Nuclear lamin stiffness is a barrier to 3D migration, but softness can limit survival

被引:472
作者
Harada, Takamasa [1 ]
Swift, Joe [1 ]
Irianto, Jerome [1 ]
Shin, Jae-Won [1 ]
Spinler, Kyle R. [1 ]
Athirasala, Avathamsa [1 ]
Diegmiller, Rocky [1 ]
Dingal, P. C. Dave P. [1 ]
Ivanovska, Irena L. [1 ]
Discher, Dennis E. [1 ,2 ]
机构
[1] Univ Penn, Mol & Cell Biophys Lab, Philadelphia, PA 19104 USA
[2] Univ Penn, Cell & Mol Biol Grad Grp, Philadelphia, PA 19104 USA
基金
美国国家科学基金会; 美国国家卫生研究院;
关键词
MESENCHYMAL STEM-CELLS; CANCER-CELLS; RNA INTERFERENCE; DNA-DAMAGE; ENVELOPE; EXPRESSION; APOPTOSIS; PATHWAYS; ACTIVATION; CHROMATIN;
D O I
10.1083/jcb.201308029
中图分类号
Q2 [细胞生物学];
学科分类号
071013 [干细胞生物学];
摘要
Cell migration through solid tissue often involves large contortions of the nucleus, but biological significance is largely unclear. The nucleoskeletal protein lamin-A varies both within and between cell types and was shown here to contribute to cell sorting and survival in migration through constraining micropores. Lamin-A proved rate-limiting in 3D migration of diverse human cells that ranged from glioma and adenocarcinoma lines to primary mesenchymal stem cells (MSCs). Stoichiometry of A- to B-type lamins established an activation barrier, with high lamin-A:B producing extruded nuclear shapes after migration. Because the juxtaposed A and B polymer assemblies respectively conferred viscous and elastic stiffness to the nucleus, subpopulations with different A:B levels sorted in 3D migration. However, net migration was also biphasic in lamin-A, as wild-type lamin-A levels protected against stress-induced death, whereas deep knockdown caused broad defects in stress resistance. In vivo xenografts proved consistent with A:B-based cell sorting, and intermediate A:B-enhanced tumor growth. Lamins thus impede 3D migration but also promote survival against migration-induced stresses.
引用
收藏
页码:669 / 682
页数:14
相关论文
共 61 条
[1]
Barnes H. A., 2000, HDB ELEMENTARY RHEOL
[2]
The role of myosin II in glioma invasion of the brain [J].
Beadle, Christopher ;
Assanah, Marcela C. ;
Monzo, Pascale ;
Vallee, Richard ;
Rosenfeld, Steven S. ;
Canoll, Peter .
MOLECULAR BIOLOGY OF THE CELL, 2008, 19 (08) :3357-3368
[3]
Loss of lamin A/C expression in stage II and III colon cancer is associated with disease recurrence [J].
Belt, E. J. Th. ;
Fijneman, R. J. A. ;
van den Berg, E. G. ;
Bril, H. ;
Delis-van Diemen, P. M. ;
Tijssen, M. ;
van Essen, H. F. ;
de lange-de Klerk, E. S. M. ;
Belien, J. A. M. ;
Stockmann, H. B. A. C. ;
Meijer, S. ;
Meijer, G. A. .
EUROPEAN JOURNAL OF CANCER, 2011, 47 (12) :1837-1845
[4]
CHAMBERLAIN JK, 1978, BLOOD, V52, P959
[5]
Micro-Environmental Mechanical Stress Controls Tumor Spheroid Size and Morphology by Suppressing Proliferation and Inducing Apoptosis in Cancer Cells [J].
Cheng, Gang ;
Tse, Janet ;
Jain, Rakesh K. ;
Munn, Lance L. .
PLOS ONE, 2009, 4 (02)
[6]
Deficiencies in lamin B1 and lamin B2 cause neurodevelopmental defects and distinct nuclear shape abnormalities in neurons [J].
Coffinier, Catherine ;
Jung, Hea-Jin ;
Nobumori, Chika ;
Chang, Sandy ;
Tu, Yiping ;
Barnes, Richard H., II ;
Yoshinaga, Yuko ;
de Jong, Pieter J. ;
Vergnes, Laurent ;
Reue, Karen ;
Fong, Loren G. ;
Young, Stephen G. .
MOLECULAR BIOLOGY OF THE CELL, 2011, 22 (23) :4683-4693
[7]
Power-law rheology of isolated nuclei with deformation mapping of nuclear substructures [J].
Dahl, KN ;
Engler, AJ ;
Pajerowski, JD ;
Discher, DE .
BIOPHYSICAL JOURNAL, 2005, 89 (04) :2855-2864
[8]
Nuclear shape, mechanics, and mechanotransduction [J].
Dahl, Kris Noel ;
Ribeiro, Alexandre J. S. ;
Lammerding, Jan .
CIRCULATION RESEARCH, 2008, 102 (11) :1307-1318
[9]
Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin [J].
Dechat, Thomas ;
Pfleghaar, Katrin ;
Sengupta, Kaushik ;
Shimi, Takeshi ;
Shumaker, Dale K. ;
Solimando, Liliana ;
Goldman, Robert D. .
GENES & DEVELOPMENT, 2008, 22 (07) :832-853
[10]
Stresses at the cell-to-substrate interface during locomotion of fibroblasts [J].
Dembo, M ;
Wang, YL .
BIOPHYSICAL JOURNAL, 1999, 76 (04) :2307-2316