Cortical Tension Allocates the First Inner Cells of the Mammalian Embryo

Developmental Cell

Volumn 34, Issue 4, 2015, Pages 435-447

  Samarage, Chaminda R ^a   White, Melanie D ^a   Álvarez, Yanina D ^a   Fierro González, Juan Carlos ^a   Henon, Yann ^a   Jesudason, Edwin C ^b   Bissiere, Stephanie ^a,c   Fouras, Andreas ^a   Plachta, Nicolas ^a,c  

^a MONASH UNIVERSITY   (Australia)

^b NATIONAL HEALTH SERVICE   (United Kingdom)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; CADHERIN;

ANIMAL EXPERIMENT; ANISOTROPY; ARTICLE; BIOMECHANICS; CELL ADHESION; CELL FATE; CELL MEMBRANE; CELL SHAPE; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; EMBRYO DEVELOPMENT; FEMALE; IN VIVO STUDY; INNER CELL MASS; LASER SURGERY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ANIMAL; C57BL MOUSE; CELL COUNT; CELL FRACTIONATION; CELL LINEAGE; CYTOLOGY; DOWN REGULATION; HUMAN; METABOLISM; PHYSIOLOGY;

MAMMALIA;

ANIMALS; BIOMECHANICAL PHENOMENA; BLASTOCYST INNER CELL MASS; CADHERINS; CELL ADHESION; CELL COUNT; CELL LINEAGE; DOWN-REGULATION; FEMALE; HUMANS; MICE, INBRED C57BL; MYOSIN TYPE II; SUBCELLULAR FRACTIONS;

EID: 84939811028     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.07.004     Document Type: Article

References (51)

1. Anani S., Bhat S., Honma-Yamanaka N., Krawchuk D., Yamanaka Y. Initiation of Hippo signaling is linked to polarity rather than to cell position in the pre-implantation mouse embryo. Development 2014, 141:2813-2824.
2. Avilion A.A., Nicolis S.K., Pevny L.H., Perez L., Vivian N., Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 2003, 17:126-140.
3. Behrndt M., Salbreux G., Campinho P., Hauschild R., Oswald F., Roensch J., Grill S.W., Heisenberg C.P. Forces driving epithelial spreading in zebrafish gastrulation. Science 2012, 338:257-260.
4. Bender C. Bestimmung der grössten Anzahl gleich Kugeln, welche sich auf eine Kugel von demselben Radius, wie die übrigen, auflegen lassen. Archiv. Math. Physik (Grunert) 1874, 56:302-306.
5. Dard N., Louvet-Vallée S., Maro B. Orientation of mitotic spindles during the 8- to 16-cell stage transition in mouse embryos. PLoS ONE 2009, 4:e8171.
6. Duan X., Chen K.L., Zhang Y., Cui X.S., Kim N.H., Sun S.C. ROCK inhibition prevents early mouse embryo development. Histochem. Cell Biol. 2014, 142:227-233.
7. Fagotto F. The cellular basis of tissue separation. Development 2014, 141:3303-3318.
8. Fernandez-Gonzalez R., Simoes Sde.M., Röper J.C., Eaton S., Zallen J.A. Myosin II dynamics are regulated by tension in intercalating cells. Dev. Cell 2009, 17:736-743.
9. Fierro-González J.C., White M.D., Silva J.C., Plachta N. Cadherin-dependent filopodia control preimplantation embryo compaction. Nat. Cell Biol. 2013, 15:1424-1433.
10. Fujita M., Onami S. Cell-to-cell heterogeneity in cortical tension specifies curvature of contact surfaces in Caenorhabditis elegans embryos. PLoS ONE 2012, 7:e30224.
11. Gelbart M.A., He B., Martin A.C., Thiberge S.Y., Wieschaus E.F., Kaschube M. Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis. Proc. Natl. Acad. Sci. USA 2012, 109:19298-19303.
12. Grill S.W. Growing up is stressful: biophysical laws of morphogenesis. Curr. Opin. Genet. Dev. 2011, 21:647-652.
13. Heisenberg C.P., Bellaïche Y. Forces in tissue morphogenesis and patterning. Cell 2013, 153:948-962.
14. Jedrusik A., Parfitt D.E., Guo G., Skamagki M., Grabarek J.B., Johnson M.H., Robson P., Zernicka-Goetz M. Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo. Genes Dev. 2008, 22:2692-2706.
15. Johnson M.H., Ziomek C.A. The foundation of two distinct cell lineages within the mouse morula. Cell 1981, 24:71-80.
16. Johnson M.H., Maro B., Takeichi M. The role of cell adhesion in the synchronization and orientation of polarization in 8-cell mouse blastomeres. J. Embryol. Exp. Morphol. 1986, 93:239-255.
17. Kaur G., Costa M.W., Nefzger C.M., Silva J., Fierro-González J.C., Polo J.M., Bell T.D., Plachta N. Probing transcription factor diffusion dynamics in the living mammalian embryo with photoactivatable fluorescence correlation spectroscopy. Nat. Commun. 2013, 4:1637.
18. Kiehart D.P., Galbraith C.G., Edwards K.A., Rickoll W.L., Montague R.A. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 2000, 149:471-490.
19. Kim J.H., Ren Y., Ng W.P., Li S., Son S., Kee Y.S., Zhang S., Zhang G., Fletcher D.A., Robinson D.N., Chen E.H. Mechanical tension drives cell membrane fusion. Dev. Cell 2015, 32:561-573.
20. Kimber S.J., Surani M.A., Barton S.C. Interactions of blastomeres suggest changes in cell surface adhesiveness during the formation of inner cell mass and trophectoderm in the preimplantation mouse embryo. J. Embryol. Exp. Morphol. 1982, 70:133-152.
21. Krieg M., Arboleda-Estudillo Y., Puech P.H., Käfer J., Graner F., Müller D.J., Heisenberg C.P. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 2008, 10:429-436.
22. Laeno A.M., Tamashiro D.A., Alarcon V.B. Rho-associated kinase activity is required for proper morphogenesis of the inner cell mass in the mouse blastocyst. Biol. Reprod. 2013, 89:122.
23. Lassen B., van Rikxoort E.M., Schmidt M., Kerkstra S., van Ginneken B., Kuhnigk J.M. Automatic segmentation of the pulmonary lobes from chest CT scans based on fissures, vessels, and bronchi. IEEE Trans. Med. Imaging 2013, 32:210-222.
24. Lecuit T., Lenne P.F. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 2007, 8:633-644.
25. Lecuit T., Lenne P.F., Munro E. Force generation, transmission, and integration during cell and tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 2011, 27:157-184.
26. Maître J.L., Berthoumieux H., Krens S.F., Salbreux G., Jülicher F., Paluch E., Heisenberg C.P. Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 2012, 338:253-256.
27. Martin A.C., Goldstein B. Apical constriction: themes and variations on a cellular mechanism driving morphogenesis. Development 2014, 141:1987-1998.
28. Mayer M., Depken M., Bois J.S., Jülicher F., Grill S.W. Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 2010, 467:617-621.
29. McDole K., Xiong Y., Iglesias P.A., Zheng Y. Lineage mapping the pre-implantation mouse embryo by two-photon microscopy, new insights into the segregation of cell fates. Dev. Biol. 2011, 355:239-249.
30. Morris S.A., Teo R.T., Li H., Robson P., Glover D.M., Zernicka-Goetz M. Origin and formation of the first two distinct cell types of the inner cell mass in the mouse embryo. Proc. Natl. Acad. Sci. USA 2010, 107:6364-6369.
31. Newton I. Mathematical Principles of Natural Philosophy 1846, Daniel Adee, New York.
32. Plachta N., Bollenbach T., Pease S., Fraser S.E., Pantazis P. Oct4 kinetics predict cell lineage patterning in the early mammalian embryo. Nat. Cell Biol. 2011, 13:117-123.
33. Plusa B., Frankenberg S., Chalmers A., Hadjantonakis A.K., Moore C.A., Papalopulu N., Papaioannou V.E., Glover D.M., Zernicka-Goetz M. Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo. J. Cell Sci. 2005, 118:505-515.
34. Porazinski S., Wang H., Asaoka Y., Behrndt M., Miyamoto T., Morita H., Hata S., Sasaki T., Krens S.F., Osada Y., et al. YAP is essential for tissue tension to ensure vertebrate 3D body shape. Nature 2015, 521:217-221.
35. Rauzi M., Lenne P.F. Cortical forces in cell shape changes and tissue morphogenesis. Curr. Top. Dev. Biol. 2011, 95:93-144.
36. Rauzi M., Verant P., Lecuit T., Lenne P.F. Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat. Cell Biol. 2008, 10:1401-1410.
37. Rossant J., Tam P.P. Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 2009, 136:701-713.
38. Samarage C.R., Carberry J., Sheard G.J., Fouras A. Polynomial Element Velocimetry (PEV): A technique for continuous in-plane velocity and velocity gradient measurements for low Reynolds number flows. Meas. Sci. Technol. 2012, 23:105304.
39. Shamonin D.P., Staring M., Bakker E., Xiao C., Stolk J., Reiber J.H.C. Automatic lung lobe segmentation of COPD patients using iterative B-spline fitting. Proc. S.P.I.E. 2012, 8314:83140W.
40. Steinberg M.S. Differential adhesion in morphogenesis: a modern view. Curr. Opin. Genet. Dev. 2007, 17:281-286.
41. Stephenson R.O., Yamanaka Y., Rossant J. Disorganized epithelial polarity and excess trophectoderm cell fate in preimplantation embryos lacking E-cadherin. Development 2010, 137:3383-3391.
42. Strumpf D., Mao C.A., Yamanaka Y., Ralston A., Chawengsaksophak K., Beck F., Rossant J. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 2005, 132:2093-2102.
43. Torres-Padilla M.E., Parfitt D.E., Kouzarides T., Zernicka-Goetz M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 2007, 445:214-218.
44. Wadell H. Volume, shape and roundness of rock particles. J. Geol. 1932, 40:443-451.
45. Watanabe T., Biggins J.S., Tannan N.B., Srinivas S. Limited predictive value of blastomere angle of division in trophectoderm and inner cell mass specification. Development 2014, 141:2279-2288.
46. Wennekamp S., Mesecke S., Nédélec F., Hiiragi T. A self-organization framework for symmetry breaking in the mammalian embryo. Nat. Rev. Mol. Cell Biol. 2013, 14:452-459.
47. Xiong F., Ma W., Hiscock T.W., Mosaliganti K.R., Tentner A.R., Brakke K.A., Rannou N., Gelas A., Souhait L., Swinburne I.A., et al. Interplay of cell shape and division orientation promotes robust morphogenesis of developing epithelia. Cell 2014, 159:415-427.
48. Yamanaka Y., Ralston A., Stephenson R.O., Rossant J. Cell and molecular regulation of the mouse blastocyst. Dev. Dyn. 2006, 235:2301-2314.
49. Yamanaka Y., Lanner F., Rossant J. FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 2010, 137:715-724.
50. Yoshida S., Barbier de Reuille P., Lane B., Bassel G.W., Prusinkiewicz P., Smith R.S., Weijers D. Genetic control of plant development by overriding a geometric division rule. Dev. Cell 2014, 29:75-87.
51. Zernicka-Goetz M., Morris S.A., Bruce A.W. Making a firm decision: multifaceted regulation of cell fate in the early mouse embryo. Nat. Rev. Genet. 2009, 10:467-477.