Cortical Tension Allocates the First Inner Cells of the Mammalian Embryo.
Every cell in our body originates from the pluripotent inner mass of the embryo, yet it is unknown how biomechanical forces allocate inner cells in vivo. Here we discover subcellular heterogeneities in tensile forces, generated by actomyosin cortical networks, which drive apical constriction to position the first inner cells of living mouse embryos. Myosin II accumulates specifically around constricting cells, and its disruption dysregulates constriction and cell fate. Laser ablations of actomyosin networks reveal that constricting cells have higher cortical tension, generate tension anisotropies and morphological changes in adjacent regions of neighboring cells, and require their neighbors to coordinate their own changes in shape. Thus, tensile forces determine the first spatial segregation of cells during mammalian development. We propose that, unlike more cohesive tissues, the early embryo dissipates tensile forces required by constricting cells via their neighbors, thereby allowing confined cell repositioning without jeopardizing global architecture.
Laboratory for Dynamic Imaging, Faculty of Engineering, Monash University, Clayton Campus, Melbourne, VIC 3800, Australia.
Chaminda R
CR
Samarage
EMBL Australia, ARMI, Monash University, Clayton Campus, Melbourne, VIC 3800, Australia.
Melanie D
MD
White
EMBL Australia, ARMI, Monash University, Clayton Campus, Melbourne, VIC 3800, Australia.
Yanina D
YD
Álvarez
EMBL Australia, ARMI, Monash University, Clayton Campus, Melbourne, VIC 3800, Australia.
Juan Carlos
JC
Fierro-González
Laboratory for Dynamic Imaging, Faculty of Engineering, Monash University, Clayton Campus, Melbourne, VIC 3800, Australia.
Yann
Y
Henon
National Health Service, Edinburgh, Scotland EH1 3EG, UK.
Edwin C
EC
Jesudason
EMBL Australia, ARMI, Monash University, Clayton Campus, Melbourne, VIC 3800, Australia; Institute of Molecular and Cell Biology, A(∗)STAR, 61 Biopolis Drive, Singapore 138673, Singapore.
Stephanie
S
Bissiere
Laboratory for Dynamic Imaging, Faculty of Engineering, Monash University, Clayton Campus, Melbourne, VIC 3800, Australia. Electronic address: andreas.fouras@monash.edu.
Andreas
A
Fouras
EMBL Australia, ARMI, Monash University, Clayton Campus, Melbourne, VIC 3800, Australia; Institute of Molecular and Cell Biology, A(∗)STAR, 61 Biopolis Drive, Singapore 138673, Singapore. Electronic address: plachtan@imcb.a-star.edu.sg.
Nicolas
N
Plachta
D000818:Animals; D001696:Biomechanical Phenomena; D053624:Blastocyst Inner Cell Mass / Q000166:cytology* / Q000502:physiology*; D015820:Cadherins / Q000378:metabolism; D002448:Cell Adhesion; D002452:Cell Count; D019070:Cell Lineage; D015536:Down-Regulation; D005260:Female; D006801:Humans; D008810:Mice, Inbred C57BL; D024462:Myosin Type II / Q000378:metabolism; D013347:Subcellular Fractions / Q000378:metabolism
D015820:Cadherins; D024462:Myosin Type II