Building the mouse gastrula: signals, asymmetry and lineages

Current Opinion in Genetics and Development

Volumn 16, Issue 4, 2006, Pages 419-425

  Tam, Patrick PL ^a   Loebel, David AF ^a   Tanaka, Satomi S ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; WNT PROTEIN;

CELL LINEAGE; CELL MOTION; ECTODERM; EMBRYO DEVELOPMENT; ENDODERM; GASTRULA; GASTRULATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; MESODERM; NIDATION; NONHUMAN; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ACTIVINS; ANIMALS; BODY PATTERNING; CELL LINEAGE; CELL MOVEMENT; ENDODERM; GASTRULA; GERM CELLS; MEMBRANE PROTEINS; MICE; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEINS;

EID: 33745618439     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2006.06.008     Document Type: Review

References (46)

1. Lawson K.A. Fate mapping the mouse embryo. Int J Dev Biol 43 (1999) 773-775
2. Tam P.P.L., and Gad J.M. Gastrulation of the mouse embryo. In: Stern C.D. (Ed). Gastrulation (2004), Cold Spring Harbor Laboratory Press, New York 223-262
3. Rossant J., and Tam P.P. Emerging asymmetry and embryonic patterning in early mouse development. Dev Cell 7 (2004) 155-164
4. Rivera-Perez J.A., and Magnuson T. Primitive streak formation in mice is preceded by localized activation of brachyury and Wnt3. Dev Biol 288 (2005) 363-371
5. Yamamoto M., Saijoh Y., Perea-Gomez A., Shawlot W., Behringer R.R., Ang S.L., Hamada H., and Meno C. Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 428 (2004) 387-392
6. Kimura-Yoshida C., Nakano H., Okamura D., Nakao K., Yonemura S., Belo J.A., Aizawa S., Matsui Y., and Matsuo I. Canonical Wnt signaling and its antagonist regulate anterior-posterior axis polarization by guiding cell migration in mouse visceral endoderm. Dev Cell 9 (2005) 639-650. This study demonstrates that a Wnt antagonist, Dkk1, can rescue defects in the movement of the AVE. That DKK1 attracts and Wnt3A repels migrating VE cells suggests that VE movement might be directed towards regions of reduced Wnt signalling activity.
7. Rodriguez T.A., Srinivas S., Clements M.P., Smith J.C., and Beddington R.S. Induction and migration of the anterior visceral endoderm is regulated by the extra-embryonic ectoderm. Development 132 (2005) 2513-2520. The extra-embryonic ectoderm is shown to influence the regionalization of the Hex-expressing VE cells to the anterior region of the embryo. The extra-embryonic ectoderm acts by repressing AVE genes and by inducing markers of posterior germ layer tissues.
8. Gotoh N., Manova K., Tanaka S., Murohashi M., Hadari Y., Lee A., Hamada Y., Hiroe T., Ito M., Kurihara T., et al. The docking protein Frs2α is an essential component of multiple fibroblast growth factor responses during early mouse development. Mol Cell Biol 25 (2005) 4105-4116. The Frs2α-null mutant phenotype demonstrates that FGF signaling is required for viability of the extra-embryonic ectoderm: loss of FGF signaling leads to downregulation of Bmp4 and, subsequently, disruption of the morphogenetic activity of the extra-embryonic ectoderm, culminating in defective gastrulation.
9. Chen C., Ware S.M., Sato A., Houston-Hawkins D.E., Habas R., Matzuk M.M., Shen M.M., and Brown C.W. The Vg1-related protein Gdf3 acts in a Nodal signaling pathway in the pre-gastrulation mouse embryo. Development 133 (2006) 319-329. Results of this study of Gdf3-mutant embryos show that, in a similar manner to Nodal, Gdf3 signals through the Activin receptor and requires Tdgf1 and FoxH1 activity. Gdf3 is essential for the proper localisation of the AVE and for the initiation of gastrulation.
10. Levine A.J., and Brivanlou A.H. GDF3, a BMP inhibitor, regulates cell fate in stem cells and early embryos. Development 133 (2006) 209-216
11. Birsoy B., Kofron M., Schaible K., Wylie C., and Heasman J. Vg1 is an essential signaling molecule in Xenopus development. Development 133 (2006) 15-20
12. Soares M.L., Haraguchi S., Torres-Padilla M.E., Kalmar T., Carpenter L., Bell G., Morrison A., Ring C.J., Clarke N.J., Glover D.M., and Zernicka-Goetz M. Functional studies of signaling pathways in peri-implantation development of the mouse embryo by RNAi. BMC Dev Biol 5 (2005) 28
13. Donnison M., Beaton A., Davey H.W., Broadhurst R., L'Huillier P., and Pfeffer P.L. Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development 132 (2005) 2299-2308. Elf5-null mouse embryos, which cannot maintain a population of trophectodermal stem cells, form an ectoplacental cone (EPC) but no ExE. Although the AVE is present, the mutant embryo does not undergo gastrulation. It is likely that the EPC has substituted for the ExE in AVE formation but not in patterning the epiblast.
14. McLaren A., and Lawson K.A. How is the mouse germ-cell lineage established?. Differentiation 73 (2005) 435-437
15. Ohinata Y., Payer B., O'Carroll D., Ancelin K., Ono Y., Sano M., Barton S.C., Obukhanych T., Nussenzweig M., Tarakhovsky A., et al. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436 (2005) 207-213. Prdm1 expression marks the precursor of the primordial germ cells in the pre-gastrula mouse embryo. It is proposed that Prdm1 functions to repress the default molecular pathway of somatic differentiation and promotes recruitment of epiblast cells to the germ cell lineage. Absence of Prdm1 activity in the Bmp4-null embryos suggests that Prdm1 expression is regulated by Bmp signalling from the extra-embryonic tissues.
16. Vincent S.D., Dunn N.R., Sciammas R., Shapiro-Shalef M., Davis M.M., Calame K., Bikoff E.K., and Robertson E.J. The zinc finger transcriptional repressor Blimp1/Prdm1 is dispensable for early axis formation but is required for specification of primordial germ cells in the mouse. Development 132 (2005) 1315-1325
17. Lawson K.A., Dunn N.R., Roelen B.A., Zeinstra L.M., Davis A.M., Wright C.V., Korving J.P., and Hogan B.L. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13 (1999) 424-436
18. de Sousa Lopes S.M., Roelen B.A., Monteiro R.M., Emmens R., Lin H.Y., Li E., Lawson K.A., and Mummery C.L. BMP signaling mediated by Alk2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo. Genes Dev 18 (2004) 1838-1849
19. Roy S., and Ng T. Blimp-1 specifies neural crest and sensory neuron progenitors in the zebrafish embryo. Curr Biol 14 (2004) 1772-1777
20. Tanaka S.S., and Matsui Y. Developmentally regulated expression of mil-1 and Mil-2, mouse interferon-induced transmembrane protein like genes, during formation and differentiation of primordial germ cells. Mech Dev 119 Suppl 1 (2002) S261-S267
21. Saitou M., Barton S.C., and Surani M.A. A molecular programme for the specification of germ cell fate in mice. Nature 418 (2002) 293-300
22. Tanaka S.S., Nagamatsu G., Tokitake Y., Kasa M., Tam P.P., and Matsui Y. Regulation of expression of mouse interferon-induced transmembrane protein like gene-3, Ifitm3 (mil-1, fragilis), in germ cells. Dev Dyn 230 (2004) 651-659
23. Tanaka S.S., Yamaguchi Y.L., Tsoi B., Lickert H., and Tam P.P. IFITM/Mil/fragilis family proteins IFITM1 and IFITM3 play distinct roles in mouse primordial germ cell homing and repulsion. Dev Cell 9 (2005) 745-756. This study reveals a novel molecular mechanism through which the activity of the cell surface interferon-induced transmembrane (Ifitm) proteins navigate the movement of primordial germ cells (PGCs) during gastrulation of the mouse embryo. Ifitm1-mediated repulsive activity is required for the transit of PGCs from the mesoderm into the endoderm, whereas expression of Ifitm3, which occurs in migratory PGCs, enables the cells to display homing behaviour.
24. Lickert H., Cox B., Wehrle C., Taketo M.M., Kemler R., and Rossant J. Dissecting Wnt/β-catenin signaling during gastrulation using RNA interference in mouse embryos. Development 132 (2005) 2599-2609
25. Kemp C., Willems E., Abdo S., Lambiv L., and Leyns L. Expression of all Wnt genes and their secreted antagonists during mouse blastocyst and postimplantation development. Dev Dyn 233 (2005) 1064-1075
26. Mohamed O.A., Clarke H.J., and Dufort D. β-catenin signaling marks the prospective site of primitive streak formation in the mouse embryo. Dev Dyn 231 (2004) 416-424
27. Liu P., Wakamiya M., Shea M.J., Albrecht U., Behringer R.R., and Bradley A. Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22 (1999) 361-365
28. Kelly O.G., Pinson K.I., and Skarnes W.C. The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 131 (2004) 2803-2815
29. Lickert H., Kutsch S., Kanzler B., Tamai Y., Taketo M.M., and Kemler R. Formation of multiple hearts in mice following deletion of β-catenin in the embryonic endoderm. Dev Cell 3 (2002) 171-181
30. Pfendler K.C., Catuar C.S., Meneses J.J., and Pedersen R.A. Overexpression of Nodal promotes differentiation of mouse embryonic stem cells into mesoderm and endoderm at the expense of neuroectoderm formation. Stem Cells Dev 14 (2005) 162-172
31. Tada S., Era T., Furusawa C., Sakurai H., Nishikawa S., Kinoshita M., Nakao K., Chiba T., and Nishikawa S. Characterization of mesendoderm: a diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 132 (2005) 4363-4374. During the Nodal- or Activin-induced differentiation of embryonic stem cells, a population of cells displaying dual potential to become mesoderm or definitive endoderm has been identified. It is believed that this cell population is the in vitro counterpart of the putative mesendodermal progenitor that is present in the primitive streak of the gastrulating mouse embryo.
32. Yasunaga M., Tada S., Torikai-Nishikawa S., Nakano Y., Okada M., Jakt L.M., Nishikawa S., Chiba T., and Era T. Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells. Nat Biotechnol 23 (2005) 1542-1550
33. Beck S., Le Good J.A., Guzman M., Haim N.B., Roy K., Beermann F., and Constam D.B. Extraembryonic proteases regulate Nodal signalling during gastrulation. Nat Cell Biol 4 (2002) 981-985
34. Lu C.C., and Robertson E.J. Multiple roles for Nodal in the epiblast of the mouse embryo in the establishment of anterior-posterior patterning. Dev Biol 273 (2004) 149-159
35. Perea-Gomez A., Vella F.D., Shawlot W., Oulad-Abdelghani M., Chazaud C., Meno C., Pfister V., Chen L., Robertson E., Hamada H., et al. Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev Cell 3 (2002) 745-756
36. Winnier G., Blessing M., Labosky P.A., and Hogan B.L. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9 (1995) 2105-2116
37. Mishina Y., Suzuki A., Ueno N., and Behringer R.R. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev 9 (1995) 3027-3037
38. Davis S., Miura S., Hill C., Mishina Y., and Klingensmith J. BMP receptor IA is required in the mammalian embryo for endodermal morphogenesis and ectodermal patterning. Dev Biol 270 (2004) 47-63
39. Beppu H., Kawabata M., Hamamoto T., Chytil A., Minowa O., Noda T., and Miyazono K. BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev Biol 221 (2000) 249-258
40. Yoshikawa Y., Fujimori T., McMahon A.P., and Takada S. Evidence that absence of Wnt-3a signaling promotes neuralization instead of paraxial mesoderm development in the mouse. Dev Biol 183 (1997) 234-242
41. Chu J., Ding J., Jeays-Ward K., Price S.M., Placzek M., and Shen M.M. Non-cell-autonomous role for Cripto in axial midline formation during vertebrate embryogenesis. Development 132 (2005) 5539-5551
42. Mesnard D., Filipe M., Belo J.A., and Zernicka-Goetz M. The anterior-posterior axis emerges respecting the morphology of the mouse embryo that changes and aligns with the uterus before gastrulation. Curr Biol 14 (2004) 184-196
43. Perea-Gomez A., Camus A., Moreau A., Grieve K., Moneron G., Dubois A., Cibert C., and Collignon J. Initiation of gastrulation in the mouse embryo is preceded by an apparent shift in the orientation of the anterior-posterior axis. Curr Biol 14 (2004) 197-207
44. Lawson K.A., Meneses J.J., and Pedersen R.A. Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113 (1991) 891-911
45. Takaoka K., Yamamoto M., Shiratori H., Meno C., Rossant J., Saijoh Y., and Hamada H. The mouse embryo autonomously acquires anterior posterior polarity at implantation. Dev Cell 10 (2006) 451-459. This study reveals that asymmetric Lefty1 expression in the primitive endoderm can be detected as early as the blastocyst stage and does not require interaction with the uterine environment through implantation. Asymmetric Lefty1 expression is induced by Nodal signalling, which is mediated by the transcription factor FoxH1.
46. Richardson L., Torres-Padilla M.E., and Zernicka-Goetz M. Regionalised signalling within the extraembryonic ectoderm regulates anterior visceral endoderm positioning in the mouse embryo. Mech Dev 123 (2006) 288-296. This study shows that the posterior but not the anterior region of the ExE is responsible for the regionalization of the AVE. The prospective posterior ExE exerts its patterning activity in a narrow time-window, prior to the migration of the presumptive AVE from the distal region of the embryo.