Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network

被引:388
作者
Efimov, Andrey
Kharitonov, Alexey
Efimova, Nadia
Loncarek, Jadranka
Miller, Paul M.
Andreyeva, Natalia
Gleeson, Paul
Galjart, Niels
Maia, Ana R. R.
McLeod, Ian X.
Yates, John R., III
Maiato, Helder
Khodjakov, Alexey
Akhmanova, Anna
Kaverina, Irina [1 ]
机构
[1] Vanderbilt Univ, Med Ctr, Dept Cell & Dev Biol, Nashville, TN 37232 USA
[2] Austrian Acad Sci, IMBA, A-1030 Vienna, Austria
[3] New York State Dept Hlth, Wadsworth Ctr Labs & Res, Albany, NY 12201 USA
[4] Univ Melbourne, Dept Biochem & Mol Biol, Bio21 Mol Sci & Biotechnol Inst, Melbourne, Vic 3010, Australia
[5] Erasmus MC, Dept Cell Biol & Genet, NL-3000 DR Rotterdam, Netherlands
[6] Univ Porto, Fac Med, Inst Mol & Cell Biol, P-4050345 Oporto, Portugal
[7] Univ Porto, Fac Med, Lab Cell & Mol Biol, P-4050345 Oporto, Portugal
[8] Scripps Res Inst, Dept Cell Biol, La Jolla, CA 93037 USA
关键词
D O I
10.1016/j.devcel.2007.04.002
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Proper organization of microtubule arrays is essential for intracellular trafficking and cell motility. It is generally assumed that most if not all microtubules in vertebrate somatic cells are formed by the centrosome. Here we demonstrate that a large number of microtubules in untreated human cells originate from the Golgi apparatus in a centrosome-independent manner. Both centrosomal and Golgi-emanating microtubules need gamma-tubulin for nucleation. Additionally, formation of microtubules at the Golgi requires CLASPs, microtubule-binding proteins that selectively coat noncentrosomal microtubule seeds. We show that CLASPs are recruited to the trans-Golgi network (TGN) at the Golgi periphery by the TGN protein GCC185. In sharp contrast to radial centrosomal arrays, microtubules nucleated at the peripheral Golgi compartment are preferentially oriented toward the leading edge in motile cells. We propose that Golgi-emanating microtubules contribute to the asymmetric microtubule networks in polarized cells and support diverse processes including post-Golgi transport to the cell front.
引用
收藏
页码:917 / 930
页数:14
相关论文
共 39 条
[1]   CLASPs are CLIP-115 and-170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts [J].
Akhmanova, A ;
Hoogenraad, CC ;
Drabek, K ;
Stepanova, T ;
Dortland, B ;
Verkerk, T ;
Vermeulen, W ;
Burgering, BM ;
De Zeeuw, CI ;
Grosveld, F ;
Galjart, N .
CELL, 2001, 104 (06) :923-935
[2]   THE SUBCELLULAR ORGANIZATION OF MADIN-DARBY CANINE KIDNEY-CELLS DURING THE FORMATION OF A POLARIZED EPITHELIUM [J].
BACALLAO, R ;
ANTONY, C ;
DOTTI, C ;
KARSENTI, E ;
STELZER, EHK ;
SIMONS, K .
JOURNAL OF CELL BIOLOGY, 1989, 109 (06) :2817-2832
[3]   Generation of noncentrosomal microtubule arrays [J].
Bartolini, Francesca ;
Gundersen, Gregg G. .
JOURNAL OF CELL SCIENCE, 2006, 119 (20) :4155-4163
[4]   POLARITY OF MICROTUBULES NUCLEATED BY CENTROSOMES AND CHROMOSOMES OF CHINESE-HAMSTER OVARY CELLS-INVITRO [J].
BERGEN, LG ;
KURIYAMA, R ;
BORISY, GG .
JOURNAL OF CELL BIOLOGY, 1980, 84 (01) :151-159
[5]   Reorganization of microtubule nucleation during muscle differentiation [J].
Bugnard, E ;
Zaal, KJM ;
Ralston, E .
CELL MOTILITY AND THE CYTOSKELETON, 2005, 60 (01) :1-13
[6]   The Golgi complex is a microtubule-organizing organelle [J].
Chabin-Brion, K ;
Marceiller, J ;
Perez, F ;
Settegrana, C ;
Drechou, A ;
Durand, G ;
Poüs, C .
MOLECULAR BIOLOGY OF THE CELL, 2001, 12 (07) :2047-2060
[7]  
CHEESEMAN IM, 2005, SCI STKE, pPI1, DOI DOI 10.1126/STKE.2662005PI1
[8]   LIS1, CLIP-170's key to the dynein/dynactin pathway [J].
Coquelle, FM ;
Caspi, M ;
Cordelières, FP ;
Dompierre, JP ;
Dujardin, DL ;
Koifman, C ;
Martin, P ;
Hoogenraad, CC ;
Akhmanova, A ;
Galjart, N ;
De Mey, JR ;
Reiner, O .
MOLECULAR AND CELLULAR BIOLOGY, 2002, 22 (09) :3089-3102
[9]   Centrosome localization determines neuronal polarity [J].
de Anda, FC ;
Pollarolo, G ;
Da Silva, JS ;
Camoletto, PG ;
Feiguin, F ;
Dotti, CG .
NATURE, 2005, 436 (7051) :704-708
[10]   Role of CLASP2 in microtubule stabilization and the regulation of persistent motility [J].
Drabek, Ksenija ;
van Ham, Marco ;
Stepanova, Tatiana ;
Draegestein, Katharina ;
van Horssen, Remco ;
Sayas, Carmen Laura ;
Akhmanova, Anna ;
ten Hagen, Timo ;
Smits, Ron ;
Fodde, Riccardo ;
Grosveld, Frank ;
Galjart, Niels .
CURRENT BIOLOGY, 2006, 16 (22) :2259-2264