1932

Abstract

Embryonic development is a dynamic process orchestrated by a delicate interplay of biochemical and biophysical factors. While the role of genetics and biochemistry in embryogenesis has been extensively studied, recent research has highlighted the significance of mechanical regulation in shaping and guiding this intricate process. Here, we provide an overview of the current understanding of the mechanical regulation of embryo development. We explore how mechanical forces generated by cells and tissues play a crucial role in driving the development of different stages. We examine key morphogenetic processes such as compaction, blastocyst formation, implantation, and egg cylinder formation, and discuss the mechanical mechanisms and cues involved. By synthesizing the current body of literature, we highlight the emerging concepts and open questions in the field of mechanical regulation. We aim to provide an overview of the field, inspiring future investigations and fostering a deeper understanding of the mechanical aspects of embryo development.

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2024-10-02
2025-02-18
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Literature Cited

  1. Abbas Y, Carnicer-Lombarte A, Gardner L, Thomas J, Brosens JJ, et al. 2019.. Tissue stiffness at the human maternal–fetal interface. . Hum. Reprod. 34:(10):19992008
    [Crossref] [Google Scholar]
  2. Aguilera-Castrejon A, Oldak B, Shani T, Ghanem N, Itzkovich C, et al. 2021.. Ex utero mouse embryogenesis from pre-gastrulation to late organogenesis. . Nature 593:(7857):11924
    [Crossref] [Google Scholar]
  3. Ajduk A, Shivhare SB, Zernicka-Goetz M. 2014.. The basal position of nuclei is one pre-requisite for asymmetric cell divisions in the early mouse embryo. . Dev. Biol. 392:(2):13340
    [Crossref] [Google Scholar]
  4. Alarcón VB, Marikawa Y. 2005.. Unbiased contribution of the first two blastomeres to mouse blastocyst development. . Mol. Reprod. Dev. 72:(3):35461
    [Crossref] [Google Scholar]
  5. Almonacid M, Terret M-É, Verlhac M-H. 2014.. Actin-based spindle positioning: new insights from female gametes. . J. Cell Sci. 127:(3):47783
    [Google Scholar]
  6. Anani S, Bhat S, Honma-Yamanaka N, Krawchuk D, Yamanaka Y. 2014.. Initiation of Hippo signaling is linked to polarity rather than to cell position in the pre-implantation mouse embryo. . Development 141:(14):281324
    [Crossref] [Google Scholar]
  7. Anderson DC, Gill JS, Cinalli RM, Nance J. 2008.. Polarization of the C. elegans embryo by RhoGAP-mediated exclusion of PAR-6 from cell contacts. . Science 320:(5884):177174
    [Crossref] [Google Scholar]
  8. Aufschnaiter R, Zamir EA, Little CD, Özbek S, Münder S, et al. 2011.. In vivo imaging of basement membrane movement: ECM patterning shapes Hydra polyps. . J. Cell Sci. 124:(23):402738
    [Crossref] [Google Scholar]
  9. Balbín M, Fueyo A, Knäuper V, López JM, Álvarez J, et al. 2001.. Identification and enzymatic characterization of two diverging murine counterparts of human interstitial collagenase (MMP-1) expressed at sites of embryo implantation. . J. Biol. Chem. 276:(13):1025362
    [Crossref] [Google Scholar]
  10. Bao M, Cornwall-Scoones J, Sanchez-Vasquez E, Cox AL, Chen D-Y, et al. 2022a.. Stem cell-derived synthetic embryos self-assemble by exploiting cadherin codes and cortical tension. . Nat. Cell Biol. 24:(9):134149
    [Crossref] [Google Scholar]
  11. Bao M, Cornwall-Scoones J, Zernicka-Goetz M. 2022b.. Stem-cell-based human and mouse embryo models. . Curr. Opin. Genet. Dev. 76::101970
    [Crossref] [Google Scholar]
  12. Bao M, Xie J, Katoele N, Hu X, Wang B, et al. 2018.. Cellular volume and matrix stiffness direct stem cell behavior in a 3D microniche. . ACS Appl. Mater. Interfaces 11:(2):175459
    [Crossref] [Google Scholar]
  13. Bao M, Xie J, Piruska A, Huck WTS. 2017.. 3D microniches reveal the importance of cell size and shape. . Nat. Commun. 8:(1):1962
    [Crossref] [Google Scholar]
  14. Bischof P, Irminger-Finger I. 2005.. The human cytotrophoblastic cell, a mononuclear chameleon. . Int. J. Biochem. Cell Biol. 37:(1):116
    [Crossref] [Google Scholar]
  15. Boden A, Pennacchietti F, Coceano G, Damenti M, Ratz M, Testa I. 2021.. Volumetric live cell imaging with three-dimensional parallelized RESOLFT microscopy. . Nat. Biotechnol. 39:(5):60918
    [Crossref] [Google Scholar]
  16. Borsos M, Perricone SM, Schauer T, Pontabry J, De Luca KL, et al. 2019.. Genome–lamina interactions are established de novo in the early mouse embryo. . Nature 569:(7758):72933
    [Crossref] [Google Scholar]
  17. Brodland GW. 2002.. The differential interfacial tension hypothesis (DITH): a comprehensive theory for the self-rearrangement of embryonic cells and tissues. . J. Biomech. Eng. 124:(2):18897
    [Crossref] [Google Scholar]
  18. Bruce AW, Zernicka-Goetz M. 2010.. Developmental control of the early mammalian embryo: competition among heterogeneous cells that biases cell fate. . Curr. Opin. Genet. Dev. 20:(5):48591
    [Crossref] [Google Scholar]
  19. Câmara DR, Kastelic JP, Thundathil JC. 2017.. Role of the Na+/K+-ATPase ion pump in male reproduction and embryo development. . Reprod. Fertil. Dev. 29:(8):145767
    [Crossref] [Google Scholar]
  20. Chazaud C, Yamanaka Y, Pawson T, Rossant J. 2006.. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. . Dev. Cell 10:(5):61524
    [Crossref] [Google Scholar]
  21. Chen Q, Shi J, Tao Y, Zernicka-Goetz M. 2018.. Tracing the origin of heterogeneity and symmetry breaking in the early mammalian embryo. . Nat. Commun. 9:(1):1819
    [Crossref] [Google Scholar]
  22. Chlasta J, Milani P, Runel G, Duteyrat JL, Arias L, et al. 2017.. Variations in basement membrane mechanics are linked to epithelial morphogenesis. . Development 144:(23):435062
    [Google Scholar]
  23. Christodoulou N, Weberling A, Strathdee D, Anderson KI, Timpson P, Zernicka-Goetz M. 2019.. Morphogenesis of extra-embryonic tissues directs the remodelling of the mouse embryo at implantation. . Nat. Commun. 10:(1):3557
    [Crossref] [Google Scholar]
  24. Cockburn K, Biechele S, Garner J, Rossant J. 2013.. The Hippo pathway member Nf2 is required for inner cell mass specification. . Curr. Biol. 23:(13):1195201
    [Crossref] [Google Scholar]
  25. Cockburn K, Rossant J. 2010.. Making the blastocyst: lessons from the mouse. . J. Clin. Investig. 120:(4):9951003
    [Crossref] [Google Scholar]
  26. Cornwall-Scoones J, Zernicka-Goetz M. 2021.. Unifying synthetic embryology. . Dev. Biol. 474::14
    [Crossref] [Google Scholar]
  27. Cowan CR, Hyman AA. 2004.. Asymmetric cell division in C. elegans: cortical polarity and spindle positioning. . Annu. Rev. Cell Dev. Biol. 20::42753
    [Crossref] [Google Scholar]
  28. Crest J, Diz-Munoz A, Chen D-Y, Fletcher DA, Bilder D. 2017.. Organ sculpting by patterned extracellular matrix stiffness. . eLife 6::e24958
    [Crossref] [Google Scholar]
  29. Crisp M, Liu Q, Roux K, Rattner J, Shanahan C, et al. 2006.. Coupling of the nucleus and cytoplasm: role of the LINC complex. . J. Cell Biol. 172:(1):4153
    [Crossref] [Google Scholar]
  30. Cuman C, Menkhorst E, Winship A, Van Sinderen M, Osianlis T, et al. 2014.. Fetal–maternal communication: the role of Notch signalling in embryo implantation. . Reproduction 147:(3):R7586
    [Crossref] [Google Scholar]
  31. Daley WP, Yamada KM. 2013.. ECM-modulated cellular dynamics as a driving force for tissue morphogenesis. . Curr. Opin. Genet. Dev. 23:(4):40814
    [Crossref] [Google Scholar]
  32. Den Z, Cheng X, Merched-Sauvage M, Koch PJ. 2006.. Desmocollin 3 is required for pre-implantation development of the mouse embryo. . J. Cell Sci. 119:(3):48289
    [Crossref] [Google Scholar]
  33. Dumortier JG, Le Verge-Serandour M, Tortorelli AF, Mielke A, De Plater L, et al. 2019.. Hydraulic fracturing and active coarsening position the lumen of the mouse blastocyst. . Science 365:(6452):46568
    [Crossref] [Google Scholar]
  34. Ebnet K. 2017.. Junctional adhesion molecules (JAMs): cell adhesion receptors with pleiotropic functions in cell physiology and development. . Physiol. Rev. 97::152954
    [Crossref] [Google Scholar]
  35. Fierro-González JC, White MD, Silva JC, Plachta N. 2013.. Cadherin-dependent filopodia control preimplantation embryo compaction. . Nat. Cell Biol. 15:(12):142433
    [Crossref] [Google Scholar]
  36. Foty RA, Steinberg MS. 2005.. The differential adhesion hypothesis: a direct evaluation. . Dev. Biol. 278:(1):25563
    [Crossref] [Google Scholar]
  37. Goldman RD, Gruenbaum Y, Moir RD, Shumaker DK, Spann TP. 2002.. Nuclear lamins: building blocks of nuclear architecture. . Genes Dev. 16:(5):53347
    [Crossref] [Google Scholar]
  38. Goolam M, Scialdone A, Graham SJ, Macaulay IC, Jedrusik A, et al. 2016.. Heterogeneity in Oct4 and Sox2 targets biases cell fate in 4-cell mouse embryos. . Cell 165:(1):6174
    [Crossref] [Google Scholar]
  39. Guo G, Huss M, Tong GQ, Wang C, Sun LL, et al. 2010.. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. . Dev. Cell 18:(4):67585
    [Crossref] [Google Scholar]
  40. Guo M, Pegoraro AF, Mao A, Zhou EH, Arany PR, et al. 2017.. Cell volume change through water efflux impacts cell stiffness and stem cell fate. . PNAS 114:(41):E861827
    [Google Scholar]
  41. Haigo SL, Bilder D. 2011.. Global tissue revolutions in a morphogenetic movement controlling elongation. . Science 331:(6020):107174
    [Crossref] [Google Scholar]
  42. Halfter W, Oertle P, Monnier CA, Camenzind L, Reyes-Lua M, et al. 2015.. New concepts in basement membrane biology. . FEBS J. 282:(23):446679
    [Crossref] [Google Scholar]
  43. Harris AK. 1976.. Is cell sorting caused by differences in the work of intercellular adhesion? A critique of the Steinberg hypothesis. . J. Theor. Biol. 61:(2):26785
    [Crossref] [Google Scholar]
  44. Hemberger M, Hanna CW, Dean W. 2020.. Mechanisms of early placental development in mouse and humans. . Nat. Rev. Genet. 21:(1):2743
    [Crossref] [Google Scholar]
  45. Hiiragi T, Solter D. 2004.. First cleavage plane of the mouse egg is not predetermined but defined by the topology of the two apposing pronuclei. . Nature 430:(6997):36064
    [Crossref] [Google Scholar]
  46. Hirate Y, Hirahara S, Inoue K-I, Suzuki A, Alarcon VB, et al. 2013.. Polarity-dependent distribution of angiomotin localizes Hippo signaling in preimplantation embryos. . Curr. Biol. 23:(13):118194
    [Crossref] [Google Scholar]
  47. Houghton FD, Humpherson PG, Hawkhead JA, Hall CJ, Leese HJ. 2003.. Na+, K+, ATPase activity in the human and bovine preimplantation embryo. . Dev. Biol. 263:(2):36066
    [Crossref] [Google Scholar]
  48. Hu D, Cross JC. 2009.. Development and function of trophoblast giant cells in the rodent placenta. . Int. J. Dev. Biol. 54:(2–3):34154
    [Google Scholar]
  49. Huang Q, Cohen MA, Alsina FC, Devlin G, Garrett A, et al. 2020.. Intravital imaging of mouse embryos. . Science 368:(6487):18186
    [Crossref] [Google Scholar]
  50. Johnson M, Ziomek C. 1981a.. Induction of polarity in mouse 8-cell blastomeres: specificity, geometry, and stability. . J. Cell Biol. 91:(1):3038
    [Crossref] [Google Scholar]
  51. Johnson MH, Ziomek CA. 1981b.. The foundation of two distinct cell lineages within the mouse morula. . Cell 24:(1):7180
    [Crossref] [Google Scholar]
  52. Kabukçu C, Çabuş Ü, Öztekin Ö, Fenkçi V. 2021.. The strain rate of endometrium measured by real-time sonoelastography as a predictive marker for pregnancy in gonadotropin stimulated intrauterine insemination cycles. . J. Obstet. Gynaecol. Res. 47:(10):356170
    [Crossref] [Google Scholar]
  53. Kang M, Garg V, Hadjantonakis A-K. 2017.. Lineage establishment and progression within the inner cell mass of the mouse blastocyst requires FGFR1 and FGFR2. . Dev. Cell 41:(5):496510.e5
    [Crossref] [Google Scholar]
  54. Käs J, Strey H, Sackmann E. 1994.. Direct imaging of reptation for semiflexible actin filaments. . Nature 368:(6468):22629
    [Crossref] [Google Scholar]
  55. Kim J, Gye MC, Kim MK. 2004.. Role of occludin, a tight junction protein, in blastocoel formation, and in the paracellular permeability and differentiation of trophectoderm in preimplantation mouse embryos. . Mol. Cells 17:(2):24854
    [Crossref] [Google Scholar]
  56. Knoblich JA. 2010.. Asymmetric cell division: recent developments and their implications for tumour biology. . Nat. Rev. Mol. Cell Biol. 11:(12):84960
    [Crossref] [Google Scholar]
  57. Korotkevich E, Niwayama R, Courtois A, Friese S, Berger N, et al. 2017.. The apical domain is required and sufficient for the first lineage segregation in the mouse embryo. . Dev. Cell 40:(3):23547.e7
    [Crossref] [Google Scholar]
  58. Krawchuk D, Honma-Yamanaka N, Anani S, Yamanaka Y. 2013.. FGF4 is a limiting factor controlling the proportions of primitive endoderm and epiblast in the ICM of the mouse blastocyst. . Dev. Biol. 384:(1):6571
    [Crossref] [Google Scholar]
  59. Krieg M, Arboleda-Estudillo Y, Puech P-H, Käfer J, Graner F, et al. 2008.. Tensile forces govern germ-layer organization in zebrafish. . Nat. Cell Biol. 10:(4):42936
    [Crossref] [Google Scholar]
  60. Kyprianou C, Christodoulou N, Hamilton RS, Nahaboo W, Boomgaard DS, et al. 2020.. Basement membrane remodelling regulates mouse embryogenesis. . Nature 582:(7811):25358
    [Crossref] [Google Scholar]
  61. Lanner F, Rossant J. 2010.. The role of FGF/Erk signaling in pluripotent cells. . Development 137:(20):335160
    [Crossref] [Google Scholar]
  62. Lecuit T, Lenne P-F. 2007.. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. . Nat. Rev. Mol. Cell Biol. 8:(8):63344
    [Crossref] [Google Scholar]
  63. Lessey BA, Young SL. 2014.. Homeostasis imbalance in the endometrium of women with implantation defects: the role of estrogen and progesterone. . Semin. Reprod. Med. 32:(5):36575
    [Crossref] [Google Scholar]
  64. Leung CL, Green KJ, Liem RK. 2002.. Plakins: a family of versatile cytolinker proteins. . Trends Cell Biol. 12:(1):3745
    [Crossref] [Google Scholar]
  65. Leung CY, Zernicka-Goetz M. 2013.. Angiomotin prevents pluripotent lineage differentiation in mouse embryos via Hippo pathway-dependent and-independent mechanisms. . Nat. Commun. 4:(1):2251
    [Crossref] [Google Scholar]
  66. Leung CY, Zernicka-Goetz M. 2015.. Mapping the journey from totipotency to lineage specification in the mouse embryo. . Curr. Opin. Genet. Dev. 34::7176
    [Crossref] [Google Scholar]
  67. Lim HYG, Alvarez YD, Gasnier M, Wang Y, Tetlak P, et al. 2020.. Keratins are asymmetrically inherited fate determinants in the mammalian embryo. . Nature 585:(7825):4049
    [Crossref] [Google Scholar]
  68. Lim HYG, Plachta N. 2021.. Cytoskeletal control of early mammalian development. . Nat. Rev. Mol. Cell Biol. 22:(8):54862
    [Crossref] [Google Scholar]
  69. Maître J-L, Niwayama R, Turlier H, Nédélec F, Hiiragi T. 2015.. Pulsatile cell-autonomous contractility drives compaction in the mouse embryo. . Nat. Cell Biol. 17:(7):84955
    [Crossref] [Google Scholar]
  70. Maître J-L, Turlier H, Illukkumbura R, Eismann B, Niwayama R, et al. 2016.. Asymmetric division of contractile domains couples cell positioning and fate specification. . Nature 536:(7616):34448
    [Crossref] [Google Scholar]
  71. Mammoto A, Ingber DE. 2009.. Cytoskeletal control of growth and cell fate switching. . Curr. Opin. Cell Biol. 21:(6):86470
    [Crossref] [Google Scholar]
  72. Marx V. 2019.. A dream of single-cell proteomics. . Nat. Methods 16:(9):80912
    [Crossref] [Google Scholar]
  73. Mintz B. 1965.. Experimental genetic mosaicism in the mouse. . In Ciba Foundation Symposium - Preimplantation Stages of Pregnancy, ed. GEW Wolstenholme, M O'Connor , pp. 194216. London:: JA Churchill
    [Google Scholar]
  74. Mistri TK, Arindrarto W, Ng WP, Wang C, Lim LH, et al. 2018.. Dynamic changes in Sox2 spatio-temporal expression promote the second cell fate decision through Fgf4/Fgfr2 signaling in preimplantation mouse embryos. . Biochem. J. 475:(6):107589
    [Crossref] [Google Scholar]
  75. Mohamed OA, Jonnaert M, Labelle-Dumais C, Kuroda K, Clarke HJ, Dufort D. 2005.. Uterine Wnt/β-catenin signaling is required for implantation. . PNAS 102:(24):857984
    [Crossref] [Google Scholar]
  76. Molè MA, Weberling A, Zernicka-Goetz M. 2020.. Comparative analysis of human and mouse development: from zygote to pre-gastrulation. . Curr. Topics Dev. Biol. 136::11338
    [Crossref] [Google Scholar]
  77. Molotkov A, Mazot P, Brewer JR, Cinalli RM, Soriano P. 2017.. Distinct requirements for FGFR1 and FGFR2 in primitive endoderm development and exit from pluripotency. . Dev. Cell 41:(5):51126.e4
    [Crossref] [Google Scholar]
  78. Morrissey MA, Sherwood DR. 2015.. An active role for basement membrane assembly and modification in tissue sculpting. . J. Cell Sci. 128:(9):166168
    [Google Scholar]
  79. Motosugi N, Bauer T, Polanski Z, Solter D, Hiiragi T. 2005.. Polarity of the mouse embryo is established at blastocyst and is not prepatterned. . Genes Dev. 19:(9):108192
    [Crossref] [Google Scholar]
  80. Nelson CM. 2022.. Mechanical control of cell differentiation: insights from the early embryo. . Annu. Rev. Biomed. Eng. 24::30722
    [Crossref] [Google Scholar]
  81. Nishioka N, Inoue K-I, Adachi K, Kiyonari H, Ota M, et al. 2009.. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. . Dev. Cell 16:(3):398410
    [Crossref] [Google Scholar]
  82. Nishioka N, Yamamoto S, Kiyonari H, Sato H, Sawada A, et al. 2008.. Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. . Mech. Dev. 125:(3–4):27083
    [Crossref] [Google Scholar]
  83. Nissen SB, Perera M, Gonzalez JM, Morgani SM, Jensen MH, et al. 2017.. Four simple rules that are sufficient to generate the mammalian blastocyst. . PLOS Biol. 15:(7):e2000737
    [Crossref] [Google Scholar]
  84. Ohnishi Y, Huber W, Tsumura A, Kang M, Xenopoulos P, et al. 2014.. Cell-to-cell expression variability followed by signal reinforcement progressively segregates early mouse lineages. . Nat. Cell Biol. 16:(1):2737
    [Crossref] [Google Scholar]
  85. Pan-Castillo B, Gazze SA, Thomas S, Lucas C, Margarit L, et al. 2018.. Morphophysical dynamics of human endometrial cells during decidualization. . Nanomedicine: Nanotechnol. Biol. Med. 14:(7):223545
    [Crossref] [Google Scholar]
  86. Papaspyropoulos A, Bradley L, Thapa A, Leung CY, Toskas K, et al. 2018.. RASSF1A uncouples Wnt from Hippo signalling and promotes YAP mediated differentiation via p73. . Nat. Commun. 9:(1):424
    [Crossref] [Google Scholar]
  87. Park JY, Mani S, Clair G, Olson HM, Paurus VL, et al. 2022.. A microphysiological model of human trophoblast invasion during implantation. . Nat. Commun. 13:(1):1252
    [Crossref] [Google Scholar]
  88. Paulin D, Babinet C, Weber K, Osborn M. 1980.. Antibodies as probes of cellular differentiation and cytoskeletal organization in the mouse blastocyst. . Exp. Cell Res. 130:(2):297304
    [Crossref] [Google Scholar]
  89. Plusa B, Frankenberg S, Chalmers A, Hadjantonakis A-K, Moore CA, et al. 2005.. Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo. . J. Cell Sci. 118:(3):50515
    [Crossref] [Google Scholar]
  90. Posfai E, Petropoulos S, De Barros FRO, Schell JP, Jurisica I, et al. 2017.. Position- and Hippo signaling-dependent plasticity during lineage segregation in the early mouse embryo. . eLife 6::e22906
    [Crossref] [Google Scholar]
  91. Röper K, Gregory SL, Brown NH. 2002.. The ‘Spectraplakins’: cytoskeletal giants with characteristics of both spectrin and plakin families. . J. Cell Sci. 115:(22):421525
    [Crossref] [Google Scholar]
  92. Rosado-Olivieri EA, Brivanlou AH. 2021.. Synthetic by design: exploiting tissue self-organization to explore early human embryology. . Dev. Biol. 474::1621
    [Crossref] [Google Scholar]
  93. Ruane PT, Garner T, Parsons L, Babbington PA, Wangsaputra I, et al. 2022.. Trophectoderm differentiation to invasive syncytiotrophoblast is promoted by endometrial epithelial cells during human embryo implantation. . Hum. Reprod. 37:(4):77792
    [Crossref] [Google Scholar]
  94. Ryan AQ, Chan CJ, Graner F, Hiiragi T. 2019.. Lumen expansion facilitates epiblast-primitive endoderm fate specification during mouse blastocyst formation. . Dev. Cell 51:(6):68497.e4
    [Crossref] [Google Scholar]
  95. Samarage CR, White MD, Álvarez YD, Fierro-González JC, Henon Y, et al. 2015.. Cortical tension allocates the first inner cells of the mammalian embryo. . Dev. Cell 34:(4):43547
    [Crossref] [Google Scholar]
  96. Saraswathibhatla A, Indana D, Chaudhuri O. 2023.. Cell–extracellular matrix mechanotransduction in 3D. . Nat. Rev. Mol. Cell Biol. 24::495516
    [Crossref] [Google Scholar]
  97. Shao Y, Fu J. 2020.. Synthetic human embryology: towards a quantitative future. . Curr. Opin. Genet. Dev. 63::3035
    [Crossref] [Google Scholar]
  98. Sherwood DR. 2021.. Basement membrane remodeling guides cell migration and cell morphogenesis during development. . Curr. Opin. Cell Biol. 72::1927
    [Crossref] [Google Scholar]
  99. Shirayoshi Y, Okada T, Takeichi M. 1983.. The calcium-dependent cell-cell adhesion system regulates inner cell mass formation and cell surface polarization in early mouse development. . Cell 35:(3):63138
    [Crossref] [Google Scholar]
  100. Skamagki M, Wicher KB, Jedrusik A, Ganguly S, Zernicka-Goetz M. 2013.. Asymmetric localization of Cdx2 mRNA during the first cell-fate decision in early mouse development. . Cell Rep. 3:(2):44257
    [Crossref] [Google Scholar]
  101. Slováková J, Sikora M, Arslan FN, Caballero-Mancebo S, Krens SG, et al. 2022.. Tension-dependent stabilization of E-cadherin limits cell–cell contact expansion in zebrafish germ-layer progenitor cells. . PNAS 119:(8):e2122030119
    [Crossref] [Google Scholar]
  102. Sousa PAD, Valdimarsson G, Nicholson BJ, Kidder GM. 1993.. Connexin trafficking and the control of gap junction assembly in mouse preimplantation embryos. . Development 117:(4):135567
    [Crossref] [Google Scholar]
  103. Steinberg MS. 1963.. Reconstruction of tissues by dissociated cells: some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation. . Science 141:(3579):4018
    [Crossref] [Google Scholar]
  104. Steinberg MS. 1970.. Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. . J. Exp. Zool. 173:(4):395433
    [Crossref] [Google Scholar]
  105. Steinberg MS. 1978.. Specific cell ligands and the differential adhesion hypothesis: How do they fit together?. In Specificity of Embryological Interactions, ed. DR Garrod , pp. 97130. Boston:: Springer
    [Google Scholar]
  106. Stelzer EH, Strobl F, Chang B-J, Preusser F, Preibisch S, et al. 2021.. Light sheet fluorescence microscopy. . Nat. Rev. Methods Primers 1:(1):73
    [Crossref] [Google Scholar]
  107. Stephenson RO, Yamanaka Y, Rossant J. 2010.. Disorganized epithelial polarity and excess trophectoderm cell fate in preimplantation embryos lacking E-cadherin. . Development 137:(20):338391
    [Crossref] [Google Scholar]
  108. Su R-W, Strug MR, Joshi NR, Jeong J-W, Miele L, et al. 2015.. Decreased Notch pathway signaling in the endometrium of women with endometriosis impairs decidualization. . J. Clin. Endocrinol. Metabol. 100:(3):E43342
    [Crossref] [Google Scholar]
  109. Sullivan W, Theurkauf WE. 1995.. The cytoskeleton and morphogenesis of the early Drosophila embryo. . Curr. Opin. Cell Biol. 7:(1):1822
    [Crossref] [Google Scholar]
  110. Tarkowski AK, Wróblewska J. 1967.. Development of blastomeres of mouse eggs isolated at the 4-and 8-cell stage. . Development 18:(1):15580
    [Crossref] [Google Scholar]
  111. Thomas FC, Sheth B, Eckert JJ, Bazzoni G, Dejana E, Fleming TP. 2004.. Contribution of JAM-1 to epithelial differentiation and tight-junction biogenesis in the mouse preimplantation embryo. . J. Cell Sci. 117:(23):5599608
    [Crossref] [Google Scholar]
  112. Tomoda K, Kime C. 2021.. Synthetic embryology: early mammalian embryo modeling systems from cell cultures. . Dev. Growth Diff. 63:(2):11626
    [Crossref] [Google Scholar]
  113. Torres-Padilla M-E, Parfitt D-E, Kouzarides T, Zernicka-Goetz M. 2007.. Histone arginine methylation regulates pluripotency in the early mouse embryo. . Nature 445:(7124):21418
    [Crossref] [Google Scholar]
  114. Vestweber D, Gossler A, Boller K, Kemler R. 1987.. Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. . Dev. Biol. 124:(2):45156
    [Crossref] [Google Scholar]
  115. Vining KH, Mooney DJ. 2017.. Mechanical forces direct stem cell behaviour in development and regeneration. . Nat. Rev. Mol. Cell Biol. 18:(12):72842
    [Crossref] [Google Scholar]
  116. Vinot S, Le T, Ohno S, Pawson T, Maro B, Louvet-Vallée S. 2005.. Asymmetric distribution of PAR proteins in the mouse embryo begins at the 8-cell stage during compaction. . Dev. Biol. 282:(2):30719
    [Crossref] [Google Scholar]
  117. Wallingford JB, Fraser SE, Harland RM. 2002.. Convergent extension: the molecular control of polarized cell movement during embryonic development. . Dev. Cell 2:(6):695706
    [Crossref] [Google Scholar]
  118. Wang F, Chen S, Liu HB, Parent CA, Coulombe PA. 2018.. Keratin 6 regulates collective keratinocyte migration by altering cell–cell and cell–matrix adhesion. . J. Cell Biol. 217:(12):431430
    [Crossref] [Google Scholar]
  119. Wang H, Ding T, Brown N, Yamamoto Y, Prince LS, et al. 2008.. Zonula occludens-1 (ZO-1) is involved in morula to blastocyst transformation in the mouse. . Dev. Biol. 318:(1):11225
    [Crossref] [Google Scholar]
  120. Weberling A, Zernicka-Goetz M. 2021.. Trophectoderm mechanics direct epiblast shape upon embryo implantation. . Cell Rep. 34:(3):108655
    [Crossref] [Google Scholar]
  121. Winkel GK, Ferguson JE, Takeichi M, Nuccitelli R. 1990.. Activation of protein kinase C triggers premature compaction in the four-cell stage mouse embryo. . Dev. Biol. 138:(1):115
    [Crossref] [Google Scholar]
  122. Wozniak MA, Chen CS. 2009.. Mechanotransduction in development: a growing role for contractility. . Nat. Rev. Mol. Cell Biol. 10:(1):3443
    [Crossref] [Google Scholar]
  123. Yang Y, Dowling J, Yu Q-C, Kouklis P, Cleveland DW, Fuchs E. 1996.. An essential cytoskeletal linker protein connecting actin microfilaments to intermediate filaments. . Cell 86:(4):65565
    [Crossref] [Google Scholar]
  124. Zenker J, White MD, Gasnier M, Alvarez YD, Lim HYG, et al. 2018.. Expanding actin rings zipper the mouse embryo for blastocyst formation. . Cell 173:(3):77691.e17
    [Crossref] [Google Scholar]
  125. Zenker J, White MD, Templin R, Parton R, Thorn-Seshold O, et al. 2017.. A microtubule-organizing center directing intracellular transport in the early mouse embryo. . Science 357:(6354):92528
    [Crossref] [Google Scholar]
  126. Zhu M, Leung CY, Shahbazi MN, Zernicka-Goetz M. 2017.. Actomyosin polarisation through PLC-PKC triggers symmetry breaking of the mouse embryo. . Nat. Commun. 8:(1):921
    [Crossref] [Google Scholar]
  127. Zhu M, Zernicka-Goetz M. 2020.. Building an apical domain in the early mouse embryo: lessons, challenges and perspectives. . Curr. Opin. Cell Biol. 62::14449
    [Crossref] [Google Scholar]
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