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Neural induction is known to involve an interaction of ectoderm with dorsal mesoderm during gastrulation, but several kinds of studies have argued that competent ectoderm can also be neutralized via an interaction with previously neuralized tissue, a process termed homeogenetic neural induction. Although homeogenetic neural induction has been proposed to play an important role in the normal induction of neural tissue, this process has not been subjected to detailed study using tissue recombinants and molecular markers. We have examined the question of homeogenetic neural induction in Xenopus embryos, both in transplant and recombinant experiments, using the expression of two neural antigens to assay the response. When ectoderm that is competent to be neuralized is transplanted to the region adjacent to the neural plate of early neurula embryos, it forms neural tissue, as assayed by staining with antibodies against the neural cell adhesion molecule, N-CAM. Transplants to the ventral region, far from the neural plate, do not express N-CAM, indicating that neuralization is not occurring as a result of the transplantation procedure itself. Because this response might be occurring as a result of interactions of ectoderm with either adjacent neural plate tissue, or with underlying dorsolateral mesoderm, recombinant experiments were performed to determine the source of the neuralizing signal. Ectoderm cultured in combination with neural plate tissue alone expresses neural markers, while ectoderm cultured in combination with dorsolateral mesoderm does not. We conclude that neural tissue can homeogenetically induce competent ectoderm to form neural tissue and argue that this induction occurs via planar signaling within the ectoderm, a mechanism that, in normal development, may be involved in interactions within presumptive neural ectoderm or in specifying structures that lie near the neural plate.
FIG. 1. Transplant and recombinant experiments to assay for neural
induction. (a) Ectoderm was removed from FLDx-labeled early gastrula
(stage 10) embryos and transplanted into a neural plate stage
(stage 14) embryo from which the corresponding portion of ectoderm
had been removed. Transplants were made to the dorsolateral head
region (presumptive lens region), or to the anteriorventral region, as
shown. In addition, transplants were made to lateralheadectoderm,
corresponding to the region lying between the two areas shown in the
figure, and to posterior ventral regions (not shown). (b) Ectoderm was
removed from FLDx-labeled early gastrula (stage 10) embryos and
cultured either alone, in combination with anterior neural platetissue,
or in combination with mesoderm underlying the dorsolateral
head region. The diagram shows ectoderm from a stage 10embryo and
neural platetissue and head mesoderm from a neural plate stage embryo.
However, both late blastula (stage 9) and early gastrula (stage
10) embryos were used as ectoderm donors, and embryos from stages
12 (late gastrula stage) to 14 (neural plate stage) were used as the
source of neural plate. In all experiments, embryos or recombinants
were cultured to the equivalent of swimming tadpole stages (stages
39-42), fixed, sectioned, and stained by immunofluorescence with antibodies
that recognize either N-CAM or the neural antigen 2G9.
FIG. 2. Neural tissue induced from ectoderm transplants. Each row shows a case in which FLDx-labeled early gastrulaectoderm was
transplanted to a neural plate stage embryo (as shown in Fig. la). In each row, the left figure shows a section viewed under differential
interference contrast (DIC), the middle figure shows FLDx fluorescence, and the right figure shows immunofluorescence staining with anti-NCAM
antibody. Note that both the host neural tube and host eye stain strongly for N-CAM. Abbreviations: e - eye, nt = neural tube, p
= pharynx. Scale bar = 200 Um. A-C: Transplant to the dorsolateral head region. Transplanted tissue (labeled tissue in B, marked by arrow) has
fused to the host eye and stains with anti-N-CAM (arrow in C). D-F: Transplant to the lateralhead area. The transplant (labeled tissue in E,
marked by arrow) is located ventral to the level of the eye, but has still made a small neural-tube-like structure that stains positively for N-CAM
(arrow in F). G-I: Transplant to anteriorventralectoderm. The transplant (labeled tissue in H, marked by arrow) is located in the region of the
ventral midline, and has formed no neural tissue, as judged by the absence of N-CAM staining of this tissue (I).
FIG. 3. Neural tissue induced in recombinants. Each row shows a section of a recombinant (as shown in Fig. lb). In each row, the figure at left
shows a section viewed with DIC, the middle figure shows FLDx fluorescence, and the right figure shows immunofluorescence (C stained with
anti-N-CAM antibody; F, I stained with monoclonal antibody 2G9.) Abbreviations: e = eyetissue, n = neural tissue, m = mesoderm. Scale bars
= 200 um. A-C: Recombinant of FLDx-labeled early gastrula (stage 10) ectoderm with stage 14 anterior neural plate stained with anti-N-CAM
antibody. Note in (A) that the neural plate tissue has formed a ring of neural tissue that has the appearance of a neural tube (n; also compare A
and C) and an eye (e) as judged by the presence of pigmented retina. Test ectoderm (labeled tissue in B) has formed a small projection from the
neural tube (large arrow in B) that stains positively for N-CAM (arrow in C). (The small arrow at the bottom of B marks an area of weak FLDx
staining within the eyetissue; this is apparently due to small amounts of transfer of FLDx from the test ectoderm as described under Materials and
Methods.) D-F: Recombinant of FLDx-labeled late blastula (stage 9) ectoderm with stage 14 anterior neural plate stained with antibody
2G9. The neural-plate-derived tissue has formed a small neural mass in the interior of the recombinant (n; cf., panels A and C). Test ectoderm
(labeled tissue in E) has been assimilated into the neural tissue (arrow in E); within this composite neural structure, both neural-plate-derived
tissue and test ectoderm (arrow in F) stain positively with the 2G9 antibody. G-I: Recombinant of FLDx-labeled late blastula (stage 9) ectoderm
and stage 1312 dorsolateral headmesoderm (see Fig. lb). In many such ectoderm-mesoderm recombinants, we have observed that, despite the
presence of sufficient ectoderm to completely surround the mesoderm, the ectoderm does not do so, but the mesoderm (m) protrudes through the
ectodermal ball. Neither the test ectoderm (labeled tissue in H) nor the mesoderm stains with the 2G9 antibody.
