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Mouse Development pp 203–217Cite as

Formation of Distinct Cell Types in the Mouse Blastocyst

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Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 55))

Abstract

Early development of the mouse comprises a sequence of cell fate decisions in which cells are guided along a pathway of restricted potential and increasing specialisation. The first choice faced by cells of the embryo is whether to become trophectoderm (TE) or inner cell mass (ICM); TE is an extra-embryonic tissue which will form the embryonic portion of the placenta, whilst ICM gives rise to cells responsible for generating the foetus. In the second cell fate decision, the ICM is further refined into pluripotent cells forming the future body of the embryo, epiblast (EPI) and extra-embryonic primitive endoderm (PE), a tissue essential for patterning the embryo and establishing the developmental circulation. Understanding this early lineage segregation is critical for informing attempts to capture pluripotency and direct cell fate in vitro. Unlike the predictability of nonmammalian cell fate, development of the mouse embryo retains the flexibility to adapt to changing circumstances during development. Here we describe these first cell fate decisions, how they can be biased whilst maintaining flexibility and, finally, some of the molecular circuitry underlying early fate choice.

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References

  • Antczak M, Van Blerkom J (1997) 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

    Article  PubMed  CAS  Google Scholar 

  • Arman E, Haffner-Krausz R, Chen Y, Heath JK, Lonai P (1998) Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl Acad Sci USA 95:5082–5087

    Article  PubMed  CAS  Google Scholar 

  • Bischoff M, Parfitt DE, Zernicka-Goetz M (2008) 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

    Article  PubMed  CAS  Google Scholar 

  • 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 10:615–624

    Article  PubMed  CAS  Google Scholar 

  • Chisholm JC, Houliston E (1987) Cytokeratin filament assembly in the preimplantation mouse embryo. Development 101:565–582

    PubMed  CAS  Google Scholar 

  • Dalcq AM (1957) Terminology of induction. Acta Anat (Basel) 30:242–253

    Article  CAS  Google Scholar 

  • Dietrich JE, Hiiragi T (2007) Stochastic patterning in the mouse pre-implantation embryo. Development 134:4219–4231

    Article  PubMed  CAS  Google Scholar 

  • Dziadek M (1979) Cell differentiation in isolated inner cell masses of mouse blastocysts in vitro: onset of specific gene expression. J Embryol Exp Morphol 53:367–379

    PubMed  CAS  Google Scholar 

  • Feldman B, Poueymirou W, Papaioannou VE, DeChiara TM, Goldfarb M (1995) Requirement of FGF-4 for postimplantation mouse development. Science 267:246–249

    Article  PubMed  CAS  Google Scholar 

  • Fleming TP, Sheth B, Fesenko I (2001) Cell adhesion in the preimplantation mammalian embryo and its role in trophectoderm differentiation and blastocyst morphogenesis. Front Biosci 6:D1000–1007

    Article  PubMed  CAS  Google Scholar 

  • Fujikura J, Yamato E, Yonemura S, Hosoda K, Masui S, Nakao K, Miyazaki Ji J, Niwa H (2002) Differentiation of embryonic stem cells is induced by GATA factors. Genes Dev 16:784–789

    Article  PubMed  CAS  Google Scholar 

  • Gardner RL (1982) Investigation of cell lineage and differentiation in the extraembryonic endoderm of the mouse embryo. J Embryol Exp Morphol 68:175–198

    PubMed  CAS  Google Scholar 

  • Gardner RL (2002) Experimental analysis of second cleavage in the mouse. Hum Reprod 17:3178–3189

    Article  PubMed  CAS  Google Scholar 

  • Graham CF, Deussen ZA (1978) Features of cell lineage in preimplantation mouse development. J Embryol Exp Morphol 48:53–72

    PubMed  CAS  Google Scholar 

  • Guo G, Huss M, Tong GQ, Wang C, Li Sun L, Clarke ND, Robson P (2010). Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 18(4):675–85

    Article  PubMed  CAS  Google Scholar 

  • Gulyas BJ (1975) A reexamination of cleavage patterns in eutherian mammalian eggs: rotation of blastomere pairs during second cleavage in the rabbit. J Exp Zool 193:235–248

    Article  PubMed  CAS  Google Scholar 

  • Handyside AH (1978) Time of commitment of inside cells isolated from preimplantation mouse embryos. J Embryol Exp Morphol 45:37–53

    PubMed  CAS  Google Scholar 

  • Handyside AH (1980) 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

    PubMed  CAS  Google Scholar 

  • Handyside AH, Lesko JG, Tarin JJ, Winston RM, Hughes MR (1992) Birth of a normal girl after in vitro fertilization and preimplantation diagnostic testing for cystic fibrosis. N Engl J Med 327:905–909

    Article  PubMed  CAS  Google Scholar 

  • Hillman N, Sherman MI, Graham C (1972) The effect of spatial arrangement on cell determination during mouse development. J Embryol Exp Morphol 28:263–278

    PubMed  CAS  Google Scholar 

  • Jedrusik A, Parfitt DE, Guo G, Skamagki M, Grabarek JB, Johnson MH, Robson P, Zernicka-Goetz M (2008) Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo. Genes Dev 22:2692–2706

    Article  PubMed  CAS  Google Scholar 

  • Johnson MH, Ziomek CA (1981) The foundation of two distinct cell lineages within the mouse morula. Cell 24:71–80

    Article  PubMed  CAS  Google Scholar 

  • Kanai-Azuma M, Kanai Y, Gad JM, Tajima Y, Taya C, Kurohmaru M, Sanai Y, Yonekawa H, Yazaki K, Tam PP et al (2002) Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 129:2367–2379

    PubMed  CAS  Google Scholar 

  • Koutsourakis M, Langeveld A, Patient R, Beddington R, Grosveld F (1999) The transcription factor GATA6 is essential for early extraembryonic development. Development 126:723–732

    CAS  Google Scholar 

  • Kurimoto K, Yabuta Y, Ohinata Y, Ono Y, Uno KD, Yamada RG, Ueda HR, Saitou M (2006) An improved single-cell cDNA amplification method for efficient high-density oligonucleotide microarray analysis. Nucleic Acids Res 34:e42

    Article  PubMed  Google Scholar 

  • Lehtonen E (1980) Changes in cell dimensions and intercellular contacts during cleavage-stage cell cycles in mouse embryonic cells. J Embryol Exp Morphol 58:231–249

    PubMed  CAS  Google Scholar 

  • Martin GR, Evans MJ (1975) Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc Natl Acad Sci USA 72:1441–1445

    Article  PubMed  CAS  Google Scholar 

  • Morris SA, Teo RT, Li H, Robson P, Glover DM, Zernicka-Goetz M (2010) 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

    Article  PubMed  CAS  Google Scholar 

  • Morrisey EE, Tang Z, Sigrist K, Lu MM, Jiang F, Ip HS, Parmacek MS (1998) GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev 12:3579–3590

    Article  PubMed  CAS  Google Scholar 

  • Murray P, Edgar D (2001) The regulation of embryonic stem cell differentiation by leukaemia inhibitory factor (LIF). Differentiation 68:227–234

    Article  PubMed  CAS  Google Scholar 

  • Niakan KK, Ji H, Maehr R, Vokes SA, Rodolfa KT, Sherwood RI, Yamaki M, Dimos JT, Chen AE, Melton DA et al (2010) Sox17 promotes differentiation in mouse embryonic stem cells by directly regulating extraembryonic gene expression and indirectly antagonizing self-renewal. Genes Dev 24:312–326

    Article  PubMed  CAS  Google Scholar 

  • Nichols J, Silva J, Roode M, Smith A (2009) Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development 136:3215–3222

    Article  PubMed  CAS  Google Scholar 

  • Nishioka N, Inoue K, Adachi K, Kiyonari H, Ota M, Ralston A, Yabuta N, Hirahara S, Stephenson RO, Ogonuki N et al (2009) The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell 16:398–410

    Article  PubMed  CAS  Google Scholar 

  • Nishioka N, Yamamoto S, Kiyonari H, Sato H, Sawada A, Ota M, Nakao K, Sasaki H (2008) Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech Dev 125:270–283

    Article  PubMed  CAS  Google Scholar 

  • Ota M, Sasaki H (2008) Mammalian Tead proteins regulate cell proliferation and contact inhibition as transcriptional mediators of Hippo signaling. Development 135:4059–4069

    Article  PubMed  CAS  Google Scholar 

  • Pan D (2007) Hippo signaling in organ size control. Genes Dev 21:886–897

    Article  PubMed  CAS  Google Scholar 

  • Parfitt DE, Zernicka-Goetz M (2010) Epigenetic modification affecting expression of cell polarity and cell fate genes to regulate lineage specification in the early mouse embryo. Mol Biol Cell 21:2649–2660

    Article  PubMed  CAS  Google Scholar 

  • Perea-Gomez A, Meilhac SM, Piotrowska-Nitsche K, Gray D, Collignon J, Zernicka-Goetz M (2007) Regionalization of the mouse visceral endoderm as the blastocyst transforms into the egg cylinder. BMC Dev Biol 7:96

    Article  PubMed  Google Scholar 

  • Piotrowska-Nitsche K, Perea-Gomez A, Haraguchi S, Zernicka-Goetz M (2005) Four-cell stage mouse blastomeres have different developmental properties. Development 132:479–490

    Article  PubMed  CAS  Google Scholar 

  • Plusa B, Frankenberg S, Chalmers A, Hadjantonakis AK, Moore CA, Papalopulu N, Papaioannou VE, Glover DM, Zernicka-Goetz M (2005) Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo. J Cell Sci 118:505–515

    Article  PubMed  CAS  Google Scholar 

  • Plusa B, Piliszek A, Frankenberg S, Artus J, Hadjantonakis AK (2008) Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135:3081–3091

    Article  PubMed  CAS  Google Scholar 

  • Ralston A, Rossant J (2008) Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev Biol 313:614–629

    Article  PubMed  CAS  Google Scholar 

  • Reeve WJ, Ziomek CA (1981) Distribution of microvilli on dissociated blastomeres from mouse embryos: evidence for surface polarization at compaction. J Embryol Exp Morphol 62:339–350

    PubMed  CAS  Google Scholar 

  • Rossant J (1975) Investigation of the determinative state of the mouse inner cell mass. II. The fate of isolated inner cell masses transferred to the oviduct. J Embryol Exp Morphol 33:991–1001

    PubMed  CAS  Google Scholar 

  • Rossant J, Chazaud C, Yamanaka Y (2003) Lineage allocation and asymmetries in the early mouse embryo. Philos Trans R Soc Lond B Biol Sci 358:1341–1348, discussion 1349

    Article  PubMed  CAS  Google Scholar 

  • Rossant J, Lis WT (1979) Potential of isolated mouse inner cell masses to form trophectoderm derivatives in vivo. Dev Biol 70:255–261

    Article  PubMed  CAS  Google Scholar 

  • Rossant J, Vijh KM (1980) Ability of outside cells from preimplantation mouse embryos to form inner cell mass derivatives. Dev Biol 76:475–482

    Article  PubMed  CAS  Google Scholar 

  • Sawada A, Kiyonari H, Ukita K, Nishioka N, Imuta Y, Sasaki H (2008) Redundant roles of Tead1 and Tead2 in notochord development and the regulation of cell proliferation and survival. Mol Cell Biol 28:3177–3189

    Article  PubMed  CAS  Google Scholar 

  • Schultz RM (2002) The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum Reprod Update 8:323–331

    Article  PubMed  CAS  Google Scholar 

  • Shimosato D, Shiki M, Niwa H (2007) Extra-embryonic endoderm cells derived from ES cells induced by GATA factors acquire the character of XEN cells. BMC Dev Biol 7:80

    Article  PubMed  Google Scholar 

  • Solter D, Knowles BB (1975) Immunosurgery of mouse blastocyst. Proc Natl Acad Sci USA 72:5099–5102

    Article  PubMed  CAS  Google Scholar 

  • Spindle AI (1978) Trophoblast regeneration by inner cell masses isolated from cultured mouse embryos. J Exp Zool 203:483–489

    Article  PubMed  CAS  Google Scholar 

  • Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F, Rossant J (2005) Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132:2093–2102

    Article  PubMed  CAS  Google Scholar 

  • Suwinska A, Czolowska R, Ozdzenski W, Tarkowski AK (2008) Blastomeres of the mouse embryo lose totipotency after the fifth cleavage division: expression of Cdx2 and Oct4 and developmental potential of inner and outer blastomeres of 16- and 32-cell embryos. Dev Biol 322:133–144

    Article  PubMed  CAS  Google Scholar 

  • Tarkowski AK (1959) Experiments on the development of isolated blastomers of mouse eggs. Nature 184:1286–1287

    Article  PubMed  CAS  Google Scholar 

  • Tarkowski AK, Wroblewska J (1967) Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. J Embryol Exp Morphol 18:155–180

    PubMed  CAS  Google Scholar 

  • 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 117:5599–5608

    Article  PubMed  CAS  Google Scholar 

  • Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M (2007) Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445:214–218

    Article  PubMed  CAS  Google Scholar 

  • Vinot S, Le T, Ohno S, Pawson T, Maro B, Louvet-Vallee S (2005) Asymmetric distribution of PAR proteins in the mouse embryo begins at the 8-cell stage during compaction. Dev Biol 282:307–319

    Article  PubMed  CAS  Google Scholar 

  • Wang QT, Piotrowska K, Ciemerych MA, Milenkovic L, Scott MP, Davis RW, Zernicka-Goetz M (2004) A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev Cell 6:133–144

    Article  PubMed  CAS  Google Scholar 

  • Watson AJ (1992) The cell biology of blastocyst development. Mol Reprod Dev 33:492–504

    Article  PubMed  CAS  Google Scholar 

  • Weber RJ, Pedersen RA, Wianny F, Evans MJ, Zernicka-Goetz M (1999) Polarity of the mouse embryo is anticipated before implantation. Development 126:5591–5598

    PubMed  CAS  Google Scholar 

  • Wiley LM, Obasaju MF (1988) Induction of cytoplasmic polarity in heterokaryons of mouse 4-cell-stage blastomeres fused with 8-cell- and 16-cell-stage blastomeres. Dev Biol 130:276–284

    Article  PubMed  CAS  Google Scholar 

  • Wilson IB, Bolton E, Cuttler RH (1972) Preimplantation differentiation in the mouse egg as revealed by microinjection of vital markers. J Embryol Exp Morphol 27:467–469

    PubMed  CAS  Google Scholar 

  • Yagi R, Kohn MJ, Karavanova I, Kaneko KJ, Vullhorst D, DePamphilis ML, Buonanno A (2007) Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 134:3827–3836

    Article  PubMed  CAS  Google Scholar 

  • Yamanaka Y, Lanner F, Rossant J (2010) FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 137:715–724

    Article  PubMed  CAS  Google Scholar 

  • Ziomek CA, Johnson MH (1980) Cell surface interaction induces polarization of mouse 8-cell blastomeres at compaction. Cell 21:935–942

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston Children’s Hospital, Boston, MA, USA

    Samantha A. Morris

  2. Wellcome Trust/Cancer Research UK Gurdon Institute, Cambridge, CB2 1QN, UK

    Magdalena Zernicka-Goetz

  3. Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge, CB2 3DY, UK

    Magdalena Zernicka-Goetz

Authors
  1. Samantha A. Morris
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  2. Magdalena Zernicka-Goetz
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Correspondence to Magdalena Zernicka-Goetz .

Editor information

Editors and Affiliations

  1. CNRS UMR 6061, Fac. Médecine, Université de Rennes 1, Rennes CX, 35043, France

    Jacek Z. Kubiak

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Morris, S.A., Zernicka-Goetz, M. (2012). Formation of Distinct Cell Types in the Mouse Blastocyst. In: Kubiak, J. (eds) Mouse Development. Results and Problems in Cell Differentiation, vol 55. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30406-4_11

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