Vimentin intermediate filament and plectin provide a scaffold for invadopodia, facilitating cancer cell invasion and extravasation for metastasis

被引:88
作者
Yoneyama, Mihoko Sutoh [1 ]
Hatakeyama, Shingo [1 ]
Habuchi, Tomonori [2 ]
Inoue, Takamitsu [2 ]
Nakamura, Toshiya [3 ]
Funyu, Tomihisa [4 ]
Wiche, Gerhard [5 ]
Ohyama, Chikara [1 ]
Tsuboi, Shigeru [1 ,4 ]
机构
[1] Hirosaki Univ, Grad Sch Med, Dept Urol, Hirosaki, Aomori, Japan
[2] Akita Univ, Grad Sch Med, Dept Urol, Akita 0108543, Japan
[3] Hirosaki Univ, Grad Sch Hlth Sci, Dept Biomed Sci, Hirosaki, Aomori, Japan
[4] Oyokyo Kidney Res Inst, Dept Canc Immunol & Cell Biol, Hirosaki, Aomori, Japan
[5] Univ Vienna, Dept Biochem & Cell Biol, Max F Perutz Labs, A-1030 Vienna, Austria
关键词
Cancer cell extravasation; Invadopodium; Invadosome; Invasion; Plectin; Vimentin; EPITHELIAL-MESENCHYMAL TRANSITION; PODOSOME FORMATION; IN-VIVO; F-ACTIN; MIGRATION; CORTACTIN; BINDING; MECHANISMS; ADHESION;
D O I
10.1016/j.ejcb.2014.03.002
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
To investigate the molecular mechanisms of cancer metastasis, we have isolated a high-metastatic bladder cancer cell subpopulation from a low-metastatic cell line by using an in vivo selection system. Cells in the subpopulation showed a high ability to form invadopodia, the filamentous actin (F-actin)-based membrane protrusions that play an essential role in cancer cell invasion. Analysis of the gene expression profile revealed that the expression of an intermediate filament (IF) protein, vimentin and a cytoskeletal linker protein, plectin was up-regulated in the high-metastatic subpopulation compared with the low metastatic cell line. Here we report a novel role of vimentin IF and plectin in metastasis. In invasive bladder cancer cells, the vimentin IF-plectin-invadopodia F-actin link was formed. Disruption of this link severely impaired invadopodia formation, reducing the capacities of extracellular matrix degradation, transendothelial migration and metastasis. In addition, the vimentin assembly into the filaments was required for invadopodia formation. Our results suggest that plectin anchoring invadopodia to vimentin IF scaffolds and stabilizes invadopodia, which is a critical molecular process for cancer cell invasion and extravasation for metastasis. (C) 2014 Elsevier GmbH. All rights reserved.
引用
收藏
页码:157 / 169
页数:13
相关论文
共 57 条
[1]   Histological variants of urothelial carcinoma: diagnostic, therapeutic and prognostic implications [J].
Amin, Mahul B. .
MODERN PATHOLOGY, 2009, 22 :S96-S118
[2]   Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation [J].
Ayala, Inmaculada ;
Baldassarre, Massimiliano ;
Giacchetti, Giada ;
Caldieri, Giusi ;
Tete, Stefano ;
Luini, Alberto ;
Buccione, Roberto .
JOURNAL OF CELL SCIENCE, 2008, 121 (03) :369-378
[3]   Plectin-1 as a Novel Biomarker for Pancreatic Cancer [J].
Bausch, Dirk ;
Thomas, Stephanie ;
Mino-Kenudson, Mari ;
Fernandez-del Castillo, Carlos ;
Bauer, Todd W. ;
Williams, Mark ;
Warshaw, Andrew L. ;
Thayer, Sarah P. ;
Kelly, Kimberly A. .
CLINICAL CANCER RESEARCH, 2011, 17 (02) :302-309
[4]   A role for the podosome/invadopodia scaffold protein Tks5 in tumor growth in vivo [J].
Blouw, Barbara ;
Seals, Darren F. ;
Pass, Ian ;
Diaz, Begona ;
Courtneidge, Sara A. .
EUROPEAN JOURNAL OF CELL BIOLOGY, 2008, 87 (8-9) :555-567
[5]   Cutting edge: Integration of human T lymphocyte cytoskeleton by the cytolinker plectin [J].
Brown, MJ ;
Hallam, JA ;
Liu, Y ;
Yamada, KM ;
Shaw, S .
JOURNAL OF IMMUNOLOGY, 2001, 167 (02) :641-645
[6]   Invadopodia: specialized tumor cell structures for the focal degradation of the extracellular matrix [J].
Buccione, Roberto ;
Caldieri, Giusi ;
Ayala, Inmaculada .
CANCER AND METASTASIS REVIEWS, 2009, 28 (1-2) :137-149
[7]   Keeping the Vimentin Network under Control: Cell-Matrix Adhesion-associated Plectin 1f Affects Cell Shape and Polarity of Fibroblasts [J].
Burgstaller, Gerald ;
Gregor, Martin ;
Winter, Lilli ;
Wiche, Gerhard .
MOLECULAR BIOLOGY OF THE CELL, 2010, 21 (19) :3362-3375
[8]   Trans-cellular migration: cell-cell contacts get intimate [J].
Carman, Christopher V. ;
Springer, Timothy A. .
CURRENT OPINION IN CELL BIOLOGY, 2008, 20 (05) :533-540
[9]   Transcellular diapedesis is initiated by invasive podosomes [J].
Carman, Christopher V. ;
Sage, Peter T. ;
Sciuto, Tracey E. ;
de la Fuente, Miguel A. ;
Geha, Raif S. ;
Ochs, Hans D. ;
Dvorak, Harold F. ;
Dvorak, Ann M. ;
Springer, Timothy A. .
IMMUNITY, 2007, 26 (06) :784-797
[10]   The dynamic properties of intermediate filaments during organelle transport [J].
Chang, Lynne ;
Barlan, Kari ;
Chou, Ying-Hao ;
Grin, Boris ;
Lakonishok, Margot ;
Serpinskaya, Anna S. ;
Shumaker, Dale K. ;
Herrmann, Harald ;
Gelfand, Vladimir I. ;
Goldman, Robert D. .
JOURNAL OF CELL SCIENCE, 2009, 122 (16) :2914-2923