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Regulative Capacity of the Archenteron During Gastrulation in the Sea Urchin

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Regulative Capacity of the Archenteron During Gastrulation in the Sea Urchin Development 122, 607-616 (1996) 607 Printed in Great Britain © The Company of Biologists Limited 1996 DEV3313 Regulative capacity of the archenteron during gastrulation in the sea urchin David R. McClay* and Catriona Y. Logan Developmental, Cellular and Molecular Biology Group, LSRC, Duke University, Durham NC 27708, USA *Author for correspondence (e-mail: [email protected]) SUMMARY Gastrulation in the sea urchin involves an extensive ognizable morphology of the archenteron was re-estab- rearrangement of cells of the archenteron giving rise to lished. Long after the archenteron reveals territorial speci- secondary mesenchyme at the archenteron tip followed by fication through expression of specific markers, the endo- the foregut, midgut and hindgut. To examine the regula- dermal cells remain capable of being respecified to other tive capacity of this structure, pieces of the archenteron gut regions. Thus, for much of gastrulation, the gut is con- were removed or transplanted at different stages of gas- ditionally specified. We propose that this regulative ability trulation. After removal of any or all parts of the archen- requires extensive and continuous short-range communi- teron, the remaining veg 1 and/or veg 2 tissue regulated to cation between cells of the archenteron in order to reor- replace the missing parts. Endoderm transplanted to ganize the tissues and position the boundaries of this ectopic positions also regulated to that new position in the structure even after experimental alterations. archenteron. This ability to replace or regulate endoderm did not decline until after full elongation of the archenteron was completed. When replacement occurred, the new gut Key words: morphogenesis, cell lineage, cell fate, differentiation, was smaller relative to the remaining embryo but the rec- specification. INTRODUCTION 1973; Ransick and Davidson, 1993, 1995) This suggests that specification of the archenteron begins with an early signal that Gastrulation in all organisms involves a highly regulated emanates from the vegetal pole. sequence of movements that places the three germ layers in Archenteron cells themselves arise from the macromere appropriate spatial contexts. In the sea urchin, formation of the lineage which at the sixth cleavage is subdivided into two archenteron is a multistep process that is accompanied by the layers, veg 1 and veg 2. The veg 2 layer lies immediately above eventual differentiation of many distinct cell types. Initially, the micromeres and was projected by Hörstadius, and in the precursors of the gut lie as a flat epithelial sheet that buckles lineage study of Cameron, to form the entire archenteron and then forms a short tube (Ettensohn, 1985b). This is (Cameron et al., 1987; Hörstadius, 1935). The veg 1 layer of followed by an extensive series of cell rearrangements as the cells (the upper layer of macromere progeny) was projected to archenteron elongates (Ettensohn, 1985a; Hardin, 1989; form ectoderm in the anal plate. We show elsewhere in Hardin and Cheng, 1986). Protrusive secondary mesenchyme marking studies that veg 1 contributes to the gut as well as to cells (SMCs) form at the archenteron tip during the midgas- the anal ectoderm in Lytechinus variegatus (McClay and trula stage and a subset of these migrate away to become Logan, unpublished data). The veg 2 layer invaginates early pigment and blastocoelar cells. Other SMCs remain associated during archenteron formation and cells of the veg 1 layer with the gut and form the circumesophageal muscle and invaginate later, leaving some remaining veg 1 cells to form coelomic sacs. After full elongation of the archenteron, con- vegetal plate ectoderm. In vitro studies have shown that veg 1 strictions subdivide the endoderm into foregut, midgut and and veg 2 cells differ in their ability to make endodermal cell hindgut, and this regionalization becomes evident not only types (Khaner and Wilt, 1990; Livingston and Wilt, 1990), morphologically but also by patterns of region-specific gene indicating that refinement of vegetal cell fates is progressive expression. and is accompanied by veg1 and veg2 becoming different from This study began with an interest in learning more about the each other. Later, once progenitors of vegetal cell types are specification and commitment of cells of the archenteron in the formed, gastrulation movements are followed by subsequent sea urchin embryo. Experiments have suggested that the regionalization and region-specific differentiation of the gut. micromeres that form at the fourth cleavage are not only suf- When cells in an embryo are rearranged with some unpre- ficient but necessary for the initial specification of endodermal dictability of cell position as occurs during archenteron mor- and mesodermal fate. Ectopic placement of micromeres can phogenesis, a problem exists for the embryo: how can it induce a secondary archenteron and removal of micromeres correctly specify and commit cells and put them in the proper can prevent the normal formation of gut tissues (Horstadius, locations. Fate mapping of the vegetal plate prior to invagina- 608 D. R. McClay and C. Y. Logan tion indicates that archenteron cells are arranged in a pattern embryo was stabbed to penetrate to the appropriate tissue. Tissue was that roughly matches their final position (Ruffins and aspirated slowly with the hydraulic syringe and tissues were cut using Ettensohn, 1995). Cell marking studies have shown that these the corner of the Scotch tape as the edge of the saw. After an operation same cells are rearranged to some extent during invagination the embryo was swept out of the chamber and transferred to a and archenteron elongation, so there is no absolute pre- microtiter plate well using a mouth pipet. Tissue transfers could also dictability of final location. (Hardin, 1989, 1990) The earlier be performed by carefully pulling tissue into the pipette and then transferring it into the appropriate donor position. For ‘intensive care’, experimental studies reveal an early conditional specification some embryos were temporarily held between two small oil droplets of endoderm, and expression of cell markers reveals that overt in the chamber for a few minutes while a cut surface healed over. For- specification can be demonstrated by the beginning of gastru- tunately for these operations, the sea urchin embryo has great lation (Wessel and McClay, 1985). Nevertheless, the experi- resilience to the insults of the operations performed. Most of the ments to be described here reveal an extensive and persistent embryos dissected recovered fully and could be handled within series of cell interactions throughout this active morphogenetic minutes of an operation. period. These lead us to conclude that, while endoderm prog- enitor cells are conditionally specified by early gastrulation, Markers and labels cells of the different regions of the archenteron retain an ability For experiments that involved donor and host combinations, donor to become any other part of the archenteron for an extended embryos were labeled by incubation of cultures in rhodamine isoth- iocyanate (Sigma #R 1755) for 30 minutes to 2 hours (Ettensohn and period of time that coincides with the active period of cell McClay, 1988). Analysis of embryos with regionally specific mono- rearrangement. It may well be that morphogenetic processes clonal antibodies were performed by standard immunofluorescent involving massive cell rearrangements have co-evolved with methods on whole-mount preparations (Ettensohn and McClay, mechanisms of information transfer between cells and with 1988). Briefly, embryos were fixed for 15-20 minutes in MeOH mechanisms that delay cell commitment events. (−20°C). Following several washes in sea water at room temperature, the embryos were incubated in monoclonal antibody for 2 hours to overnight. They were washed in sea water containing normal goat MATERIALS AND METHODS serum (1:30) and incubated in Cy3-goat antimouse IgG (Jackson Labs) (1:50), for 30 minutes to 2 hours. Alternatively, the embryos Animals and embryos were stained with FITC-labeled goat anti-mouse IgG (Jackson Labs). Embryos were photographed or frames were grabbed electronically Lytechinus variegatus was obtained from Beaufort, NC, or from Key for a videorecord of the operations and their consequences. Biscayne, Florida. Gametes were obtained by injection of 0.5 M KCl. Eggs were fertilized in artificial sea water and embryos were grown at temperatures ranging from 17° to 24°C. Growth at several different temperatures assured a staggered supply of embryos at a single stage RESULTS throughout the day of an operation. Lower temperatures had no adverse effects on development aside from slowing the overall rate. The vegetal plate is highly regulative After a surgical operation, embryos were grown in Millipore-filtered From lineage marking studies, most cells normally fated to sea water in the wells of 96-well plates, a single embryo per well. become secondary mesenchyme cells are within 15° of the Older embryos were fed with Duniella tertiolecta. vegetal pole, and progenitors of the foregut, midgut and Embryo manipulations hindgut are concentrically arranged progressively more distant Single embryos were transferred by mouth pipet to a Kiehart Chamber from the vegetal pole (Ruffins and Ettensohn, 1995) (Fig. 1). (Kiehart, 1982). Glass pipets were used to perform surgery on the However, such a fate map does not reveal the degree to which embryos. Thin-walled glass capillary tubes were pulled on a cells at this time are specified or committed to their respective Narashige glass pipette puller, then the tips were broken to achieve a normal fates. Our first set of experiments, therefore, was hollow blunt tip with an opening of 4-15 µm depending upon the par- designed to ask whether the fates of vegetal plate cells were ticular operation being performed. The capillary pipet was attached to fixed or whether these cells would regulate under experimen- a micromanipulator with a fine hydraulic control. The back of the tal perturbations. pipet was attached via intramedic tubing to a Gilmont glass syringe To investigate these questions, a blunt tipped glass needle (0.2 ml).
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