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The Mechanism of Chick Blastoderm Expansion

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The Mechanism of Chick Blastoderm Expansion /. Embryol. exp. Morph. Vol. 35, 3, pp. 559-575, 1976 559 Printed in Great Britain The mechanism of chick blastoderm expansion By J. R. DOWNIE1 From the Department of Zoology, University of Glasgow SUMMARY At the time of laying, the domestic fowl blastoderm measures 4 mm across. After 4 days* incubation, the extra-embryonic yolk-sac tissues have expanded to encompass the whole yolk mass. This expansion involves the migration over the inner surface of the vitelline membrane of a specialized band of 'edge cells' at the blastoderm periphery. As they move, they pull out the blastoderm behind them, setting up a considerable tension. Expansion also involves cell proliferation and changes in cell shape. This paper attempts to show how locomotion, tension, proliferation and changes in cell shape all contribute to the orderly process of expansion. As a simplification, only the extra-embryonic epiblast is considered here. The findings are: 1. Expansion does not occur at a constant rate, but starts slowly, rises to a peak (over 500 /*m/h) at around 3 days, and then slows as coverage of the yolk mass nears completion. 2. During the first day of incubation, edge-cell migration produces a tension in the blastoderm. This rises to a peak at 20-24 h, then declines. This tension may be due to an imbalance between expansion by migration and expansion by proliferation. 3. Migration of edge cells can be affected by tension in the blastoderm, i.e. very high tension may hold them back. However, the tension level normally found in the blastoderm seems not to do so. The low rate of expansion in the first day is therefore not due to the high level of tension. It may instead be due to changes in edge-cell organization. 4. Proliferation occurs throughout the extra-embryonic epiblast during the expansion period. It is not restricted to the blastoderm periphery. After the yolk has been covered, the epiblast continues to grow, with proliferation restricted largely to a band just distal to the advancing edge of the area vasculosa. 5. Cell shape and arrangement change considerably during expansion. The epiblast of the unincubated embryo is a monolayer of tall cells. During expansion, these become con- siderably flattened so that each contributes a larger amount to yolk-sac surface area. INTRODUCTION One of the most impressive features of early avian development is blastoderm expansion. At laying, the domestic fowl blastoderm measures about 4 mm across. After 4 days' incubation, the extra-embryonic yolk-sac tissues have totally encompassed the yolk mass, a more than 200-fold increase in tissue area. The mechanism of blastoderm expansion has been investigated several times. Schlesinger (1952) believed that the periphery was a syncytium, throughout 1 Author's address: Developmental Biology Building, Department of Zoology, University of Glasgow, Glasgow G12 8QQ, Scotland U.K. 560 J. R. DOWNIE expansion, and that expansion was the result of the growth of this syncytium across the yolk surface, with individual cells being formed behind as the syncytium spread outwards. Rather similarly, Haas & Spratt (1968) envisaged a 'ring blastema' zone just within the blastoderm periphery, where cells proliferate very rapidly and move out centrifugally. However New (1959), without ignoring the importance of cell proliferation, emphasized the role of active cell migration. He noted that cells in a narrow band round the blastoderm margin attach to the overlying vitelline membrane and, using this membrane as a substrate for locomotion, move out centrifugally until the yolk mass is surrounded. The properties of these specialized blastoderm 'edge cells' have been the subject of several studies (Bellairs & New, 1962; Bellairs, 1963; Bellairs, Boyde & Heays- man, 1968; Downie & Pegrum, 1971; Downie, 1975). New (1959) also noted that the blastoderm during expansion is under a tension, presumably generated by the activity of the edge cells. He believed this tension essential for expansion, the main effect being to maintain the sheet-like arrangement of the cells, and to prevent their piling up. This paper investigates the changing pattern of locomotion, tension and proliferation in blastoderm expansion. The details of individual experiments are described with the results. Hens' eggs used were White Leghorn or De Kaalb. EDGE CELL LOCOMOTION AND SHEET TENSION IN THE EXPANDING BLASTODERM (1) Rate of expansion This was determined by measuring how far round the circumference of the yolk mass the blastoderm edge had travelled after different times. This was not an entirely simple matter since (1) there is considerable individual variation, but any attempt to follow the whole expansion process in a single specimen involves interference with the egg; and (2) it is difficult to make accurate measurements on the surface of a soft wet sphere. The results shown in Fig. 1 were obtained by taking samples from a single large batch of eggs at regular time intervals, remov- ing the yolks and assessing the expansion distance by comparison with known standards. These were drawings of the yolk mass as circles of 3 cm diameter (close to the usual yolk-mass diameter) with the expanding blastoderm drawn from above and from the side. Expansion was divided into 20 equal stages (in terms of sphere surface area). It was always possible to assign any actual embryos to one of these standards. Each standard is easily converted into blastoderm radius as a proportion of the circumference of a circle of diameter 3 cm. Each embryo is plotted in this way in Fig. 1. The broad pattern of results is consistent with those from more direct measuring methods, and shows several points of interest. (1) Expansion does not start immediately, but after about 10 h. This period is Mechanics of chick blastoderm expansion 561 PQ 20 30 40 50 60 70 80 90 Incubation time (h) Fig. 1. Blastoderm expansion rate in ovo, plotted as blastoderm radius after different incubation times. Each spot represents a different embryo. The line is drawn through the mean radius for each incubation time. much longer than the warming-up time of around 2 h. This pre-expansion period has been previously reported (Downie, 1974). (2) The rate of expansion is not constant. There is an initial slow phase to 16 h, when the rate is 200 /*m/h. From 24-84 h, the average rate is much faster (555 /tm/h) and this slows again over the final phase, to 96 h at 292 /^m/h. The exact time of completion of expansion is very variable, the last little patch of vitelline membrane often taking a long time to cover. (2) Blastoderm retraction No method was found of measuring directly the tension generated by the edge cells. The problem lies in holding the thin cell sheet without tearing it. Only occasionally, as in the work of James & Taylor (1969), has this problem been overcome in simple cell sheets. An indirect method was, however, success- ful in giving relative measurements. Attached blastoderms of known incubation time were set up as New (1955) cultures, using a glass ring of 25 mm internal diameter, staged (Hamburger & Hamilton, 1951) and an outline drawing made using a Wild drawing tube and microscope. The edge of each embryo was then detached from the vitelline membrane and, after allowing a few seconds for any retraction to occur, a new outline drawing was made. Since it is the centrifugal movement of the edge cells which stretches the blastoderm, a comparison of the stretched and retracted blastoderm size gives a relative measure of the tension exerted by the edge cells. A difficulty in relating retraction directly to tension exerted by the edge cells is that the tension required to stretch a cell varies with the mechanical properties 562 J. R. DOWNIE Up to 30 31-3-8 3-9-4-5 4-6-6-0 61-7-5 7-6-90 91 and over Initial blastoderm radius (mm) Fig. 2. Blastoderm retraction after loosening of the edge. Retraction is given as the percentage area reduction from the original (attached) area. Embryos are grouped according to their original radius. The number of embryos in each group is given in brackets. The histograms represent the mean retraction ± standard deviation for each radius group. of the cell. This may not alter much over the rather short incubation time covered by these measurements, but is at present an indeterminate factor. The results, involving measurements of 68 different embryos, are given in Fig. 2. Only embryos between 12 and 36 h incubation were used. Before 12 h, embryos are rarely reliably attached, and after 36 h, embryos are too large and too curved to be measured by this method. From Fig. 2, we see that newly attached blastoderms retract little; retraction rises to a peak when the blastoderm has a radius of around 6 mm (after 20-24 h incubation), then falls again to a low level when the blastoderm radius passes 9 mm (after about 36 h incubation). A blastoderm area retraction of 30 % - found when the radius is in the range 4-6-6-0 mm - implies that the cells are each occupying 30/70 x 100 = 43 % more than their resting area when the edge is attached. It is impossible to say what happens to tension later in development but, as the blastoderm becomes more curved, it is difficult to imagine how a tension generated at the edge could be transmitted throughout the cell sheet. (3) The relationship between locomotion and tension What might cause the changes in rate of movement of the edge cells during the expansion period? There are two general possibilities: (1) external con- straints, (2) changes in edge-cell organization. Mechanics of chick blastoderm expansion 563 oq Incubation time (h) Fig.
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