Mouse Development pp 203-217

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

Formation of Distinct Cell Types in the Mouse Blastocyst

Chapter

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.

References

  1. 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 3:1067–1086PubMedCrossRefGoogle Scholar
  2. 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 95:5082–5087PubMedCrossRefGoogle Scholar
  3. 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 135:953–962PubMedCrossRefGoogle Scholar
  4. 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 10:615–624PubMedCrossRefGoogle Scholar
  5. Chisholm JC, Houliston E (1987) Cytokeratin filament assembly in the preimplantation mouse embryo. Development 101:565–582PubMedGoogle Scholar
  6. Dalcq AM (1957) Terminology of induction. Acta Anat (Basel) 30:242–253CrossRefGoogle Scholar
  7. Dietrich JE, Hiiragi T (2007) Stochastic patterning in the mouse pre-implantation embryo. Development 134:4219–4231PubMedCrossRefGoogle Scholar
  8. Dziadek M (1979) Cell differentiation in isolated inner cell masses of mouse blastocysts in vitro: onset of specific gene expression. J Embryol Exp Morphol 53:367–379PubMedGoogle Scholar
  9. Feldman B, Poueymirou W, Papaioannou VE, DeChiara TM, Goldfarb M (1995) Requirement of FGF-4 for postimplantation mouse development. Science 267:246–249PubMedCrossRefGoogle Scholar
  10. 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:D1000–1007PubMedCrossRefGoogle Scholar
  11. 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 16:784–789PubMedCrossRefGoogle Scholar
  12. Gardner RL (1982) Investigation of cell lineage and differentiation in the extraembryonic endoderm of the mouse embryo. J Embryol Exp Morphol 68:175–198PubMedGoogle Scholar
  13. Gardner RL (2002) Experimental analysis of second cleavage in the mouse. Hum Reprod 17:3178–3189PubMedCrossRefGoogle Scholar
  14. Graham CF, Deussen ZA (1978) Features of cell lineage in preimplantation mouse development. J Embryol Exp Morphol 48:53–72PubMedGoogle Scholar
  15. 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):675–85PubMedCrossRefGoogle Scholar
  16. 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 193:235–248PubMedCrossRefGoogle Scholar
  17. Handyside AH (1978) Time of commitment of inside cells isolated from preimplantation mouse embryos. J Embryol Exp Morphol 45:37–53PubMedGoogle Scholar
  18. 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 60:99–116PubMedGoogle Scholar
  19. 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 327:905–909PubMedCrossRefGoogle Scholar
  20. Hillman N, Sherman MI, Graham C (1972) The effect of spatial arrangement on cell determination during mouse development. J Embryol Exp Morphol 28:263–278PubMedGoogle Scholar
  21. 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 22:2692–2706PubMedCrossRefGoogle Scholar
  22. Johnson MH, Ziomek CA (1981) The foundation of two distinct cell lineages within the mouse morula. Cell 24:71–80PubMedCrossRefGoogle Scholar
  23. 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 129:2367–2379PubMedGoogle Scholar
  24. Koutsourakis M, Langeveld A, Patient R, Beddington R, Grosveld F (1999) The transcription factor GATA6 is essential for early extraembryonic development. Development 126:723–732Google Scholar
  25. 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:e42PubMedCrossRefGoogle Scholar
  26. Lehtonen E (1980) Changes in cell dimensions and intercellular contacts during cleavage-stage cell cycles in mouse embryonic cells. J Embryol Exp Morphol 58:231–249PubMedGoogle Scholar
  27. Martin GR, Evans MJ (1975) Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc Natl Acad Sci USA 72:1441–1445PubMedCrossRefGoogle Scholar
  28. 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 107:6364–6369PubMedCrossRefGoogle Scholar
  29. 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 12:3579–3590PubMedCrossRefGoogle Scholar
  30. Murray P, Edgar D (2001) The regulation of embryonic stem cell differentiation by leukaemia inhibitory factor (LIF). Differentiation 68:227–234PubMedCrossRefGoogle Scholar
  31. 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 24:312–326PubMedCrossRefGoogle Scholar
  32. Nichols J, Silva J, Roode M, Smith A (2009) Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development 136:3215–3222PubMedCrossRefGoogle Scholar
  33. 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 16:398–410PubMedCrossRefGoogle Scholar
  34. 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 125:270–283PubMedCrossRefGoogle Scholar
  35. Ota M, Sasaki H (2008) Mammalian Tead proteins regulate cell proliferation and contact inhibition as transcriptional mediators of Hippo signaling. Development 135:4059–4069PubMedCrossRefGoogle Scholar
  36. Pan D (2007) Hippo signaling in organ size control. Genes Dev 21:886–897PubMedCrossRefGoogle Scholar
  37. 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 21:2649–2660PubMedCrossRefGoogle Scholar
  38. 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 7:96PubMedCrossRefGoogle Scholar
  39. Piotrowska-Nitsche K, Perea-Gomez A, Haraguchi S, Zernicka-Goetz M (2005) Four-cell stage mouse blastomeres have different developmental properties. Development 132:479–490PubMedCrossRefGoogle Scholar
  40. 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 118:505–515PubMedCrossRefGoogle Scholar
  41. Plusa B, Piliszek A, Frankenberg S, Artus J, Hadjantonakis AK (2008) Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135:3081–3091PubMedCrossRefGoogle Scholar
  42. Ralston A, Rossant J (2008) Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev Biol 313:614–629PubMedCrossRefGoogle Scholar
  43. Reeve WJ, Ziomek CA (1981) Distribution of microvilli on dissociated blastomeres from mouse embryos: evidence for surface polarization at compaction. J Embryol Exp Morphol 62:339–350PubMedGoogle Scholar
  44. 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 33:991–1001PubMedGoogle Scholar
  45. 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 1349PubMedCrossRefGoogle Scholar
  46. Rossant J, Lis WT (1979) Potential of isolated mouse inner cell masses to form trophectoderm derivatives in vivo. Dev Biol 70:255–261PubMedCrossRefGoogle Scholar
  47. Rossant J, Vijh KM (1980) Ability of outside cells from preimplantation mouse embryos to form inner cell mass derivatives. Dev Biol 76:475–482PubMedCrossRefGoogle Scholar
  48. 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 28:3177–3189PubMedCrossRefGoogle Scholar
  49. Schultz RM (2002) The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum Reprod Update 8:323–331PubMedCrossRefGoogle Scholar
  50. 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 7:80PubMedCrossRefGoogle Scholar
  51. Solter D, Knowles BB (1975) Immunosurgery of mouse blastocyst. Proc Natl Acad Sci USA 72:5099–5102PubMedCrossRefGoogle Scholar
  52. Spindle AI (1978) Trophoblast regeneration by inner cell masses isolated from cultured mouse embryos. J Exp Zool 203:483–489PubMedCrossRefGoogle Scholar
  53. 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 132:2093–2102PubMedCrossRefGoogle Scholar
  54. 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 322:133–144PubMedCrossRefGoogle Scholar
  55. Tarkowski AK (1959) Experiments on the development of isolated blastomers of mouse eggs. Nature 184:1286–1287PubMedCrossRefGoogle Scholar
  56. Tarkowski AK, Wroblewska J (1967) Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. J Embryol Exp Morphol 18:155–180PubMedGoogle Scholar
  57. 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 117:5599–5608PubMedCrossRefGoogle Scholar
  58. Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M (2007) Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445:214–218PubMedCrossRefGoogle Scholar
  59. 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 282:307–319PubMedCrossRefGoogle Scholar
  60. 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 6:133–144PubMedCrossRefGoogle Scholar
  61. Watson AJ (1992) The cell biology of blastocyst development. Mol Reprod Dev 33:492–504PubMedCrossRefGoogle Scholar
  62. Weber RJ, Pedersen RA, Wianny F, Evans MJ, Zernicka-Goetz M (1999) Polarity of the mouse embryo is anticipated before implantation. Development 126:5591–5598PubMedGoogle Scholar
  63. 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 130:276–284PubMedCrossRefGoogle Scholar
  64. Wilson IB, Bolton E, Cuttler RH (1972) Preimplantation differentiation in the mouse egg as revealed by microinjection of vital markers. J Embryol Exp Morphol 27:467–469PubMedGoogle Scholar
  65. 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 134:3827–3836PubMedCrossRefGoogle Scholar
  66. Yamanaka Y, Lanner F, Rossant J (2010) FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 137:715–724PubMedCrossRefGoogle Scholar
  67. Ziomek CA, Johnson MH (1980) Cell surface interaction induces polarization of mouse 8-cell blastomeres at compaction. Cell 21:935–942PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Samantha A. Morris
    • 1
  • Magdalena Zernicka-Goetz
    • 2
    • 3
  1. 1.Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical SchoolBoston Children’s HospitalBostonUSA
  2. 2.Wellcome Trust/Cancer Research UK Gurdon InstituteCambridgeUK
  3. 3.Department of Physiology, Development and NeuroscienceUniversity of CambridgeCambridgeUK

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