Compression Generated by a 3D Supracellular Actomyosin Cortex Promotes Embryonic Stem Cell Colony Growth and Expression of Nanog and Oct4

Jing Du; Yanlei Fan; Zheng Guo; Youguang Wang; Xu Zheng; Chong Huang; Baihui Liang; Lingyu Gao; Yanping Cao; Yunping Chen; Xi Zhang; Lei Li; Luping Xu; Congying Wu; David A Weitz; Xiqiao Feng

doi:10.1016/j.cels.2019.05.008

Compression Generated by a 3D Supracellular Actomyosin Cortex Promotes Embryonic Stem Cell Colony Growth and Expression of Nanog and Oct4

Cell Syst. 2019 Aug 28;9(2):214-220.e5. doi: 10.1016/j.cels.2019.05.008. Epub 2019 Jul 3.

Authors

Jing Du¹, Yanlei Fan², Zheng Guo³, Youguang Wang², Xu Zheng⁴, Chong Huang², Baihui Liang⁵, Lingyu Gao⁶, Yanping Cao², Yunping Chen², Xi Zhang³, Lei Li⁷, Luping Xu⁵, Congying Wu⁸, David A Weitz⁹, Xiqiao Feng¹⁰

Affiliations

¹ Institute of Biomechanics and Medical Engineering, Department of Mechanical Engineering, School of Aerospace, Tsinghua University, Beijing 100084, China; Key Laboratory for Biomechanics and Mechanobiology of Chinese Education Ministry, School of Biological Science and Medical Engineering, Beihang University, Beijing 100083, China; Beijing Advanced Innovation Centre for Biomedical Engineering, Beihang University, Beijing 102402, China. Electronic address: dringcin@126.com.
² Institute of Biomechanics and Medical Engineering, Department of Mechanical Engineering, School of Aerospace, Tsinghua University, Beijing 100084, China.
³ Key Laboratory for Biomechanics and Mechanobiology of Chinese Education Ministry, School of Biological Science and Medical Engineering, Beihang University, Beijing 100083, China; Beijing Advanced Innovation Centre for Biomedical Engineering, Beihang University, Beijing 102402, China.
⁴ State Key Laboratory of Nonlinear Mechanics, Beijing Key Laboratory of Engineered Construction and Mechanobiology, Institute of Mechanics, Chinese Academy of Sciences, Beijing 100190, China.
⁵ Center for Nano and Micro Mechanics, School of Aerospace Engineering, Tsinghua University, Beijing 100084, China.
⁶ Department of Physics, Tsinghua University, Beijing 100084, China.
⁷ State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
⁸ Institute of Systems Biomedicine, School of Basic Medical Sciences, Peking University Health Science Center, Beijing 100191, China.
⁹ Department of Physics and School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138, USA. Electronic address: weitz@seas.harvard.edu.
¹⁰ Institute of Biomechanics and Medical Engineering, Department of Mechanical Engineering, School of Aerospace, Tsinghua University, Beijing 100084, China. Electronic address: fengxq@tsinghua.edu.cn.

PMID: 31279504
DOI: 10.1016/j.cels.2019.05.008

Abstract

Mechanical factors play critical roles in mammalian development. Here, we report that colony-growing mouse embryonic stem cells (mESCs) generate significant tension on the colony surface through the contraction of a three-dimensional supracellular actomyosin cortex (3D-SAC). Disruption of the 3D-SAC, whose organization is dependent on the Rho/Rho-associated kinase (ROCK) signals and E-cadherin, results in mESC colony destruction. Reciprocally, compression force, which is generated by the 3D-SAC, promotes colony growth and expression of Nanog and Oct4 in mESCs and blastocyst development of mouse embryos. These findings suggest that autonomous cell forces regulate embryonic stem cells fate determination and provide insight regarding the biomechanical regulation of embryonic development.

Keywords: biomechanics; blastocyst development; compression force; mouse embryonic stem cells; supracellular actomyosin.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Actomyosin / metabolism
Animals
Biomechanical Phenomena
Blastomeres / cytology*
Blastomeres / metabolism
Cadherins / metabolism
Cell Differentiation
Cell Proliferation / physiology
Mice
Mouse Embryonic Stem Cells / cytology*
Mouse Embryonic Stem Cells / metabolism
Nanog Homeobox Protein / genetics
Nanog Homeobox Protein / metabolism*
Octamer Transcription Factor-3 / genetics
Octamer Transcription Factor-3 / metabolism*
Pluripotent Stem Cells / cytology
Pluripotent Stem Cells / metabolism
Primary Cell Culture
rho-Associated Kinases / metabolism

Substances

Cadherins
Nanog Homeobox Protein
Nanog protein, mouse
Octamer Transcription Factor-3
Pou5f1 protein, mouse
Actomyosin
rho-Associated Kinases