway. Mol. Cell. Biol. 22 (2002) 3089-3102
9. de Anda F.C., Pollarolo G., Da Silva J.S., Camoletto P.G., Feiguin F., and Dotti C.G. Centrosome localization determines neuronal polarity. Nature 436 (2005) 704-708
10. Drabek K., van Ham M., Stepanova T., Draegestein K., van Horssen R., Sayas C.L., Akhmanova A., Ten Hagen T., Smits R., Fodde R., et al. Role of CLASP2 in microtubule stabilization and the regulation of persistent motility. Curr. Biol. 16 (2006) 2259-2264
11. Eng J., McCormack A., and Yates J. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5 (1994) 976-989
12. Higginbotham H., Tanaka T., Brinkman B.C., and Gleeson J.G. GSK3β and PKCζ function in centrosome localization and process stabilization during Slit-mediated neuronal repolarization. Mol. Cell. Neurosci. 32 (2006) 118-132
13. Khodjakov A., and Rieder C.L. Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. J. Cell Biol. 153 (2001) 237-242
14. Khodjakov A., Cole R.W., Oakley B.R., and Rieder C.L. Centrosome-independent mitotic spindle formation in vertebrates. Curr. Biol. 10 (2000) 59-67
15. Komarova Y.A., Vorobjev I.A., and Borisy G.G. Life cycle of MTs: persistent growth in the cell interior, asymmetric transition frequencies and effects of the cell boundary. J. Cell Sci. 115 (2002) 3527-3539
16. Ladinsky M.S., Wu C.C., McIntosh S., McIntosh J.R., and Howell K.E. Structure of the Golgi and distribution of reporter molecules at 20°C reveals the complexity of the exit compartments. Mol. Biol. Cell 13 (2002) 2810-2825
17. Lansbergen G., Grigoriev I., Mimori-Kiyosue Y., Ohtsuka T., Higa S., Kitajima I., Demmers J., Galjart N., Houtsmuller A.B., Grosveld F., and Akhmanova A. CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5β. Dev. Cell 11 (2006) 21-32
18. La Terra S., English C.N., Hergert P., McEwen B.F., Sluder G., and Khodjakov A. The de novo centriole assembly pathway in HeLa cells: cell cycle progression and centriole assembly/maturation. J. Cell Biol. 168 (2005) 713-722
19. Luders J., Patel U.K., and Stearns T. GCP-WD is a γ-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation. Nat. Cell Biol. 8 (2006) 137-147
20. Luke M.R., Kjer-Nielsen L., Brown D.L., Stow J.L., and Gleeson P.A. GRIP domain-mediated targeting of two new coiled-coil proteins, GCC88 and GCC185, to subcompartments of the trans-Golgi network. J. Biol. Chem. 278 (2003) 4216-4226
21. Malikov V., Kashina A., and Rodionov V. Cytoplasmic dynein nucleates microtubules to organize them into radial arrays in vivo. Mol. Biol. Cell 15 (2004) 2742-2749
22. Mimori-Kiyosue Y., Grigoriev I., Lansbergen G., Sasaki H., Matsui C., Severin F., Galjart N., Grosveld F., Vorobjev I., Tsukita S., and Akhmanova A. CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J. Cell Biol. 168 (2005) 141-153
23. Mironov A.A., Beznoussenko G.V., Polishchuk R.S., and Trucco A. Intra-Golgi transport: a way to a new paradigm?. Biochim. Biophys. Acta 1744 (2005) 340-350
24. Musch A. Microtubule organization and function in epithelial cells. Traffic 5 (2004) 1-9
25. Piehl M., Tulu U.S., Wadsworth P., and Cassimeris L. Centrosome maturation: measurement of microtubule nucleation throughout the cell cycle by using GFP-tagged EB1. Proc. Natl. Acad. Sci. USA 101 (2004) 1584-1588
26. Preisinger C., Short B., De Corte V., Bruyneel E., Haas A., Kopajtich R., Gettemans J., and Barr F.A. YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14-3-3ζ. J. Cell Biol. 164 (2004) 1009-1020
27. Presley J.F., Smith C., Hirschberg K., Miller C., Cole N.B., Zaal K.J., and Lippincott-Schwartz J. Golgi membrane dynamics. Mol. Biol. Cell 9 (1998) 1617-1626
28. Prigozhina N.L., and Waterman-Storer C.M. Protein kinase D-mediated anterograde membrane trafficking is required for fibroblast motility. Curr. Biol. 14 (2004) 88-98
29. Raftopoulou M., and Hall A. Cell migration: Rho GTPases lead the way. Dev. Biol. 265 (2004) 23-32
30. Reilein A., and Nelson W.J. APC is a component of an organizing template for cortical microtubule networks. Nat. Cell Biol. 7 (2005) 463-473
31. Rid R., Schiefermeier N., Grigoriev I., Small J.V., and Kaverina I. The last but not the least: the origin and significance of trailing adhesions in fibroblastic cells. Cell Motil. Cytoskeleton 61 (2005) 161-171
32. Rios R.M., Sanchis A., Tassin A.M., Fedriani C., and Bornens M. GMAP-210 recruits γ-tubulin complexes to cis-Golgi membranes and is required for Golgi ribbon formation. Cell 118 (2004) 323-335
33. Salaycik K.J., Fagerstrom C.J., Murthy K., Tulu U.S., and Wadsworth P. Quantification of microtubule nucleation, growth and dynamics in wound-edge cells. J. Cell Sci. 118 (2005) 4113-4122
34. Shanks R.A., Steadman B.T., Schmidt P.H., and Goldenring J.R. AKAP350 at the Golgi apparatus. I. Identification of a distinct Golgi apparatus targeting motif in AKAP350. J. Biol. Chem. 277 (2002) 40967-40972
35. Suter D.M., Schaefer A.W., and Forscher P. Microtubule dynamics are necessary for SRC family kinase-dependent growth cone steering. Curr. Biol. 14 (2004) 1194-1199
36. Washburn M.P., Wolters D., and Yates III J.R. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19 (2001) 242-247
37. Waterman-Storer C.M., Worthylake R.A., Liu B.P., Burridge K., and Salmon E.D. Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts. Nat. Cell Biol. 1 (1999) 45-50
38. Wittmann T., and Waterman-Storer C.M. Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3β in migrating epithelial cells. J. Cell Biol. 169 (2005) 929-939
39. Yvon A.M., and Wadsworth P. Non-centrosomal microtubule formation and measurement of minus end microtubule dynamics in A498 cells. J. Cell Sci. 110 (1997) 2391-2401