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David R Mcclay – 1st expert on this subject based on the ideXlab platform
Gastrulation in the sea urchin.Current Topics in Developmental Biology, 2019Co-Authors: David R Mcclay, Jacob Warner, Megan L. Martik, Esther Miranda, Leslie A. SlotaAbstract:
Abstract Gastrulation is arguably the most important evolutionary innovation in the animal kingdom. This process provides the basic embryonic architecture, an inner layer separated from an outer layer, from which all animal forms arise. An extraordinarily simple and elegant process of gastrulation is observed in the sea urchin embryo. The cells participating in sea urchin gastrulation are specified early during cleavage. One outcome of that specification is the expression of transcription factors that control each of the many subsequent morphogenetic changes. The first of these movements is an epithelial-mesenchymal transition (EMT) of skeletogenic mesenchyme cells, then EMT of pigment cell progenitors. Shortly thereafter, invagination of the Archenteron occurs. At the end of Archenteron extension, a second wave of EMT occurs to release immune cells into the blastocoel and primordial germ cells that will home to the coelomic pouches. The Archenteron then remodels to establish the three parts of the gut, and at the anterior end, the gut fuses with the stomodaeum to form the through-gut. As part of the anterior remodeling, mesodermal coelomic pouches bud off the lateral sides of the Archenteron tip. Multiple cell biological processes conduct each of these movements and in some cases the upstream transcription factors controlling this process have been identified. Remarkably, each event seamlessly occurs at the right time to orchestrate formation of the primitive body plan. This review covers progress toward understanding many of the molecular mechanisms underlying this sequence of morphogenetic events.
New insights from a high-resolution look at gastrulation in the sea urchin, Lytechinus variegatus.Mechanisms of Development, 2017Co-Authors: Megan L. Martik, David R McclayAbstract:
Abstract Background Gastrulation is a complex orchestration of movements by cells that are specified early in development. Until now, classical convergent extension was considered to be the main contributor to sea urchin Archenteron extension, and the relative contributions of cell divisions were unknown. Active migration of cells along the axis of extension was also not considered as a major factor in invagination. Results Cell transplantations plus live imaging were used to examine endoderm cell morphogenesis during gastrulation at high-resolution in the optically clear sea urchin embryo. The invagination sequence was imaged throughout gastrulation. One of the eight macromeres was replaced by a fluorescently labeled macromere at the 32 cell stage. At gastrulation those patches of fluorescent endoderm cell progeny initially about 4 cells wide, released a column of cells about 2 cells wide early in gastrulation and then often this column narrowed to one cell wide by the end of Archenteron lengthening. The primary movement of the column of cells was in the direction of elongation of the Archenteron with the narrowing (convergence) occurring as one of the two cells moved ahead of its neighbor. As the column narrowed, the labeled endoderm cells generally remained as a contiguous population of cells, rarely separated by intrusion of a lateral unlabeled cell. This longitudinal cell migration mechanism was assessed quantitatively and accounted for almost 90% of the elongation process. Much of the extension was the contribution of Veg2 endoderm with a minor contribution late in gastrulation by Veg1 endoderm cells. We also analyzed the contribution of cell divisions to elongation. Endoderm cells in Lytechinus variagatus were determined to go through approximately one cell doubling during gastrulation. That doubling occurs without a net increase in cell mass, but the question remained as to whether oriented divisions might contribute to Archenteron elongation. We learned that indeed there was a biased orientation of cell divisions along the plane of Archenteron elongation, but when the impact of that bias was analyzed quantitatively, it contributed a maximum 15% to the total elongation of the gut. Conclusions The major driver of Archenteron elongation in the sea urchin, Lytechinus variagatus, is directed movement of Veg2 endoderm cells as a narrowing column along the plane of elongation. The narrowing occurs as cells in the column converge as they migrate, so that the combination of migration and the angular convergence provide the major component of the lengthening. A minor contributor to elongation is oriented cell divisions that contribute to the lengthening but no more than about 15%.
Morphogenesis in sea urchin embryos: linking cellular events to gene regulatory network states.Wiley Interdisciplinary Reviews-Developmental Biology, 2011Co-Authors: Deirdre C. Lyons, Stacy L. Kaltenbach, David R McclayAbstract:
Gastrulation in the sea urchin begins with ingression of the primary mesenchyme cells (PMCs) at the vegetal pole of the embryo. After entering the blastocoel the PMCs migrate, form a syncitium, and synthesize the skeleton of the embryo. Several hours after the PMCs ingress the vegetal plate buckles to initiate invagination of the Archenteron. That morphogenetic process occurs in several steps. The non-skeletogenic cells produce the initial inbending of the vegetal plate. Endoderm cells then rearrange and extend the length of the gut across the blastocoel to a target near the animal pole. Finally, cells that will form part of the midgut and hindgut are added to complete gastrulation. Later, the stomodeum invaginates from the oral ectoderm and fuses with the foregut to complete the Archenteron. In advance of, and during these morphogenetic events an increasingly complex gene regulatory network controls the specification and the cell biological events that conduct the gastrulation movements.
Jeff Hardin – 2nd expert on this subject based on the ideXlab platform
cell rearrangement induced by filopodial tension accounts for the late phase of convergent extension in the sea urchin ArchenteronMolecular Biology of the Cell, 2019Co-Authors: Jeff Hardin, Michael WelikyAbstract:
: George Oster was a pioneer in using mechanical models to interrogate morphogenesis in animal embryos. Convergent extension is a particularly important morphogenetic process to which George Oster gave significant attention. Late elongation of the sea urchin Archenteron is a classic example of convergent extension in a monolayered tube, which has been proposed to be driven by extrinsic axial tension due to the activity of secondary mesenchyme cells. Using a vertex-based mechanical model, we show that key features of Archenteron elongation can be accounted for by passive cell rearrangement due to applied tension. The model mimics the cell elongation and the Poisson effect (necking) that occur in actual Archenterons. We also show that, as predicted by the model, ablation of secondary mesenchyme cells late in Archenteron elongation does not result in extensive elastic recoil. Moreover, blocking the addition of cells to the base of the Archenteron late in Archenteron elongation leads to excessive cell rearrangement consistent with tension-induced rearrangement of a smaller cohort of cells. Our mechanical simulation suggests that responsive rearrangement can account for key features of Archenteron elongation and provides a useful starting point for designing future experiments to examine the mechanical properties of the Archenteron.
a homologue of snail is expressed transiently in subsets of mesenchyme cells in the sea urchin embryo and is down regulated in axis deficient embryosDevelopmental Dynamics, 2006Co-Authors: Jeff Hardin, Charles A IllingworthAbstract:
Vertebrate members of the zinc finger transcription factor family related to Drosophila snail are expressed in neural crest and paraxial mesoderm along the left–right axis of the embryo. As simple deuterostomes, echinoderms are an important sister phylum for the chordates. We have identified populations of patterned, nonskeletogenic mesenchyme in the sea urchin Lytechinus variegatus by their expression of a sea urchin member of the snail family (Lv-snail). Lv-snail mRNA and protein are detectable at the midgastrula stage within the Archenteron. At the late gastrula stage, a contiguous cluster of cells on the left side of the tip of the Archenteron is Lv-snail–positive. At the early prism stage, two small clusters of mesenchyme cells near the presumptive arm buds are also Lv-snail–positive. At the pluteus stage, staining is detectable in isolated mesenchyme cells and the ciliated band. Based on fate mapping of secondary mesenchyme cells (SMCs) and double-label immunostaining, these patterns are consistent with expression of SNAIL by novel subsets of SMCs that are largely distinct from skeletogenic mesenchyme. In radialized embryos lacking normal bilateral symmetry, mesenchymal expression of Lv-SNAIL is abolished. These results suggest that transient expression of Lv-snail may be important for the differentiation of a subset of axially patterned nonskeletogenic mesenchyme cells and suggest conserved functions for snail family members in deuterostome development. Developmental Dynamics 235:3121–3131, 2006. © 2006 Wiley-Liss, Inc.
Archenteron precursor cells can organize secondary axial structures in the sea urchin embryoDevelopment, 1997Co-Authors: Helene A Benink, Gregory A Wray, Jeff HardinAbstract:
Local cell-cell signals play a crucial role in establishing major tissue territories in early embryos. The sea urchin embryo is a useful model system for studying these interactions in deuterostomes. Previous studies showed that ectopically implanted micromeres from the 16-cell embryo can induce ectopic guts and additional skeletal elements in sea urchin embryos. Using a chimeric embryo approach, we show that implanted Archenteron precursors differentiate autonomously to produce a correctly proportioned and patterned gut. In addition, the ectopically implanted presumptive Archenteron tissue induces ectopic skeletal patterning sites within the ectoderm. The ectopic skeletal elements are bilaterally symmetric, and flank the ectopic Archenteron, in some cases resulting in mirror-image, symmetric skeletal elements. Since the induced patterned ectoderm and supernumerary skeletal elements are derived from the host, the ectopic presumptive Archenteron tissue can act to ‘organize’ ectopic axial structures in the sea urchin embryo. SUMMARY
John B Morrill – 3rd expert on this subject based on the ideXlab platform
Characterization of Involution during Sea Urchin Gastrulation Using Two-Photon Excited Photorelease and Confocal Microscopy.Microscopy and Microanalysis, 1998Co-Authors: David W. Piston, Robert G Summers, Susan M. Knobel, John B MorrillAbstract:
Sea urchin embryos have served as a model system for the investigation of many concepts in developmental biology. Their gastrulation consists of two stages; primary invagination, where part of the epithelium invaginates into the blastocoel, and secondary invagination, where the Archenteron elongates to completely traverse the blastocoel. Primary invagination involves proliferation of cells within the vegetal plate during primary invagination, but until recently, it was assumed that the larval gastrointestinal (GI) tract developed without further involution of epithelial cells. To investigate rigorously the contribution of epithelial cell involution during Archenteron and GI tract development in the sea urchin, Lytechinus variegatus , we developed a new method for cell tracking based on two-photon excited photorelease of caged fluorophores. Single-cell embryos were injected with caged dye and two-photon excitation uncaging was employed to mark small groups of cells throughout gastrulation. Two-photon excitation allowed for noninvasive, three-dimensionally resolved uncaging inside living cells with minimal biological damage. Cellular involution into the Archenteron was observed throughout primary and secondary invagination, and the larval intestine was formed by further involution of cells following secondary invagination, which is inconsistent with the traditional model of sea urchin gastrulation. Further, as two-photon excitation microscopy becomes accessible to many researchers, the novel techniques described here will be broadly applicable to development of other invertebrate and vertebrate embryos.
cells are added to the Archenteron during and following secondary invagination in the sea urchin lytechinus variegatusDevelopmental Biology, 1998Co-Authors: Gabriel G Martins, Robert G Summers, John B MorrillAbstract:
In the present investigation, nuclei of endodermal cells, primary and secondary mesenchyme cells (PMCs and SMCs), and small micromere descendants (SMDs) of the sea urchin Lytechinus variegatus were counted and mapped at five developmental stages, ranging from primary invagination to pluteus larva. The Archenteron and its derivatives were measured three dimensionally with STERECON analytical software. For the first time SMC production is included in the kinetic analysis of Archenteron formation. While the Archenteron lumen doubled in length during secondary invagination, the number of Archenteron cells increased by at least 38% (over 50% when SMCs that emigrated from the tip of the Archenteron were included). The volume of the Archenteron epithelial wall plus the volume of 17 new SMCs increased by 40% over the equivalent volumes at the end of primary invagination. Because secondary invagination involves the addition of Archenteron cells and an increase in volume of the Archenteron epithelium, we conclude that secondary invagination is not accomplished simply by the rearrangement and reshaping of the primary Archenteron cells. Both Archenteron cell number and wall volume continued to increase at the same rates from the end of secondary invagination until the 27-h prism stage, although the lumen lengthened more slowly. SMCs were also produced at a constant rate from primary invagination until the prism stage. Because the production of both endodermal and mesodermal cells continues until the late prism stage, we conclude that gastrulation (defined as the establishment of the germ layers) also extends into the late prism stage.