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Clonal Analysis of Epiblast Fate During Germ Layer Formation in the Mouse Embryo

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Clonal Analysis of Epiblast Fate During Germ Layer Formation in the Mouse Embryo Development 113, 891-911 (1991) 891 Printed in Great Britain © The Company of Biologists Limited 1991 Clonal analysis of epiblast fate during germ layer formation in the mouse embryo KIRSTIE A. LAWSON1, JUANITO J. MENESES2 and ROGER A. PEDERSEN23 1Hubrecht Laboratory, Netherlands Institute for Developmental Biology, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands 2Laboratory of Radiobiology and Environmental Health, University of California, San Francisco, CA 94143, USA 3Department of Anatomy, University of California, San Francisco, CA 94143, USA Summary The fate of cells in the epiblast at prestreak and early single germ layer or to extraembryonic mesoderm, primitive streak stages has been studied by injecting indicating that these lineages are not separated at the horseradish peroxidase (HRP) into single cells in situ of beginning of gastrulation. 6.7-day mouse embryos and identifying the labelled The embryonic axis lengthened up to the neural plate descendants at midstreak to neural plate stages after one stage by (1) elongation of the primitive streak through day of culture. progressive incorporation of the expanding lateral and Ectoderm was composed of descendants of epiblast initially more anterior regions of epiblast and, (2) progenitors that had been located in the embryonic axis expansion of the region of epiblast immediately cranial anterior to the primitive streak. Embryonic mesoderm to the anterior end of the primitive streak. The was derived from all areas of the epiblast except the population doubling time of labelled cells was 7.5 h; a distal tip and the adjacent region anterior to it: the most calculated 43 % were in, or had completed, a 4th cell anterior mesoderm cells originated posteriorly, travers- cycle, and no statistically significant regional differences ing the primitive streak early; labelled cells in the in the number of descendants were found. This clonal posterior part of the streak at the neural plate stage were analysis also showed that (1) growth in the epiblast was derived from extreme anterior axial and paraxial noncoherent and in most regions anisotropic and epiblast progenitors; head process cells were derived directed towards the primitive streak and (2) the midline from epiblast at or near the anterior end of the primitive did not act as a barrier to clonal spread, either in the streak. Endoderm descendants were most frequently epiblast in the anterior half of the axis or in the primitive derived from a region that included, but extended streak. These results taken together with the fate map beyond, the region producing the head process: descend- indicate that, while individual cells in the epiblast sheet ants of epiblast were present in endoderm by the behave independently with respect to their neighbours, midstreak stage, as well as at later stages. Yolk sac and morphogenetic movement during germ layer formation amnion mesoderm developed from posterolateral and is coordinated hi the population as a whole. posterior epiblast. The resulting fate map is essentially the same as those of the chick and urodele and indicates that, despite geometrical differences, topological fate Key words: germ layer formation, mouse embryo, cell fate, relationships are conserved among these vertebrates. fate map, cell lineage, embryo growth, gastrulation, Clonal descendants were not necessarily confined to a microinjection, HRP. Introduction cysts: of the subsequent clones analysed at mid- gestation, a minority of those derived from ICM cells The epiblast or primitive ectoderm of the mouse gave rise to derivatives of both epiblast and hypoblast. embryo is the sole source of all the fetal tissues, both Whereas recognisable epiblast contributed to fetal somatic and germline, and it also forms the amnion tissues, hypoblast contributed to extraembryonic endo- ectoderm and all the extraembryonic mesoderm derm, and neither epiblast nor hypoblast had descend- (Gardner and Papaionnou, 1975; Gardner and Rossant, ants in both fetus and extraembryonic endoderm 1979; Gardner et al. 1985). Allocation of cells in the (Gardner and Rossant, 1979; Gardner, 1985). Fetal ICM (inner cell mass) to either epiblast or hypoblast clones were widely distributed through many tissues (primitive endoderm) during the periimplantation and over all three germ layers (Beddington et al. 1989). period at 4i days of gestation has been inferred from The establishment and divergence of embryonic cell chimaeras made by injecting single cells into blasto- lineages in the postimplantation conceptus cannot be 892 K. A. Lawson and others followed using blastocyst chimaeras because epiblast presumptive fate can be mapped at the onset of cells from 5i days gestation and older embryos do not gastrulation. develop in the blastocyst environment (Gardner et al. Gastrulation involves the formation of mesoderm 1985; reviewed by Rossant, 1986). Experiments in and definitive endoderm from the epiblast: its first which murine epiblasts were transferred to ectopic sites manifestation is the initiation of the primitive streak demonstrated the potency of the epiblast to form locally at the junction of the epiblast and extraembry- derivatives of all three germ layers (reviewed by onic ectoderm (Tarn and Meier, 1982; Hashimoto and Beddington, 1986; Svajger et al. 1986), this capacity Nakatsuji, 1989). The appearance of the primitive being present in gastrulating (Grobstein, 1952; Levak- streak visibly establishes the anterior-posterior axis of Svajger and sVajger, 1974; Beddington, 1983a) as well the embryo in the hitherto radially symmetrical cup- as preprimitive-streak-stage embryos (Diwan and Ste- shaped epiblast, although there is morphological vens, 1976; Levak-Svajger and Svajger, 1971). No evidence that this axis is already specified at the time of regional differences in the histogenic capacity of the implantation (Smith, 1980, 1985). Mesoderm forms epiblast were found (Svajger et al. 1981; Beddington, from the edge of the primitive streak, according to 1983a). However, heterotopic transplants of epiblast at Poelmann (1981a) by delamination without subsequent the late primitive-streak stage into host embryos migration, while growth of the epiblast displaces the showed some restriction of potency and also position streak away from the already delaminated mesoderm. dependency for the development of some tissue types: The pattern in which the somitomeres (paraxial surface ectoderm developed from both orthotopic and mesoderm) are laid down between the midstreak and heterotopic grafts in an anterior position, and loose late streak stages supports this view (Tarn and Meier, mesoderm developed posteriorly; generally, heteroto- 1982). On the other hand, cinematography of gastrulat- pic grafts colonized a smaller range of tissue types than ing embryos has revealed mesoderm cells migrating expected from their grafted position and failed to form anteriorally and distally (Nakatsuji et al. 1986). Prolifer- tissue types expected from their site of origin but not ation kinetics are incompatible with the primitive streak appropriate to their grafted position (Beddington, 1981, acting as a stem cell population and exfoliating the 1982). About half a day later in development, when the entire mesoderm (Snow, 1977); but in the absence of neural folds have elevated and the foregut indentation cell labelling in situ, it is unclear whether the source of is evident, the epiblast/ectoderm has lost the capacity the mesoderm is the lateral epiblast (Poelmann, 1981a) to form endoderm derivatives in ectopic sites, but is still or all but the distal epiblast (Snow, 1977; Snow and able to form mesoderm (Levak-Svajger and Svajger, Bennett, 1978). 1974). These results indicate that the epiblast as a whole, or in substantial pieces, retains considerable The replacement of the visceral embryonic endo- potency until late in gastrulation. derm, derived from primitive endoderm, by definitive endoderm derived from the epiblast has been partly Labelled orthotopic grafts of the epiblast gave elucidated: histology (Jolly and F6rester-Tadie\ 1936; sufficiently consistent results (Beddington, 1981, 1982; Snell and Stevens, 1966; Poelmann, 19816; Lamers etal. Copp et al. 1986; Tarn and Beddington, 1987; Tarn, 1987), labelling (Lawson et al. 1986; Kadokawa et al. 1989) for partial maps of presumptive fate of the late- 1987), orthotopic transplants (Beddington, 1981) and streak-stage epiblast to be drawn (Beddington, 19836; transplants to ectopic sites (Levak-Svajger and Svajger, Tarn, 1989). Full thickness explants, i.e. explants 1974; Beddington, 1983a) all indicate that definitive containing both epiblast and visceral endoderm from endoderm is derived from the same population of cells midstreak-stage embryos, or containing epiblast, meso- as the notochord, i.e. the head process or anterior derm and endoderm from late-streak-stage embryos, extension of the primitive streak, and forms at least part showed pronounced regional autonomy in vitro and the of the axial endoderm at the neural plate stage. fate map obtained (Snow, 1981) is consistent with the Experiments in which single endoderm cells were data from the orthotopic transplants of epiblast. These labelled in situ and their descendants traced to early results, complementing the potency experiments, in somite stages indicate that, already during gastrulation, which normal cell relationships were disrupted, suggest there is a subpopulation of endoderm cells that will that maintenance of tissue architecture and local cell colonise the foregut
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