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Mammalian Development: New Trick for an Old Dog Anthony Graham

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Mammalian Development: New Trick for an Old Dog Anthony Graham View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Dispatch R401 Mammalian development: New trick for an old dog Anthony Graham A recent study has shown that the T-box gene Xenopus mesoderm differentiation [2]. If eomesodermin is eomesodermin, which was first identified in Xenopus, ectopically expressed in animal caps, then it induces the not only plays a conserved role in vertebrates directing transcription of early mesodermal genes. Moreover, Eome- gastrulation, but interestingly in mammals has acquired sodermin acts in a concentration-dependent manner, with a new function in the development of the trophoblast. higher levels inducing more dorsal cell types. Correspond- ingly, if eomesodermin function is interfered with, then Address: Molecular Neurobiology Group, 4th Floor New Hunts House, Guys Campus, Kings College London, London SE1 9RT, UK. embryonic development is arrested during gastrulation, E-mail: [email protected] and mesoderm formation is severely perturbed. Current Biology 2000, 10:R401–R403 The mouse eomesodermin gene shares many characteristics 0960-9822/00/$ – see front matter with its Xenopus orthologue, displaying a high degree of © 2000 Elsevier Science Ltd. All rights reserved. sequence relatedness — up to 95% amino acid sequence identity in the T-box region [3,5] — as well as prominent Mammals are viviparous, their embryos developing and expression in the mesodermal cells of the gastrula stage being nurtured within the safe uterine environment. This embryo. The mouse eomesodermin gene is notable, reproductive strategy has been very successful, as it greatly however, as it is also expressed at the very early blastocyst increases the chances of survival of the neonate, and it has stages of development [3,6,7]. The blastocyst consists of involved major adaptations of early embryogenesis. In con- two groups of cells, the internally located inner cell mass trast to other vertebrate classes, the early phase of mam- and the externally located trophectoderm (Figure 1), and malian development is not concerned with establishing it is this latter group of cells which first expresses eomeso- and organising the embryonic body plan, but rather time is dermin. The specification of trophectoderm versus the spent generating the various extra-embryonic tissues which inner cell mass is the earliest cell-fate choice in mam- are essential for the embryo to implant into the uterine malian development, and the one which separates the wall [1]. Obviously, if one is to understand how the early cells of the trophoblast lineage, which form the foetal events in mammalian development are controlled, one portion of the placenta, from the embryonic lineages. must examine mammalian embryos, but, as with many other aspects of developmental biology, insights can come The function of eomesodermin in this peculiarly mammalian from unexpected places. Eomesodermin, a T-box gene first phase of development has recently been uncovered by characterised in Xenopus as being a key regulator of meso- mutational analysis in mice [3]. While heterozygous derm formation [2], has recently been functionally animals, which carry a normal and a mutated form of eome- analysed in mice [3]. This work has shown that, beside sodermin, are healthy and fertile, they never yield any playing a conserved role in mesoderm formation, this gene homozygous mutant offspring when crossed, suggesting has also acquired a novel function in regulating one of the that eomesodermin function is absolutely required for earliest events in mammalian development — the genera- normal development. Morphological analysis of mutant tion of the trophoblast lineage. embryos showed that, in the absence of eomesodermin, embryos arrest soon after implantation. Eomesodermin was first isolated in Xenopus as part of a screen for clones that were specifically expressed in the Eomesodermin mutant embryos reach the blastocyst stage, gastrula stage embryo [2]. An interesting feature of this generating trophectoderm and the inner cell mass, but the clone, from amongst the 120 that were initially isolated, trophectodermal cells are unable to progress and form the was that it was expressed in the equatorial region of the trophoblast [3]. If normal blastocyst embryos are grown early gastrula. In fact, further expression analysis demon- in vitro, they hatch from the zona pellucida, which has strated that this gene is expressed in all mesoderm cells, protected them since fertilisation, and settle, and which in Xenopus lie as a band at the equator of the early trophoblast cells readily form and spread across the embryo, and it was from this characteristic that the name culture dish. But although cultured mutant embryos hatch of this gene arises — from the Greek Eoσ, for dawn, indi- normally, they maintain their blastocyst morphology and cating its early expression. The sequence of this clone trophoblast cells never form. It has been shown that tro- revealed that the gene encodes a member of the T-box phoblast stem cell lines can be derived from blastocysts in family of transcription factors [4], which are defined by a culture, that these cells strongly express eomesodermin and shared DNA binding domain, and functional analysis has that their maintenance requires the presence of the suggested that this gene plays a key role in regulating fibroblast growth factor FGF-4 [8]. The lack of production R402 Current Biology Vol 10 No 11 Figure 1 One can create chimeras in which the extra-embryonic tissues are wild-type, but the embryonic tissues are mutant, (a) by introducing mutant embryonic stem cells, or inner cell masses, into a tetraploid host; tetraploid cells can only gen- Inner cell mass erate extra-embryonic tissues. When this is done, the chimeras show no obvious abnormalities at early gastrula- tion stages, indicating that the wild-type cells have formed the trophoblast [3]. At slightly later stages, however, defects become apparent. Although the primitive streak forms, it does not elongate and the node, the organising center of the Trophectoderm mammalian embryo, is absent from its anterior end [3]. The fact that the primitive streak forms demonstrates that the necessary early mesoderm inducing signals are present, but (b) it seems that the mesoderm never emerges from the primi- Visceral Proximal tive streak. Analysis of the prospective neural tissue of the endoderm Mesoderm mutants also reveals that the anterior patterning of this Primitive embryonic layer is slightly perturbed [3]. streak This results mirrors what was observed in Xenopus, suggesting that eomesodermin has a conserved role in gastrulation and that the absence of its function results in gastrulation arrest. This phenotype could, however be due Anterior to this gene being necessary for mesoderm differentiation Posterior or, more specifically, for the recruitment of prospective mesodermal cells into the primitive streak, or indeed both. While the experiments in Xenopus do not allow us to differ- entiate between these two scenarios, the analytical tools available in mice do. In chimeras made from diploid wild- Epiblast Distal type cells and mutant cells, mesoderm formation is partially Current Biology rescued [3]. In this situation, wild-type and mutant cells intermingle in the epiblast, but only the wild-type cells (a) Schematic diagram of a blastocyst — a 3.5 day mouse embryo. The migrate through the primitive streak; the eomesodermin locations of the inner cell mass and the trophectoderm are highlighted. (b) Schematic diagram of a 6.5 day mouse embryo during the early mutant cells remain within the epiblast. In normal develop- period of gastrulation. As gastrulation proceeds, the cells of the ment, the differentiation of cells into mesodermal tissues presumptive mesodermal cells of epiblast move to and through the follows from their migration through the primitive streak, primitive streak, shown by blue arrows. The primitive streak itself will and so the block in early gastrulation observed in the eome- also extend anteriorly, indicated by the red arrow, and at its anterior end the node will be established. sodermin mutants does not tell us as whether or not this gene is also necessary for the differentiation of mesodermal cell types. But this issue can be addressed by producing of trophoblast cells from eomesodermin mutant embryos teratomas from the mutant cells, and analysing the range of cannot be overcome by the addition of FGF-4, however, differentiated cell types that are produced. When this is and it seems that eomesodermin must be required cell done, the eomesodermin mutant cells form muscle, cartilage autonomously for the initial transition from trophecto- and haemopoetic tissue. It thus seems that the function of derm to trophoblast [3]. eomesodermin during gastrulation is in directing the migra- tion of cells from the epiblast into the primitive streak. While the fact that eomesodermin is required for the development of the trophoblast is in itself of great inter- The results from the mutational analysis of the function of est, the early lethality that results in the absence of this eomesodermin in mice [3] are interesting for a number of gene means that one cannot quite so straightforwardly reasons. They confirm that this gene has a prominent role analyse its later roles in development. Of particular inter- in controlling gastrulation across the vertebrates. The est would be to probe the role of this gene in gastrulation results also, however,
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