A self-organization framework for symmetry breaking in the mammalian embryo (original) (raw)

• Rossant, J. & Tam, P. P. L. Emerging asymmetry and embryonic patterning in early mouse development. Dev. Cell 7, 155–164 (2004).
  CAS PubMed Google Scholar
• Rossant, J. & Tam, P. P. L. Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136, 701–713 (2009).
  CAS PubMed Google Scholar
• Guo, G. et al. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev. Cell 18, 675–685 (2010).
  CAS PubMed Google Scholar
• Johnson, M. H. & Ziomek, C. A. The foundation of two distinct cell lineages within the mouse morula. Cell 24, 71–80 (1981).
  CAS PubMed Google Scholar
• Graham, C. F. & Lehtonen, E. Formation and consequences of cell patterns in preimplantation mouse development. J. Embryol. Exp. Morphol. 49, 277–294 (1979).
  CAS PubMed Google Scholar
• Fleming, T. P. A quantitative analysis of cell allocation to trophectoderm and inner cell mass in the mouse blastocyst. Dev. Biol. 119, 520–531 (1987).
  CAS PubMed Google Scholar
• Hiiragi, T. & Solter, D. First cleavage plane of the mouse egg is not predetermined but defined by the topology of the two apposing pronuclei. Nature 430, 360–364 (2004).
  CAS PubMed Google Scholar
• Motosugi, N., Bauer, T., Polanski, Z., Solter, D. & Hiiragi, T. Polarity of the mouse embryo is established at blastocyst and is not prepatterned. Gene. Dev. 19, 1081–1092 (2005).
  CAS PubMed Google Scholar
• Louvet-Vallee, S., Vinot, S. & Maro, B. Mitotic spindles and cleavage planes are oriented randomly in the two-cell mouse embryo. Curr. Biol. 15, 464–469 (2005).
  CAS PubMed Google Scholar
• Kurotaki, Y., Hatta, K., Nakao, K., Nabeshima, Y.-I. & Fujimori, T. Blastocyst axis is specified independently of early cell lineage but aligns with the ZP shape. Science 316, 719–723 (2007).
  CAS PubMed Google Scholar
• Rossant, J. & Lis, W. T. Potential of isolated mouse inner cell masses to form trophectoderm derivatives in vivo. Dev. Biol. 70, 255–261 (1979).
  CAS PubMed Google Scholar
• Rossant, J. & Vijh, K. M. Ability of outside cells from preimplantation mouse embryos to form inner cell mass derivatives. Dev. Biol. 76, 475–482 (1980).
  CAS PubMed Google Scholar
• Driever, W. & Nüsslein-Volhard, C. A gradient of bicoid protein in Drosophila embryos. Cell 54, 83–93 (1988).
  CAS PubMed Google Scholar
• Driever, W. & Nüsslein-Volhard, C. The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54, 95–104 (1988).
  Article CAS Google Scholar
• Goldstein, B. & Hird, S. N. Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122, 1467–1474 (1996).
  CAS PubMed Google Scholar
• Speman, H. Embryonic development and induction. Am. J. Med. Sci. 196, 738 (1938).
  Google Scholar
• Vincent, J. P., Oster, G. F. & Gerhart, J. C. Kinematics of gray crescent formation in Xenopus eggs: the displacement of subcortical cytoplasm relative to the egg surface. Dev. Biol. 113, 484–500 (1986).
  CAS PubMed Google Scholar
• Dalcq, A. Introduction to General Embryology (Oxford Univ. Press, 1957).
  Google Scholar
• Piotrowska, K. & Zernicka-Goetz, M. Role for sperm in spatial patterning of the early mouse embryo. Nature 409, 517–521 (2001).
  CAS PubMed Google Scholar
• Piotrowska, K., Wianny, F., Pedersen, R. A. & Zernicka-Goetz, M. Blastomeres arising from the first cleavage division have distinguishable fates in normal mouse development. Development 128, 3739–3748 (2001).
  CAS PubMed Google Scholar
• Gardner, R. Specification of embryonic axes begins before cleavage in normal mouse development. Development 128, 839–847 (2001).
  CAS PubMed Google Scholar
• Piotrowska-Nitsche, K., Perea-Gomez, A., Haraguchi, S. & Zernicka-Goetz, M. Four-cell stage mouse blastomeres have different developmental properties. Development 132, 479–490 (2005).
  CAS PubMed Google Scholar
• Gardner, R. Experimental analysis of second cleavage in the mouse. Hum. Reprod. 17, 3178–3189 (2002).
  CAS PubMed Google Scholar
• Hiiragi, T. et al. Where do we stand now? Mouse early embryo patterning meeting in Freiburg, Germany (2005). Int. J. Dev. Biol. 50, 581–586 (2005).
  Google Scholar
• Littwin, T. & Denker, H. W. Segregation during cleavage in the mammalian embryo? A critical comparison of whole-mount/CLSM and section immunohistochemistry casts doubts on segregation of axis-relevant leptin domains in the rabbit. Histochem. Cell Biol. 135, 553–570 (2011).
  CAS PubMed Google Scholar
• Schulz, L. C. & Roberts, R. M. Dynamic changes in leptin distribution in the progression from ovum to blastocyst of the pre-implantation mouse embryo. Reproduction 141, 767–777 (2011).
  CAS PubMed PubMed Central Google Scholar
• Antczak, M. & Van Blerkom, J. Oocyte influences on early development: the regulatory proteins leptin and STAT3 are polarized in mouse and human oocytes and differentially distributed within the cells of the preimplantation stage embryo. Mol. Hum. Reprod. 3, 1067–1086 (1997).
  CAS PubMed Google Scholar
• Antczak, M. & Van Blerkom, J. Temporal and spatial aspects of fragmentation in early human embryos: possible effects on developmental competence and association with the differential elimination of regulatory proteins from polarized domains. Hum. Reprod. 14, 429–447 (1999).
  CAS PubMed Google Scholar
• Marikawa, Y. & Alarcon, V. B. Establishment of trophectoderm and inner cell mass lineages in the mouse embryo. Mol. Reprod. Dev. 76, 1019–1032 (2009).
  CAS PubMed PubMed Central Google Scholar
• Tarkowski, A. K. Experiments on the development of isolated blastomers of mouse eggs. Nature 184, 1286–1287 (1959).
  CAS PubMed Google Scholar
• Tarkowski, A. K. & Wróblewska, J. Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. J. Embryol. Exp. Morphol. 18, 155–180 (1967).
  CAS PubMed Google Scholar
• Nishioka, N. et al. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell 16, 398–410 (2009).
  CAS PubMed Google Scholar
• Dietrich, J. E. & Hiiragi, T. Stochastic patterning in the mouse pre-implantation embryo. Development 134, 4219–4231 (2007).
  CAS PubMed Google Scholar
• Ralston, A. & Rossant, J. Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev. Biol. 313, 614–629 (2008).
  CAS PubMed Google Scholar
• Plusa, B., Piliszek, A., Frankenberg, S., Artus, J. & Hadjantonakis, A. K. Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135, 3081–3091 (2008).
  CAS PubMed PubMed Central Google Scholar
• Ducibella, T. & Anderson, E. Cell shape and membrane changes in the eight-cell mouse embryo: prerequisites for morphogenesis of the blastocyst. Dev. Biol. 47, 45–58 (1975).
  CAS PubMed Google Scholar
• Handyside, A. H. Distribution of antibody- and lectin-binding sites on dissociated blastomeres from mouse morulae: evidence for polarization at compaction. J. Embryol. Exp. Morphol. 60, 99–116 (1980).
  CAS PubMed Google Scholar
• Louvet, S., Aghion, J., Santa-Maria, A., Mangeat, P. & Maro, B. Ezrin becomes restricted to outer cells following asymmetrical division in the preimplantation mouse embryo. Dev. Biol. 177, 568–579 (1996).
  CAS PubMed Google Scholar
• Vinot, S. et al. Asymmetric distribution of PAR proteins in the mouse embryo begins at the 8-cell stage during compaction. Dev. Biol. 282, 307–319 (2005).
  CAS PubMed Google Scholar
• Stephenson, R. O., Yamanaka, Y. & Rossant, J. Disorganized epithelial polarity and excess trophectoderm cell fate in preimplantation embryos lacking E-cadherin. Development 137, 3383–3391 (2010).
  CAS PubMed Google Scholar
• Dard, N., Louvet-Vallée, S. & Maro, B. Orientation of mitotic spindles during the 8- to 16-cell stage transition in mouse embryos. PLoS ONE 4, e8171 (2009).
  PubMed PubMed Central Google Scholar
• Bischoff, M., Parfitt, D.-E. & Zernicka-Goetz, M. Formation of the embryonic–abembryonic axis of the mouse blastocyst: relationships between orientation of early cleavage divisions and pattern of symmetric/asymmetric divisions. Development 135, 953–962 (2008).
  CAS PubMed PubMed Central Google Scholar
• Yamanaka, Y., Lanner, F. & Rossant, J. FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 137, 715–724 (2010).
  CAS PubMed Google Scholar
• Morris, S. A. et al. Origin and formation of the first two distinct cell types of the inner cell mass in the mouse embryo. Proc. Natl Acad. Sci. USA 107, 6364–6369 (2010).
  CAS PubMed Google Scholar
• Chazaud, C., Yamanaka, Y., Pawson, T. & Rossant, J. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2–MAPK pathway. Dev. Cell 10, 615–624 (2006).
  CAS PubMed Google Scholar
• Dietrich, J. E. & Hiiragi, T. Stochastic processes during mouse blastocyst patterning. Cells Tissues Organs 188, 46–51 (2008).
  PubMed Google Scholar
• Chambers, I. et al. Nanog safeguards pluripotency and mediates germline development. Nature 450, 1230–1234 (2007).
  CAS PubMed Google Scholar
• Kalmar, T. et al. Regulated fluctuations in Nanog expression mediate cell fate decisions in embryonic stem cells. PLoS Biol. 7, e1000149 (2009).
  PubMed PubMed Central Google Scholar
• Silva, J. & Smith, A. Capturing pluripotency. Cell 132, 532–536 (2008).
  CAS PubMed PubMed Central Google Scholar
• Kurimoto, K. et al. An improved single-cell cDNA amplification method for efficient high-density oligonucleotide microarray analysis. Nucleic Acids Res. 34, e42 (2006).
  PubMed PubMed Central Google Scholar
• Tang, F. et al. mRNA-seq whole-transcriptome analysis of a single cell. Nature Methods 6, 377–382 (2009).
  CAS PubMed Google Scholar
• Tang, F. et al. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-seq analysis. Cell Stem Cell 6, 468–478 (2010).
  CAS PubMed PubMed Central Google Scholar
• Tang, F. et al. Deterministic and stochastic allele specific gene expression in single mouse blastomeres. PLoS ONE 6, e21208 (2011).
  CAS PubMed PubMed Central Google Scholar
• Itzkovitz, S., Blat, I. C., Jacks, T., Clevers, H. & van Oudenaarden, A. Optimality in the development of intestinal crypts. Cell 148, 608–619 (2012).
  CAS PubMed PubMed Central Google Scholar
• Itzkovitz, S. et al. Single-molecule transcript counting of stem-cell markers in the mouse intestine. Nature Cell Biol. 14, 106–114 (2011).
  PubMed Google Scholar
• Raj, A., van den Bogaard, P., Rifkin, S. A., van Oudenaarden, A. & Tyagi, S. Imaging individual mRNA molecules using multiple singly labeled probes. Nature Methods 5, 877–879 (2008).
  CAS PubMed PubMed Central Google Scholar
• Raj, A., Rifkin, S. A., Andersen, E. & van Oudenaarden, A. Variability in gene expression underlies incomplete penetrance. Nature 463, 913–918 (2010).
  CAS PubMed PubMed Central Google Scholar
• Buganim, Y. et al. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150, 1209–1222 (2012).
  CAS PubMed PubMed Central Google Scholar
• Plachta, N., Bollenbach, T., Pease, S., Fraser, S. E. & Pantazis, P. Oct4 kinetics predict cell lineage patterning in the early mammalian embryo. Nature Cell Biol. 13, 117–123 (2011).
  CAS PubMed Google Scholar
• Lorthongpanich, C., Doris, T. P. Y., Limviphuvadh, V., Knowles, B. B. & Solter, D. Developmental fate and lineage commitment of singled mouse blastomeres. Development 139, 3722–3731 (2012).
  CAS PubMed Google Scholar
• Johnson, M. H. From mouse egg to mouse embryo: polarities, axes, and tissues. Annu. Rev. Cell Dev. Biol. 25, 483–512 (2009).
  CAS PubMed Google Scholar
• Wennekamp, S. & Hiiragi, T. Stochastic processes in the development of pluripotency in vivo. Biotechnol. J. 7, 737–744 (2012).
  CAS PubMed Google Scholar
• Müller, P. et al. Differential diffusivity of Nodal and Lefty underlies a reaction–diffusion patterning system. Science 336, 721–724 (2012).
  PubMed PubMed Central Google Scholar
• Nakamura, T. et al. Generation of robust left–right asymmetry in the mouse embryo requires a self-enhancement and lateral-inhibition system. Dev. Cell 11, 495–504 (2006).
  CAS PubMed Google Scholar
• Niwa, H. et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123, 917–929 (2005).
  CAS PubMed Google Scholar
• Honda, H., Motosugi, N., Nagai, T., Tanemura, M. & Hiiragi, T. Computer simulation of emerging asymmetry in the mouse blastocyst. Development 135, 1407–1414 (2008).
  CAS PubMed Google Scholar
• To, T. L. & Maheshri, N. Noise can induce bimodality in positive transcriptional feedback loops without bistability. Science 327, 1142–1145 (2010).
  CAS PubMed Google Scholar
• Chang, H. H., Hemberg, M., Barahona, M., Ingber, D. E. & Huang, S. Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453, 544–547 (2008).
  CAS PubMed PubMed Central Google Scholar
• Meilhac, S. M. et al. Active cell movements coupled to positional induction are involved in lineage segregation in the mouse blastocyst. Dev. Biol. 331, 210–221 (2009).
  CAS PubMed PubMed Central Google Scholar
• McDole, K. & Zheng, Y. Generation and live imaging of an endogenous Cdx2 reporter mouse line. Genesis 50, 775–782 (2012).
  CAS PubMed PubMed Central Google Scholar
• Krzic, U., Gunther, S., Saunders, T. E., Streichan, S. J. & Hufnagel, L. Multiview light-sheet microscope for rapid in toto imaging. Nature Methods 9, 730–733 (2012).
  CAS PubMed Google Scholar
• Tomer, R., Khairy, K., Amat, F. & Keller, P. J. Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy. Nature Methods 9, 755–763 (2012).
  CAS PubMed Google Scholar
• Camazine, S. et al. Self-Organization in Biological Systems (Princeton Univ. Press, 2003).
  Google Scholar
• Krupinski, P., Chickarmane, V. & Peterson, C. Simulating the mammalian blastocyst — molecular and mechanical interactions pattern the embryo. PLoS Comput. Biol. 7, e1001128 (2011).
  CAS PubMed PubMed Central Google Scholar
• Shipley, R. J., Bonsall, M. B., Allwright, D. J. & Graham, C. F. Theoretical exploration of blastocyst morphogenesis. Int. J. Dev. Biol. 53, 447–457 (2009).
  PubMed Google Scholar
• Strumpf, D. et al. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132, 2093–2102 (2005).
  CAS PubMed Google Scholar
• Nishioka, N. et al. Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech. Dev. 125, 270–283 (2008).
  CAS PubMed Google Scholar
• Yagi, R. et al. Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 134, 3827–3836 (2007).
  CAS PubMed Google Scholar
• Nichols, J. et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379–391 (1998).
  CAS PubMed Google Scholar
• Avilion, A. A. et al. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17, 126–140 (2003).
  CAS PubMed PubMed Central Google Scholar
• Chambers, I. et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643–655 (2003).
  CAS PubMed Google Scholar
• Mitsui, K. et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631–642 (2003).
  CAS PubMed Google Scholar
• Kang, M., Piliszek, A., Artus, J. & Hadjantonakis, A.-K. FGF4 is required for lineage restriction and salt-and-pepper distribution of primitive endoderm factors but not their initial expression in the mouse. Development 140, 267–279 (2013).
  CAS PubMed PubMed Central Google Scholar
• Tarkowski, A. K. Mouse chimaeras developed from fused eggs. Nature 190, 857–860 (1961).
  CAS PubMed Google Scholar
• Mitalipov, S. M., Yeoman, R. R., Kuo, H.-C. & Wolf, D. P. Monozygotic twinning in rhesus monkeys by manipulation of _in vitro_-derived embryos. Biol. Reprod. 66, 1449–1455 (2002).
  CAS PubMed Google Scholar
• Gärtner, K. & Baunack, E. Is the similarity of monozygotic twins due to genetic factors alone? Nature 292, 646–647 (1981).
  PubMed Google Scholar
• Gardner, R. L. Mouse chimeras obtained by the injection of cells into the blastocyst. Nature 220, 596–597 (1968).
  CAS PubMed Google Scholar
• Bradley, A., Evans, M., Kaufman, M. H. & Robertson, E. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 309, 255–256 (1984).
  CAS PubMed Google Scholar
• Saetzler, K., Sonnenschein, C. & Soto, A. M. Systems biology beyond networks: generating order from disorder through self-organization. Semin. Cancer Biol. 21, 165–174 (2011).
  CAS PubMed PubMed Central Google Scholar
• Karsenti, E. Self-organization in cell biology: a brief history. Nature Rev. Mol. Cell Biol. 9, 255–262 (2008).
  CAS Google Scholar
• Sasai, Y. Cytosystems dynamics in self-organization of tissue architecture. Nature 493, 318–326 (2013).
  CAS PubMed Google Scholar
• Clayton, E. et al. A single type of progenitor cell maintains normal epidermis. Nature 446, 185–189 (2007).
  CAS PubMed Google Scholar
• Doupé, D. P., Klein, A. M., Simons, B. D. & Jones, P. H. The ordered architecture of murine ear epidermis is maintained by progenitor cells with random fate. Dev. Cell 18, 317–323 (2010).
  PubMed Google Scholar
• Lopez-Garcia, C., Klein, A. M., Simons, B. D. & Winton, D. J. Intestinal stem cell replacement follows a pattern of neutral drift. Science 330, 822–825 (2010).
  CAS PubMed Google Scholar
• Snippert, H. J. et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143, 134–144 (2010).
  CAS PubMed Google Scholar
• Klein, A. M., Nakagawa, T., Ichikawa, R., Yoshida, S. & Simons, B. D. Mouse germ line stem cells undergo rapid and stochastic turnover. Cell Stem Cell 7, 214–224 (2010).
  CAS PubMed Google Scholar
• Klein, A. M. & Simons, B. D. Universal patterns of stem cell fate in cycling adult tissues. Development 138, 3103–3111 (2011).
  CAS PubMed Google Scholar
• Hamant, O. et al. Developmental patterning by mechanical signals in Arabidopsis. Science 322, 1650–1655 (2008).
  CAS PubMed Google Scholar
• Heisler, M. G. et al. Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol. 8, e1000516 (2010).
  PubMed PubMed Central Google Scholar
• Gerisch, G. Zellfunktionen und Zellfunktionswechsel in der Entwicklung von Dictyostelium discoideum. Exp. Cell Res. 25, 535–554 (1961).
  CAS PubMed Google Scholar
• Glazier, J. A. & Graner, F. Simulation of the differential adhesion driven rearrangement of biological cells. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 47, 2128–2154 (1993).
  CAS PubMed Google Scholar
• Savill, N. J. & Hogeweg, P. Modelling morphogenesis: from single cells to crawling slugs. J. Theor. Biol. 184, 229–235 (1997).
  Google Scholar
• Maree, A. F. M. & Hogeweg, P. How amoeboids self-organize into a fruiting body: multicellular coordination in Dictyostelium discoideum. Proc. Natl Acad. Sci. USA 98, 3879–3883 (2001).
  CAS PubMed Google Scholar
• Sawai, S., Thomason, P. A. & Cox, E. C. An autoregulatory circuit for long-range self-organization in Dictyostelium cell populations. Nature 433, 323–326 (2005).
  CAS PubMed Google Scholar
• Hayashi, T. & Carthew, R. W. Surface mechanics mediate pattern formation in the developing retina. Nature 431, 647–652 (2004).
  CAS PubMed Google Scholar