TY - JOUR
T1 - High stretchability, strength, and toughness of living cells enabled by hyperelastic vimentin intermediate filaments
AU - Hu, Jiliang
AU - Li, Yiwei
AU - Hao, Yukun
AU - Zheng, Tianqi
AU - Gupta, Satish K.
AU - Parada, German Alberto
AU - Wu, Huayin
AU - Lin, Shaoting
AU - Wang, Shida
AU - Zhao, Xuanhe
AU - Goldman, Robert D.
AU - Cai, Shengqiang
AU - Guo, Ming
N1 - Funding Information:
ACKNOWLEDGMENTS. We thank P. Ronceray, Y. Zheng, and the M.G. laboratory for helpful discussions. This work is supported by National Cancer Institute Grant 1U01CA202123. S.C. acknowledges support from Hellman Fellows Fund. H.W. and R.D.G. acknowledge the support from the National Institutes of Health (Grant 2P01GM096971-06A1).
Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.
PY - 2019/8/27
Y1 - 2019/8/27
N2 - In many developmental and pathological processes, including cellular migration during normal development and invasion in cancer metastasis, cells are required to withstand severe deformations. The structural integrity of eukaryotic cells under small deformations has been known to depend on the cytoskeleton including actin filaments (F-actin), microtubules (MT), and intermediate filaments (IFs). However, it remains unclear how cells resist severe deformations since both F-actin and microtubules yield or disassemble under moderate strains. Using vimentin containing IFs (VIFs) as a model for studying the large family of IF proteins, we demonstrate that they dominate cytoplasmic mechanics and maintain cell viability at large deformations. Our results show that cytoskeletal VIFs form a stretchable, hyperelastic network in living cells. This network works synergistically with other cytoplasmic components, substantially enhancing the strength, stretchability, resilience, and toughness of cells. Moreover, we find the hyperelastic VIF network, together with other quickly recoverable cytoskeletal components, forms a mechanically robust structure which can mechanically recover after damage.
AB - In many developmental and pathological processes, including cellular migration during normal development and invasion in cancer metastasis, cells are required to withstand severe deformations. The structural integrity of eukaryotic cells under small deformations has been known to depend on the cytoskeleton including actin filaments (F-actin), microtubules (MT), and intermediate filaments (IFs). However, it remains unclear how cells resist severe deformations since both F-actin and microtubules yield or disassemble under moderate strains. Using vimentin containing IFs (VIFs) as a model for studying the large family of IF proteins, we demonstrate that they dominate cytoplasmic mechanics and maintain cell viability at large deformations. Our results show that cytoskeletal VIFs form a stretchable, hyperelastic network in living cells. This network works synergistically with other cytoplasmic components, substantially enhancing the strength, stretchability, resilience, and toughness of cells. Moreover, we find the hyperelastic VIF network, together with other quickly recoverable cytoskeletal components, forms a mechanically robust structure which can mechanically recover after damage.
KW - Cell mechanics
KW - Cytoplasm
KW - Cytoskeleton
KW - Intermediate filament
KW - Vimentin
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U2 - 10.1073/pnas.1903890116
DO - 10.1073/pnas.1903890116
M3 - Article
C2 - 31409716
AN - SCOPUS:85071401763
SN - 0027-8424
VL - 116
SP - 17175
EP - 17180
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 35
ER -
