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The Rotated Hypoblast of the Chicken Embryo Does Not Initiate an Ectopic Axis in the Epiblast

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Proc. Natl. Acad. Sci. USA Vol. 92, pp. 10733-10737, November 1995 Developmental Biology The rotated hypoblast of the chicken embryo does not initiate an ectopic axis in the epiblast ODED KHANER Department of Cell and Animal Biology, The Hebrew University, Jerusalem, Israel 91904 Communicated by John Gerhart, University of California, Berkeley, CA, July 14, 1995 ABSTRACT In the amniotes, two unique layers of cells, of the hypoblast and that the orientation of the streak and axis the epiblast and the hypoblast, constitute the embryo at the can be predicted from the polarity of the stage XIII epiblast. blastula stage. All the tissues of the adult will derive from the Still it was thought that the polarity of the epiblast is sufficient epiblast, whereas hypoblast cells will form extraembryonic for axial development in experimental situations, although in yolk sac endoderm. During gastrulation, the endoderm and normal development the polarity of the hypoblast is dominant the mesoderm of the embryo arise from the primitive streak, (5, 6). These reports (1-3, 5, 6), taken together, would imply which is an epiblast structure through which cells enter the that cells of the hypoblast not only have the ability to change interior. Previous investigations by others have led to the the fate of competent cells in the epiblast to initiate an ectopic conclusion that the avian hypoblast, when rotated with regard axis, but also have the ability to repress the formation of the to the epiblast, has inductive properties that can change the original axis in committed cells of the epiblast. At the same fate of competent cells in the epiblast to form an ectopic time, the results showed that the epiblast is not wholly depen- embryonic axis. Thus, it has been suggested that the hypoblast dent on the organized hypoblast to establish an axis. normally induces the epiblast to form a primitive streak at a In the present work, an attempt was made to reexamine the specific locus. In the work reported here, an attempt was made experiments of Waddington and of Azar and Eyal-Giladi. to reexamine the issue of induction. In contrast to previous Experiments were designed to examine whether the polarity of reports, it was found that the rotated hypoblast of the chicken the hypoblast is actually superior to the polarity of the epiblast embryo does not initiate formation of an ectopic axis in the in determining the site where the embryonic axis will be epiblast. The embryonic axis always initiates and develops initiated. Moreover, an attempt was made to learn whether according to the basic polarity of the epiblast layer. These there is any influence of the size of the rotated hypoblast or of results provoke a reinterpretation of the issues of mesoderm the direction, left or right, of hypoblast rotation on the induction and primitive streak initiation in the avian embryo. development of the embryonic axis or whether the rotated hypoblast might more effectively initiate an ectopic axis in a Cell interactions during the early stages of avian development blastoderm from which the resident posterior marginal zone are crucial for the process of axis determination. Two unique had been removed (7). layers of cells, the epiblast and the hypoblast, constitute the embryo at the blastula stage of the chicken embryo. The MATERIALS AND METHODS interactions between these layers of cells during the stages of axis formation were studied by Waddington (1, 2), who sep- Chicken eggs (Leghorn x Leghorn) were incubated for the arated the hypoblast from the epiblast, rotated it through 900, acquire stage XIII (EG&K) blastoderms. The operation of the and then replaced it so that the anterior-posterior axes of the blastoderm was done with care according to published proce- two layers were at right angles to one another. As a result, the dures (8, 9). The prospective anterior-posterior polarity was primitive streak curved so that its anterior end pointed toward determined on the basis of Koller's sickle ridge, which marks the original anterior region of the hypoblast. Since these the posterior side of the blastoderm. experiments seemed to demonstrate an effect of the hypo- The hypoblast (in experimental series A and C) and/or the blast's orientation on the direction of elongation of the prim- blastoderm (in experimental series Bi, B2, and C) were itive streak, Waddington suggested that the hypoblast deter- dissected as a disc of one of three sizes: (i) Small disc: The mines the direction of tissue movements in the epiblast, by circular cut was made central to Koller's sickle and the mar- which the primitive streak is formed. ginal zone. (ii) Medium disc: The circular cut was made central Azar and Eyal-Giladi (3), making use of a new normal table to the marginal zone, on the edge of Koller's sickle. (iii) Large of chicken development (4), reexamined this issue in an effort disc: The circular cut was made within the marginal zone, near to define the interactions between the epiblast and the hypo- the posterior junction of the marginal zone and the area opaca. blast during the blastula stage [stage XIII, Eyal-Giladi and This disc contains Koller's sickle and marginal zone cells. Kochav (EG&K)]. The hypoblast at this stage was separated All the experiments reported here were done with blasto- from the epiblast and rotated 900. It was reported that the derms in which morphological features were clearly observ- subsequent primitive streak developed according to the pre- able, as defined in Fig. 1. In experimental series Bi, B2, and sumptive anterior-posterior polarity of the hypoblast. The C, dissected blastoderm regions peripheral to the discs were main interpretation from this research was that, at stage XIII, the experimental conditions of rotation produce a polarity Epiblast An-terior conflict between two gradient fields- one the inductiveness of and Hvpoblast \ the hypoblast and the other the competence of the epiblast- Marghinal zone and that the inductiveness of the hypoblast always dominates. Koller's sickle In subsequent research, it was found that the epiblast can Area Opaca develop a primitive streak and embryonic axis in the absence Posterior FIG. 1. Diagram of the main morphological characteristics of the The publication costs of this article were defrayed in part by page charge chicken blastula (stage XIII, EG&K). Blastoderm is shown in ventral payment. This article must therefore be hereby marked "advertisement" in view-that is, the hypoblast is toward the viewer and the epiblast is accordance with 18 U.S.C. §1734 solely to indicate this fact. away from the viewer. The yolk has been removed. 10733 Downloaded by guest on September 30, 2021 10734 Developmental Biology: Khaner Proc. Natl. Acad. Sci. USA 92 (1995) discarded while the remaining disc regions were incubated. Table 1. Rotation of the hypoblast 900 relative to the epiblast During the time of incubation, in a humid environment for does not alter orientation in which embryonic axis develops 36-48 hr at 37.5°C the embryos were observed, photographed, (series A and controls) and analyzed with reference to stages of the normal table of Deviation of axis chicken development (10). Operation N R-L 0° 5°-60° Bent Series A: Hypoblast RESULTS rotated From the reports of Waddington and Azar and Eyal-Giladi it Small 9 6-3 6 2 1 is unclear whether the whole hypoblast or only a circular Medium 14 6-8 10 3 1 subregion of it was dissected and rotated. Since previous work Large 28 12-16 18 8 2 (8) had shown that rotated blastoderm discs of different sizes Controls have different effects on the development of the primitive Unoperated 20 - 14 4 2 streak, it was considered important in the present analysis to Operated 10 - 8 1 1 examine the effects of rotated hypoblasts of several sizes. Hypoblast dissected Rotation of the Hypoblast Relative to an Epiblast That (large disc), replaced, Remains in Planar Contact with the Marginal Zone. In this not rotated type of experiment, only the hypoblast was dissected as a disc The hypoblast was rotated to the right or left (R-L). Deviation of the of small, medium, or large size. It was removed and rotated 900 embryonic axis from the orientation predicted from the anterior- in relation to the presumptive posterior side of the blastoderm, posterior polarity of the stage XIII epiblast is shown. Controls included to either the right or the left, and replaced on the epiblast (Fig. unoperated or operated but unrotated blastoderms. N, number of 2, series A). In 60-70% of the operated blastoderms, the blastoderms scored. Deviation of embryonic axis: 00, within 5° of that range displacements from the predicted orientation; axis developed in an orientation strictly in accord predicted; 5°-60°, embryonic bent, cases in which the primitive streak was bent 5°-60° from the with the presumptive anterior-posterior polarity of the epi- predicted orientation. blast. The rotated hypoblast did not influence the primitive streak to deflect toward the anterior end of the hypoblast, in orientation predicted from the presumptive anterior-posterior contrast to Waddington's report (1), or to reorient the prim- polarity of the epiblast, while in -10% the primitive streak itive streak 900 toward its own posterior side (3). The size of initially developed in a straight line oriented with the pre- the rotated disc did not make a significant difference in the sumptive epiblast axis, but later the embryonic axis came to results, nor was there an effect of rotating to the right or left bend 5°-60° from this polarity. However, in about one-half of (Table 1; Fig. 3A-E). In -25% of the cases, the embryonic axis these cases of the 25% and 10% groups, the embryonic axis developed in a straight line displaced 5°-60° from the axis developed from the side toward which the hypoblast was rotated, but in the other half the axis developed from the Series A: Rotation of the Hypoblast 900 opposite side-that is, the deviation was random with respect to the direction of hypoblast rotation.
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