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Cell Fate, Morphogenetic Movement and Population Kinetics of Embryonic Endoderm at the Time of Germ Layer Formation in the Mouse

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Cell Fate, Morphogenetic Movement and Population Kinetics of Embryonic Endoderm at the Time of Germ Layer Formation in the Mouse Development 101, 627-652 (1987) 627 Printed in Great Britain (G) The Company of Biologists Lunited 1987 Cell fate, morphogenetic movement and population kinetics of embryonic endoderm at the time of germ layer formation in the mouse KIRSTIE A. LAWSON1 and ROGER A. PEDERSEN23 with an appendix by SARA VAN DE GEER4 lHubrecht Laboratory, Netherlands Institute for Developmental Biology, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands, 2Laboratory of Radiobtology and Environmental Health and ^Department of Anatomy, University of California, San Francisco, CA 94143, USA ^Centre for Mathematics and Computer Science, Knuslaan 413, 1098 SJ Amsterdam, The Netherlands Summary The fate of the embryonic endoderm (generally called and early-streak-stage embryos is heterogeneous in its visceral embryonic endoderm) of prestreak and early germ layer fate. Whereas the germ layer location of primitive streak stages of the mouse embryo was descendants from anterior sites did not differ after 1 studied in vitro by microinjecting horseradish peroxi- day from that expected from the initial controls dase into single axial endoderm cells of 6 7-day-old (approx. 90 % exclusively in endoderm), only 62 % of embryos and tracing the labelled descendants either the successfully injected posterior sites resulted in through gastrulation (1 day of culture) or to early labelled cells exclusively in endoderm; the remainder somite stages (2 days of culture). contributed partially or entirely to ectoderm and Descendants of endoderm cells from the anterior mesoderm. This loss from the endoderm layer was half of the axis were found at the extreme cranial end compensated by posterior-derived cells that remained of the embryo after 1 day and in the visceral yolk sac in endoderm having more surviving descendants (8-4 h endoderm after 2 days, i.e. they were displaced population doubling time) than did anterior-derived anteriorly and anterolaterally. Descendants of cells cells (10-5 h population doubling time). There was no originating over and near the anterior end of the early indication of cell death at the prestreak and early primitive streak, i.e. posterior to the distal tip of the streak stages; at least 93 % of the cells were prolifer- egg cylinder, were found after 1 day over the entire ating and more than half of the total axial population embryonic axis and after 2 days in the embryonic were in, or had completed, a third cell cycle after 22 h endoderm at the anterior intestinal portal, in the culture. foregut, along the trunk and postnodally, as well as We suggest that the visceral embryonic endoderm, anteriorly and posteriorly in the visceral yolk sac. derived from the primitive endoderm of the late Endoderm covering the posterior half of the early blastocyst, is displaced onto the yolk sac by a new primitive streak contributed to postnodal endoderm population of endoderm inserted from epiblast at the after 1 day (at the late streak stage) and mainly to anterior end of the early primitive streak. This cell posterior visceral yolk sac endoderm after 2 days. population has colonized the axial endoderm by the Clonal descendants of axial endoderm were located neural plate stage and contributes to the embryonic after 2 days either over the embryo or in the yolk sac; endoderm of the early somite embryo. the few exceptions spanned the caudal end of the embryo and the posterior yolk sac. Key words: cell fate, morphogenetic movement, cell proliferation, embryonic endoderm, mouse embryo, The clonal analysis also showed that the endoderm postimplantation development, cell lineage, horseradish layer along the posterior half of the axis of prestreak- peroxidase, microinjection. Introduction layer of primitive endoderm that faces the blastocyst cavity and a core of primitive ectoderm (Nadijcka & During late preimplantation development of the Hillman, 1974; Enders, Given & Schlafke, 1978). The mammal, the inner cell mass differentiates into a fate of the primitive endoderm has been studied in 628 K. A. Lawson, R. A. Pedersen and S. van de Geer rodent embryos using preimplantation injection streak from embryos on the 9th day of gestation also chimaeras and by analysis of tissue potency at early contributed to gut endoderm (Tarn & Beddington, postimplantation stages. Primitive endoderm cells 1987). No gut derivatives were formed by distal isolated from 4-5 day of gestation mouse embryos and donors transferred to other host locations or from injected into 3-5-day host blastocysts formed only other donor sites transferred to a distal host location visceral and parietal yolk sac endoderm (Gardner (Beddington, 1982). These apparent constraints in & Papaioannou, 1975; Gardner & Rossant, 1979). contribution to gut tissues in the postimplantation Single primitive endoderm cells from 5-5-day donors chimaeras imply that formation of the definitive and groups of visceral embryonic endoderm cells endoderm in the intact mouse embryo is a precisely from 6-5- or 7-5-day embryos formed both parietal organized morphogenetic process. and visceral endoderm descendants, leading to the We have recently described the fate of axial embry- concept that the primitive endoderm lineage con- onic endoderm cells in midstreak and late streak/ tains stem cells capable of forming both cell types neural plate stage (7-5 day) mouse embryos using (Gardner, 1982, 1984). Cells isolated from the primi- microinjected horseradish peroxidase (HRP) as a tive ectoderm layer at 4-5 days and injected into host short-term lineage tracer (Lawson, Meneses & Peder- blastocysts were capable of forming all the fetal sen, 1986). This lineage tracer (Weisblat, Sawyer & tissues, including the embryonic gut, as well as Stent, 1978; Balakier & Pedersen, 1982), while lack- extraembryonic mesoderm and amniotic ectoderm. ing some of the advantages of a cell-autonomous There is no evidence from the blastocyst injection genetic marker (Rossant, Vijh, Siracusa & Chapman, studies (using glucose phosphate isomerase as a 1983; Gardner, 1984), nonetheless facilitates labelling lineage tracer) that visceral embryonic endoderm of single cells in situ without disrupting the native cell contributes any descendants to the fetal gut at mid- relationships of the intact embryo. Our analysis gestation, although a minor contribution might not revealed that the visceral embryonic endoderm (here- have been detected with this approach (reviewed by after called embryonic endoderm) is a mixed popu- Rossant, 1986). lation at midstreak and late streak stages, consisting When visceral embryonic and extraembryonic en- of progenitors of visceral extraembryonic (yolk sac) doderm are isolated from primitive-streak-stage rat endoderm and progenitors of the embryonic gut and mouse embryos, they have extremely limited endoderm. Based on the relative locations of these tissue potency, as determined by ectopic grafting. distinct progenitor cell populations, we proposed that Visceral embryonic or extraembryonic endoderm the progenitors of embryonic foregut endoderm either yielded only parietal endoderm-like cells emerge from the epiblast earlier in gastrulation, (Solter & Damjanov, 1973; Diwan & Stevens, 1976) replacing the primitive endoderm cells, which con- or did not survive in ectopic grafts (Levak-Svajger & tribute to yolk sac endoderm. This proposal em- Svajger, 1971, 1974). By contrast, embryonic ecto- phasizes the similarity between rodent and avian derm isolated from mouse and rat embryos before embryos, as previously noted (Levak-Svajger & and during gastrulation and grafted to ectopic sites Svajger, 1974; Rossant & Papaioannou, 1977; has broad tissue potency (Grobstein, 1952; Levak- Gardner, 1978; Beddington, 19836). Svajger & Svajger, 1971; Diwan & Stevens, 1976). In the current study, we extend this approach to Both distal and anterior regions of the mouse embry- prestreak- and early-streak-stage mouse embryos (6-7 onic ectoderm isolated at the primitive streak stage days) to trace the origin of the axial endoderm of and grafted to ectopic sites formed midgut and midstreak- and late-streak-stage embryos and to foregut derivatives (Beddington, 1983a). Taken examine the extent of the contribution of embryonic together with the blastocyst injection studies, these endoderm to the yolk sac. This was accomplished by patterns of postimplantation tissue potency imply marking axial endoderm cells with HRP at prestreak that the primitive ectoderm or its derivatives, rather and early streak stages, culturing embryos for 1 or 2 than the primitive endoderm, gives rise to the defini- days, then determining the location of labelled de- tive fetal gut tissues. scendants. This approach also provides information Little is known about when the definitive endo- about the morphogenetic movements and population derm forms (reviewed by Beddington, 1983b, 1986). dynamics of the embryonic endoderm during this When postimplantation mouse chimaeras were period. formed by transferring small groups of [3H]thymi- dine-labelled donor ectoderm cells from the distal Materials and methods region of the egg cylinder on the 8th day of gestation to a distal host site, labelled descendants were Embryos detected in the embryonic gut (specifically, midgut) Noninbred Swiss mice of the Dub:(ICR) strain were used. (Beddington, 1981); orthotopic grafts of the primitive Gestation was considered to have begun at midnight before Cell fate in mouse endoderm 629 the morning on which a copulation plug was found. Females Cells containing HRP were detected by treating the intact were killed by cervical
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