HURP permits MTOC sorting for robust meiotic spindle bipolarity, similar to extra centrosome clustering in cancer cells

被引:88
作者
Breuer, Manuel [1 ]
Kolano, Agnieszka [1 ]
Kwon, Mijung [2 ]
Li, Chao-Chin [3 ,4 ]
Tsai, Ting-Fen [3 ,4 ]
Pellman, David [2 ]
Brunet, Stephane [1 ]
Verlhac, Marie-Helene [1 ]
机构
[1] Univ Paris 06, CNRS, Unite Mixte Rech 7622, F-75005 Paris, France
[2] Harvard Univ, Sch Med, Howard Hughes Med Inst, Dept Pediat Oncol,Dana Farber Canc Inst, Boston, MA 02115 USA
[3] Natl Yang Ming Univ, Dept Life Sci, Taipei 112, Taiwan
[4] Natl Yang Ming Univ, Inst Genome Sci, Taipei 112, Taiwan
关键词
MOUSE OOCYTES; MICROTUBULE ORGANIZATION; HEPATOCELLULAR-CARCINOMA; METAPHASE SPINDLE; MEIOSIS-I; CHROMOSOMES; DYNAMICS; DIVISION; ROLES; MOTOR;
D O I
10.1083/jcb.201005065
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
In contrast to somatic cells, formation of acentriolar meiotic spindles relies on the organization of microtubules (MTs) and MT-organizing centers (MTOCs) into a stable bipolar structure. The underlying mechanisms are still unknown. We show that this process is impaired in hepatoma up-regulated protein (Hurp) knockout mice, which are viable but female sterile, showing defective oocyte divisions. HURP accumulates on interpolar MTs in the vicinity of chromosomes via Kinesin-5 activity. By promoting MT stability in the spindle central domain, HURP allows efficient MTOC sorting into distinct poles, providing bipolarity establishment and maintenance. Our results support a new model for meiotic spindle assembly in which HURP ensures assembly of a central MT array, which serves as a scaffold for the genesis of a robust bipolar structure supporting efficient chromosome congression. Furthermore, HURP is also required for the clustering of extra centrosomes before division, arguing for a shared molecular requirement of MTOC sorting in mammalian meiosis and cancer cell division.
引用
收藏
页码:1251 / 1260
页数:10
相关论文
共 32 条
[11]   Resolution of chiasmata in oocytes requires separase-mediated proteolysis [J].
Kudo, Nobuaki R. ;
Wassmann, Katja ;
Anger, Martin ;
Schuh, Melina ;
Wirth, Karin G. ;
Xu, Huiling ;
Helmhart, Wolfgang ;
Kudo, Hiromi ;
Mckay, Michael ;
Maro, Bernard ;
Ellenberg, Jan ;
de Boer, Peter ;
Nasmyth, Kim .
CELL, 2006, 126 (01) :135-146
[12]   Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes [J].
Kwon, Mijung ;
Godinho, Susana A. ;
Chandhok, Namrata S. ;
Ganem, Neil J. ;
Azioune, Ammar ;
Thery, Manuel ;
Pellman, David .
GENES & DEVELOPMENT, 2008, 22 (16) :2189-2203
[13]   Mature Drosophila Meiosis I Spindles Comprise Microtubules of Mixed Polarity [J].
Liang, Zhang-Yi ;
Hallen, Mark Andrew ;
Endow, Sharyn Anne .
CURRENT BIOLOGY, 2009, 19 (02) :163-168
[14]   Transient exposure to the Eg5 kinesin inhibitor monastrol leads to syntelic orientation of chromosomes and aneuploidy in mouse oocytes [J].
Mailhes, JB ;
Mastromatteo, C ;
Fuseler, JW .
MUTATION RESEARCH-GENETIC TOXICOLOGY AND ENVIRONMENTAL MUTAGENESIS, 2004, 559 (1-2) :153-167
[15]   APCcdh1 activity in mouse oocytes prevents entry into the first meiotic division [J].
Reis, A ;
Chang, HY ;
Levasseur, M ;
Jones, KT .
NATURE CELL BIOLOGY, 2006, 8 (05) :539-540
[16]   MITOTIC SPINDLE ORGANIZATION BY A PLUS-END-DIRECTED MICROTUBULE MOTOR [J].
SAWIN, KE ;
LEGUELLEC, K ;
PHILIPPE, M ;
MITCHISON, TJ .
NATURE, 1992, 359 (6395) :540-543
[17]   Self-organization of MTOCs replaces Centrosome Function during Acentrosomal Spindle Assembly in Live Mouse Oocytes [J].
Schuh, Melina ;
Ellenberg, Jan .
CELL, 2007, 130 (03) :484-498
[18]   A New Model for Asymmetric Spindle Positioning in Mouse Oocytes [J].
Schuh, Melina ;
Ellenberg, Jan .
CURRENT BIOLOGY, 2008, 18 (24) :1986-1992
[19]   HURP is a ran-importin β-regulated protein that stabilizes kinetochore microtubules in the vicinity of chromosomes [J].
Silljé, HHW ;
Nagel, S ;
Körner, R ;
Nigg, EA .
CURRENT BIOLOGY, 2006, 16 (08) :731-742
[20]   Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis [J].
Srayko, Martin ;
O'Toole, Eileen T. ;
Hyman, Anthony A. ;
Mueller-Reichert, Thomas .
CURRENT BIOLOGY, 2006, 16 (19) :1944-1949