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Hensen's Node Induces Neural Tissue in Xenopus Ectoderm. Implications for the Action of the Organizer in Neural Induction

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Hensen's Node Induces Neural Tissue in Xenopus Ectoderm. Implications for the Action of the Organizer in Neural Induction Development 113, 1495-1505 (1991) 1495 Printed in Great Britain © The Company of Biologists Limited 1991 Hensen's node induces neural tissue in Xenopus ectoderm. Implications for the action of the organizer in neural induction C. R. KINTNER1 and J. DODD2 ^Molecular Neurobiology Laboratory, The Salk Institute, San Diego, CA 92186, USA 2Department of Physiology and Cellular Biophysics, Center for Neurobiology and Behavior, Columbia University, New York, NY 10032, USA Summary The development of the vertebrate nervous system is ectoderm to respond to Hensen's node extends much initiated in amphibia by inductive interactions between later in development than that to activin-A or to ectoderm and a region of the embryo called the induction by vegetal cells, and parallels the extended organizer. The organizer tissue in the dorsal lip of the competence to neural induction by axial mesoderm. The blastopore of Xenopus and Hensen's node in chick actions of activin-A and Hensen's node are further embryos have similar neural inducing properties when distinguished by their effects on lithium-treated ecto- transplanted into ectopic sites in then" respective em- derm. These results suggest that neural induction can bryos. To begin to determine the nature of the inducing occur efficiently in response to inducing signals from signals of the organizer and whether they are conserved organizer tissue arrested at a stage prior to gastrulation, across species we have examined the ability of Hensen's and that such early interactions in the blastula may be an node to induce neural tissue in Xenopus ectoderm. We important component of neural induction in vertebrate show that Hensen's node induces large amounts of embryos. neural tissue in Xenopus ectoderm. Neural induction proceeds in the absence of mesodermal differentiation and is accompanied by tissue movements which may Key words: neural induction, organizer, activin-A, reflect notoplate induction. The competence of the Hensen's node, notoplate. Introduction tissue when transplanted to ectopic sites in chick or amphibian embryos, respectively. In addition, both Vertebrate neural development begins when ectoderm tissues pattern the induced neural tissue along the on the dorsal side of the embryo is induced to form anterior-posterior axis (Spemann, 1931; Tsung et al., neural tissue. The neural inducer is a region of tissue, 1965; see Hara, 1978). The similarities in the properties known as the organizer, whose properties have been of the organizer in different vertebrate embryos defined by transplantation studies in several vertebrate suggests that the inducing signals underlying neural species. When the organizer is transplanted from one induction may be conserved. To examine this idea, we blastula to the ventral side of another, the host embryo have asked whether Xenopus ectoderm responds to the forms a second dorsal axis (Spemann and Mangold, organizer taken from the chick embryo as it does to its 1924). The nervous system in this second axis is derived own organizer. Chick Hensen's node was isolated and from host ectoderm which, in the absence of the graft, cultured with Xenopus ectoderm in a standard animal would have formed ventral epidermis. This result cap assay. The assay was carried out at room indicates that ectoderm can be induced to form neural temperature (approximately 22°C) such that the ecto- tissue upon appropriate interaction with the organizer, derm can respond to inducing signals while the chick an event that normally occurs only on the dorsal side of tissue is developmentally static. Thus tissue differen- the embryo. In amphibia, the organizer maps to the tiation and morphogenetic movements observed rep- dorsal lip of the blastopore (DLB), a region of the resent the response of Xenopus ectoderm, while the marginal zone of the blastula just above the first site of inducing signals detected in the assay can be attributed invagination at gastrulation. In birds, the organizer to Hensen's node tissue as it existed at the stage of maps to the anterior end of the primitive streak, a isolation from the embryo. region called Hensen's node (Waddington and Schmidt, We show that Xenopus ectoderm responds to 1933; see Hara, 1978). Hensen's node by forming large amounts of neural Both Hensen's node and the DLB induce neural tissue without detectably forming dorsal mesodermal 1496 C. R. Kintner and J. Dodd derivatives. The inducing activity of Hensen's node is embryos. In every assay the size of undigested probes for each different from the potent embryonic inducer, activin-A transcript used was measured on the same gel as the (Asashima et al., 1990; Eijnden-Van Raaij et al., 1990; experimental samples. This permitted us to determine Smith et al., 1990; Thompsen et al., 1990). In addition, whether probe escaped RNAase protection in any experimen- Hensen's node induces ectoderm to undergo morpho- tal samples. logical movements resulting in axial elongation in the Histology and immunohistochemistry absence of mesoderm. These results are discussed in the Recombinants were fixed in 3% trichloracetic acid at 4°C for light of the model in which an early interaction between 30 min. After extensive washing, they were dehydrated ectoderm and organizer tissue in the blastula is an through an ethanol series and embedded in paraffin using important component of neural induction in vertebrate standard procedures (Kintner, 1988). Tissue was sectioned at embryos. 10 fsm on a rotary microtome and mounted on gelatin-subbed slides. For histology, sections were stained with haematoxylin and eosin or Giemsa's stain. For immunohistochemistry, the Methods sections were dewaxed, labelled with monoclonal antibodies, using a fluorescein-labelled second antibody and counter- Animals and reagents stained with Hoechst dye. Monoclonal antibodies used were Embryos were obtained from Xenopus laevis adult frogs as follows: anti-NCAM (gift of Drs K. Sakaguchi and W. (NASCO and Xenopus 1) by hormone-induced egg-laying Harris, UCSD), 12/101 (Kintner and Brockes, 1985) and Not- and in vitro fertilization using standard protocols. Animal 1 (Placzek et al., 1990; Yamada et al., 1991). caps were dissected from appropriately staged (Nieuwkoop and Faber, 1967) embryos in 0.5x MMR containing penicillin and streptomycin, as previously described (Dixon and Results Kintner, 1989). For lithium treatment, embryos were incu- bated at the 64 cell stage with 0.25 M LiCl for 10 minutes and Hensen's node induces neural tissue then washed extensively with 0.5 x MMR. To measure Fate mapping and transplantation studies have led to competence, ectodermal caps were isolated from embryos at the idea that Hensen's node in the chick is functionally appropriate times after the start of gastrulation by removing equivalent to the dorsal lip of the blastopore (DLB) in ectoderm that was not yet contacted by involuting tissue. amphibia (see Hara, 1978). We therefore examined Hensen's node tissue was dissected from chick embryos whether Hensen's node could substitute for DLB tissue (White Leghorns from Spafas, CT, Truslow Farms, VA, and Mclntyre Poultry, CA) at stages 3-10 (Hamburger and in a Xenopus animal cap assay by combining Hensen's Hamilton, 1951) in ice cold L15 medium. The chick tissue was nodes, dissected from stage 3.5 and stage 4 chick placed between two pieces of animal cap tissue as shown in embryos, with pairs of ectodermal caps dissected from Fig. 1, and the resulting recombinants maintained on agarose- stage 9 Xenopus laevis embryos (Fig. 1). The recombi- coated dishes in 0.5 x MMR with penicillin and streptomycin nants were allowed to develop for 18-24 hours at room at room temperature (approximately 22°C). Recombinants temperature and then assayed for the expression of were harvested for RNA analysis after 20 hours or were tissue-specific RNA transcripts. maintained for 2.5 days with frequent changes of the culture medium for observation and histological analysis. The recombinants were examined for the presence of A highly purified preparation of porcine activin-A was neural tissue by measuring the expression of two kindly provided by Drs W. Vale and J. Vaughan in the Peptide neural-specific transcripts, NCAM and NF-3. NCAM is Biology Laboratory at the Salk Institute for Biological expressed in Xenopus ectoderm soon after neural Studies. induction and is restricted to neural tissue (Jacobson and Rutishauser, 1986; Kintner and Melton, 1987) RNA analysis providing an early general marker of neural differen- RNA was isolated from embryos or explants and assayed for tiation. NP-3 encodes a neuronal intermediate filament the expression of specific RNA transcripts using an RNAase protein (Charnas et al., 1987) that is expressed in protection assay described previously (Melton et al., 1984; neurons beginning about 4 hours after neural tube Kintner and Melton, 1987). The hybridization probes used to closure (Dixon and Kintner, 1989). All transcripts were detect NCAM, NF3, muscle-specific actin and EF-1 alpha detected with an RNAase protection assay in which the RNA are described elsewhere (Kintner and Melton, 1987; Dixon and Kintner, 1989). The hybridization probe for Xenopus tissue but not the chick tissue generated full- XlHbox6 RNA is a fragment of the XlHbox6 cDNA (Sharpe length protected fragments. et al., 1987) kindly provided by Drs C. Wright and E. Recombinants formed between Xenopus ectoderm DeRobertis. The hybridization probe for en-2 RNA is a and Hensen's node expressed both NCAM and NF-3 portion of the Xenopus engrailed-2 cDNA that was isolated transcripts (Fig. 2, lane 4). The levels of the two and provided for us by Drs R. Harland and A. Hemmati- transcripts expressed in the ectodermal caps after Brivanlou (Hemmati-Brivanlou et al., 1991). The amounts of induction by Hensen's node were approximately equiv- RNA in each sample were normalized by monitoring the alent to the levels observed in stage-matched control levels of EF-1 alpha RNA (Krieg et al., 1989).
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