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The Cleavage Stage Origin of Spemann's Organizer: Analysis Of Development 120, 1179-1189 (1994) 1179 Printed in Great Britain © The Company of Biologists Limited 1994 The cleavage stage origin of Spemann’s Organizer: analysis of the movements of blastomere clones before and during gastrulation in Xenopus Daniel V. Bauer1, Sen Huang2 and Sally A. Moody2,* 1Department of Anatomy and Cell Biology, University of Virginia 2Department of Anatomy and Neuroscience Program, The George Washington University Medical Center, 2300 I Street, NW Washington, DC 20037, USA *Author for correspondence SUMMARY Recent investigations into the roles of early regulatory the ventral animal clones extend across the entire dorsal genes, especially those resulting from mesoderm induction animal cap. These changes in the blastomere constituents or first expressed in the gastrula, reveal a need to elucidate of the animal cap during epiboly may contribute to the the developmental history of the cells in which their tran- changing capacity of the cap to respond to inductive growth scripts are expressed. Although fates both of the early blas- factors. Pregastrulation movements of clones also result in tomeres and of regions of the gastrula have been mapped, the B1 clone occupying the vegetal marginal zone to the relationship between the two sets of fate maps is not become the primary progenitor of the dorsal lip of the clear and the clonal origin of the regions of the stage 10 blastopore (Spemann’s Organizer). This report provides embryo are not known. We mapped the positions of each the fundamental descriptions of clone locations during the blastomere clone during several late blastula and early important periods of axis formation, mesoderm induction gastrula stages to show where and when these clones move. and neural induction. These will be useful for the correct We found that the dorsal animal clone (A1) begins to move targeting of genetic manipulations of early regulatory away from the animal pole at stage 8, and the dorsal animal events. marginal clone (B1) leaves the animal cap by stage 9. The ventral animal clones (A4 and B4) spread into the dorsal Key words: fate map, epiboly, dorsal lip, cell lineage, animal cap animal cap region as the dorsal clones recede. At stage 10, assays. INTRODUCTION of the gastrula that express unique gene products could be iden- tified. Since many experiments use the cleavage stage embryo Gastrulation movements morphologically transform the for targeting foreign gene products, and rely on changes in fate amphibian embryo from a ball of cells into an elongated for the interpretation of gene function, the comprehensive map tadpole with distinct dorsal-ventral and anterior-posterior axes. of blastomere clones at blastula and gastrula stages will allow In addition, during this time, many tissue and phenotype spec- investigators to target correct progenitors for gene misexpres- ifications occur, and many region-specific regulatory genes are sion, ‘knockout,’ and dominant negative experiments. This first expressed, e.g., Xlim-1, fork head, and goosecoid (Taira study demonstrates that some clones move prior to gastrula- et al., 1992; Dirksen and Jamrich, 1992; Blumberg et al., tion, such that important developmental regions of the embryo 1991). Identification of the developmental history of the cells change in composition over time. For example, the animal cap occupying the various regions of the gastrula is fundamental is used to assay the inductive capacity of exogenous molecules for understanding the role of these genes and the upstream or ectopically expressed gene products (e.g., Slack et al., 1987; events that lead to their region-specific expression. Currently, Kimelman and Kirschner, 1987; Smith, 1987; Rosa et al., we know the developmental fate of the early cleavage stage 1988; Sokol and Melton, 1992; Christian et al., 1992). Inves- blastomeres (Hirose and Jacobson, 1979; Jacobson and Hirose, tigators have used animal caps of various sizes and stages, 1981; Jacobson, 1983; Dale and Slack, 1987; Moody, 1987a,b; which can lead to different results (see Dawid, 1991). Our Moody and Kline, 1990), and there is a detailed fate map of study demonstrates that animal caps of different sizes at the early gastrula (Keller, 1975, 1976). However, there are few different stages in fact contain different clones. Another data that relate these two maps; we do not know where the blas- important developmental region is Spemann’s Organizer, the tomere clones are located in the gastrula. In this study, the inducer of the nervous system. This region has been identified locations of the blastomere clones prior to and during gastru- in the stage 10 embryo (Keller, 1976), but investigators lation were mapped so that the existing early and late maps disagree on the identity of the cleavage stage progenitors could be integrated and the blastomere progenitors of regions (Gimlich, 1986; Takasaki, 1987; Masho, 1988). It often has 1180 D. V. Bauer, S. Huang and S. A. Moody Fig. 1. The location and nomenclature of blastomeres used in this study. (A) 16-cell embryo (Hirose and Jacobson, 1979). (B) 32-cell embryo labeled with the nomenclature of Jacobson and Hirose (1981). (C) 32-cell embryo labeled with the nomenclature of Nakamura and Kishiyama (1971). been assumed that Spemann’s Organizer region arises from the 8 and 9, video images of sagittal sections were measured with a vegetal hemisphere of the cleavage stage embryo (see review Hamamatsu Argus-10 image processor. Sections were chosen from Elinson and Kao, 1989) but, in fact, our initial studies (Hainski each embryo (four at stage 8 and five at stage 9) that contained the and Moody, 1992) and those of others (Takasaki, 1987; Masho, largest area of the labeled B1 clone. The circumference of the tissue 1988) show that most of the dorsal blastopore lip actually section was divided into 360° of arc. The animal-most and vegetal- arises from an animal hemisphere blastomere. In the present most boundaries of the B1 clone were measured relative to a linear projection of the floor of the blastocoel to the surface. These bound- study, we detail the blastomeres (from 16- and 32-cell aries were expressed in degrees of arc. embryos) that contribute to the Organizer region, as well as the lateral and ventral lips, and provide a developmental history of the pregastrulation movements of these important clones. RESULTS MATERIALS AND METHODS The positions of clones change before gastrulation Although the appearance of the dorsal lip of the blastopore at Embryos were obtained from natural matings of adult frogs that had stage 10 is commonly used as the indicator of the onset of gas- been induced to mate with chorionic gonadotropin (Sigma). Fertilized trulation, Xenopus blastula cells become motile at stage 8 eggs were dejellied and selected for lineage dye injections as detailed (Newport and Kirschner, 1982), clones have intermixed by in previous reports (Moody, 1987a,b). Only embryos with stereotyped three cell diameters by stage 9 (Wetts and Fraser, 1989) and cleavage furrows (Fig. 1) were used in order to label consistently the same progenitor in all embryos. Embryos were held in Steinberg’s cellular events indicative of gastrulation movements begin solution until they reached the 16- or 32-cell stage.To study clones nearly an hour before stage 10 (Keller, 1978). We investigated derived from the 16-cell embryo, each of the eight different blas- both the movements of each blastomere clone and the mixing tomeres (Fig. 1A) was injected with 1 nl of 5% horseradish peroxi- between clones before stage 10 to determine whether these dase (HRP, Boeringer-Mannheim). To study clones derived from the movements reorganize the clones prior to the invagination at 32-cell embryo, two neighboring blastomeres were injected, one with the dorsal blastopore lip. 1 nl of 0.5% Texas Red-dextran-amine (TRDA, Molecular Probes) The stage 7 clones were in the original position and wedge and the other with 2 nl of 0.5% fluorescein-dextran-amine (FDA, shape of the injected blastomere (Figs 2,3). Clones of animal Molecular Probes). Only the midline blastomeres of the three animal- blastomeres interdigitated along their edges with neighboring most tiers were examined (Fig. 1B,C). For easier reading, the nomen- unlabeled cells, especially at the marginal zone border of the clature of Nakamura (Fig. 1C) is used in the text when referring to 32-cell blastomeres. However, Jacobson’s nomenclature is illustrated clone (Fig. 3). The D1.1 clone was the most intermixed (Fig. in Fig. 1B so that reference can be made to mother cells (Fig. 1A) and 3B), especially with the contralateral D1.1 clone (Fig. 4). to the 32-cell fate map of Moody (1987b). Clones of vegetal blastomeres had little mixing at the borders Injected embryos were raised in Steinberg’s solution, the fluores- (Figs 2,3). At stage 8 some clones began to shift positions. The cent ones in the dark, at room temperature. Embryos were fixed, at A4 clone extended a few cell diameters across the geometric intervals from stage 7 to stage 13 (Nieuwkoop and Faber, 1967), in animal pole into the dorsal area, while the animal-most descen- 4% paraformaldehyde in 0.1 M P04 buffer (pH 7.4). Most of the HRP- dants of A1 receded one or two cell diameters away from the labeled embryos were processed as whole mounts. They were washed, animal pole (Figs 5,6B). In addition, all of the clones mixed ′ reacted in 3,3 -diaminobenzidine (Sigma), dehydrated, cut in half and along their borders with neighboring clones at a depth of one embedded in clear plastic (Eukitt, Calibrated Instruments, Inc.). Most or two cell diameters (Figs 5,6B). of the fluorescently labeled embryos were sectioned at 17 µm with a cryostat, washed and coverslipped with Tris/glycerol. For stages 7- At stage 9, several of the clones had moved from their 10, the animal pole was identified by determining the center of the original positions.
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