Morphological polarity of intercalating deep mesodermal cells in the organzer of Xenopus laevis gastrulae

Author(s):  
Ray Keller ◽  
John Shih ◽  
Paul Wilson

The dorsal lip of the blastopore constitutes the “organizer” of the amphibian body plan, both in terms of its tissue interactions and its morphogenetic movements of convergence and extension during gastrulation. This tissue autonomously narrows (converges) and lengthens (extends) during early development, functioning prominently in the morphogenetic movements of both gastrulation and neurulation Xenopus laevis. High resolution time-lapse recording of cell behavior in cultured explants and cell labelling studies have shown that the movements of convergence and extension are produced by radial intercalation of cells, in which several layers rearrange to produce fewer layers of greater area, and by mediolateral intercalation of cells, in which several rows of cells rearrange to produce a narrower, longer array. By labelling individual cells with the fluorescent compound, DiI, and making low light level recordings, we found that cells of the notochord intercalate mediolaterally using polarized protrusive activity at their internal medial or lateral ends. Thus polarized protrusive activity appears to play a major role in mediolateral cell intercalation after the boundary between the notochord and somites forms in the late gastrula stage.We examine further the morphology of the deep mesodermal cells with scanning electron microscopy at earlier stages, to search for morphological manifestations of a similar polarity of protrusive activity. The dorsal deep mesodermal cells of early gastrulae were exposed by rapidly pulling the. epithelial endoderm off the deep cells with forceps, in Danilchik's solution, and fixing the embryo within 15 seconds in 2% glutaraldehyde in 0.1 M sodium cacodylate buffer (pH 7.4) as described previously. The dorsal deep cells adjacent to the epithelium are elongate and aligned parallel to one another and to the circumference of the glastopore (Fig. 1). The medial and lateral ends bear broad, lamelliform protrusions (large pointers, Fig. 1, 2) whereas the anterior and posterior ends bear numerous small filiform protrusions (small pointers, Fig. 1, 2). This characteristic morphology is found only in the dorsal marginal zone, which undergoes convergence and extension by mediolateral intercalation.

Development ◽  
1988 ◽  
Vol 103 (1) ◽  
pp. 193-209 ◽  
Author(s):  
R. Keller ◽  
M. Danilchik

We show with time-lapse micrography that narrowing in the circumblastoporal dimension (convergence) and lengthening in the animal-vegetal dimension (extension) of the involuting marginal zone (IMZ) and the noninvoluting marginal zone (NIMZ) are the major tissue movements driving blastopore closure and involution of the IMZ during gastrulation in the South African clawed frog, Xenopus laevis. Analysis of blastopore closure shows that the degree of convergence is uniform from dorsal to ventral sides, whereas the degree of extension is greater on the dorsal side of the gastrula. Explants of the gastrula show simultaneous convergence and extension in the dorsal IMZ and NIMZ. In both regions, convergence and extension are most pronounced at their common boundary, and decrease in both animal and vegetal directions. Convergent extension is autonomous to the IMZ and begins at stage 10.5, after the IMZ has involuted. In contrast, expression of convergent extension in the NIMZ appears to be dependent on basal contact with chordamesoderm or with itself. The degree of extension decreases progressively in lateral and ventral sectors. Isolated ventral sectors show convergence without a corresponding degree of extension, perhaps reflecting the transient convergence and thickening that occurs in this region of the intact embryo. We present a detailed mechanism of how these processes are integrated with others to produce gastrulation. The significance of the regional expression of convergence and extension in Xenopus is discussed and compared to gastrulation in other amphibians.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Robert J Tetley ◽  
Guy B Blanchard ◽  
Alexander G Fletcher ◽  
Richard J Adams ◽  
Bénédicte Sanson

Convergence and extension movements elongate tissues during development. Drosophila germ-band extension (GBE) is one example, which requires active cell rearrangements driven by Myosin II planar polarisation. Here, we develop novel computational methods to analyse the spatiotemporal dynamics of Myosin II during GBE, at the scale of the tissue. We show that initial Myosin II bipolar cell polarization gives way to unipolar enrichment at parasegmental boundaries and two further boundaries within each parasegment, concomitant with a doubling of cell number as the tissue elongates. These boundaries are the primary sites of cell intercalation, behaving as mechanical barriers and providing a mechanism for how cells remain ordered during GBE. Enrichment at parasegment boundaries during GBE is independent of Wingless signaling, suggesting pair-rule gene control. Our results are consistent with recent work showing that a combinatorial code of Toll-like receptors downstream of pair-rule genes contributes to Myosin II polarization via local cell-cell interactions. We propose an updated cell-cell interaction model for Myosin II polarization that we tested in a vertex-based simulation.


2017 ◽  
Author(s):  
Francesca Caroti ◽  
Everardo González Avalos ◽  
Viola Noeske ◽  
Paula González Avalos ◽  
Dimitri Kromm ◽  
...  

ABSTRACTExtraembryonic tissues contribute to animal development, which often entails spreading over embryo or yolk. Apart from changes in cell shape, the requirements for this tissue spreading are not well understood. Here we analyze spreading of the extraembryonic serosa in the scuttle fly Megaselia abdita. The serosa forms from a columnar blastoderm anlage, becomes a squamous epithelium, and eventually spreads over the embryo proper. We describe the dynamics of this process in long-term, whole-embryo time-lapse recordings, demonstrating that free serosa spreading is preceded by a prolonged pause in tissue expansion. Closer examination of this pause reveals mechanical coupling to the underlying yolk sac, which is later released. We find mechanical coupling prolonged and serosa spreading impaired after knockdown of M. abdita Matrix metalloprotease 1. We conclude that tissue-tissue interactions provide a critical functional element to constrain spreading epithelia.Impact StatementExtraembryonic tissue spreading in the scuttle fly Megaselia abdita requires mechanical decoupling from the underlying yolk sac.


Development ◽  
1992 ◽  
Vol 116 (Supplement) ◽  
pp. 81-91 ◽  
Author(s):  
Ray Keller ◽  
John Shih ◽  
Carmen Domingo

We discuss the cellular basis and tissue interactions regulating convergence and extension of the vertebrate body axis in early embryogenesls of Xenopus. Convergence and extension occur in the dorsal mesoderm (prospective notochord and somite) and in the posterior nervous system (prospective hindbrain and spinal cord) by sequential cell intercalations. Several layers of cells intercalate to form a thinner, longer array (radial intercalation) and then cells intercalate in the mediolateral orientation to form a longer, narrower array (mediolateral intercalation). Fluorescence microscopy of labeled mesodermal cells in explants shows that protrusive activity is rapid and randomly directed until the midgastrula stage, when it slows and is restricted to the medial and lateral ends of the cells. This bipolar protrusive activity results in elongation, alignment and mediolateral intercalation of the cells. Mediolateral intercalation behavior (MIB) is expressed in an anterior-posterior and lateral-medial progression in the mesoderm. MIB is first expressed laterally in both somitic and notochordal mesoderm. From its lateral origins in each tissue, MIB progresses medially. If convergence does not bring the lateral boundaries of the tissues closer to the medial cells in the notochordal and somitic territories, these cells do not express MIB. Expression of tissue-specific markers follows and parallels the expression of MIB. These facts argue that MIB and some aspects of tissue differentiation are induced by signals emanating from the lateral boundaries of the tissue territories and that convergence must bring medial cells and boundaries closer together for these signals to be effective. Grafts of dorsal marginal zone epithelium to the ventral sides of other embryos, to ventral explants and to UV-ventralized embryos show that it has a role in organising convergence and extension, and dorsal tissue differentiation among deep mesodermal cells. Grafts of involuting marginal zone to animal cap tissue of the early gastrula shows that convergence and extension of the hindbrain-spinal cord are induced by planar signals from the involuting marginal zone.


Development ◽  
2002 ◽  
Vol 129 (20) ◽  
pp. 4719-4728 ◽  
Author(s):  
Jonathan D. Gilthorpe ◽  
Elli-Kalliopi Papantoniou ◽  
Alain Chédotal ◽  
Andrew Lumsden ◽  
Richard J. T. Wingate

We have used cell labelling, co-culture and time-lapse confocal microscopy to investigate tangential neuronal migration from the rhombic lip. Cerebellar rhombic lip derivatives demonstrate a temporal organisation with respect to their morphology and response to migration cues. Early born cells, which migrate into ventral rhombomere 1, have a single long leading process that turns at the midline and becomes an axon. Later born granule cell precursors also migrate ventrally but halt at the lateral edge of the cerebellum, correlating with a loss of sensitivity to netrin 1 and expression of Robo2. The rhombic lip and ventral midline express Slit2 and both early and late migrants are repelled by sources of Slit2 in co-culture. These studies reveal an intimate relationship between birthdate, response to migration cues and neuronal fate in an identified population of migratory cells. The use of axons in navigating cell movement suggests that tangential migration is an elaboration of the normal process of axon extension. Movies available on-line


Development ◽  
1990 ◽  
Vol 108 (3) ◽  
pp. 461-470 ◽  
Author(s):  
A.K. Sater ◽  
A.G. Jacobson

We have examined the tissue interactions responsible for the expression of heart-forming potency during gastrulation. By comparing the specification of different regions of the marginal zone, we show that heart-forming potency is expressed only in explants containing both the dorsal lip of the blastopore and deep mesoderm between 30 degrees and 45 degrees lateral to the dorsal midline. Embryos from which both of these 30 degrees-45 degrees dorsolateral regions have been removed undergo heart formation in two thirds of cases, as long as the dorsal lip is left intact. If the dorsal lip is removed along with the 30 degrees-45 degrees regions, heart formation does not occur. These results indicate that the dorsolateral deep mesoderm must interact with the dorsal lip in order to express heart-forming potency. Transplantation of the dorsal lip into the ventral marginal zone of host embryos results in the formation of a secondary axis; in over half of cases, this secondary axis includes a heart derived from the host mesoderm. These findings suggest that the establishment of heart mesoderm is initiated by a dorsalizing signal from the dorsal lip of the blastopore.


Development ◽  
1993 ◽  
Vol 117 (1) ◽  
pp. 307-317 ◽  
Author(s):  
S.M. Purcell ◽  
R. Keller

Ceratophrys ornata, the Argentinean horned frog, has a significantly different pattern of early morphogenesis than does the most studied amphibian, Xenopus laevis. Time-lapse videomicroscopy, scanning electron microscopy, histological sections and lineage tracers have shown that, in C. ornata, some prospective notochord, somite and tailbud mesoderm cells leave the surface epithelium of the archenteron by ingression. After gastrulation, SEM reveals cells with constricted apices and a bottle shape in three zones on the archenteron roof and in a fourth zone around the blastopore. Prospective somitic tissue ingresses first from two lateral zones, followed by ingression of prospective notochord from the medial zone and tailbud mesoderm from the circumblastoporal zone. This is unlike X. laevis, in which no cells with constricted apices are present on the dorsal surface of the archenteron, nor do any cells ingress into the deep mesodermal layers from the surface layer.


Development ◽  
1976 ◽  
Vol 35 (1) ◽  
pp. 149-157
Author(s):  
C. C. Wylie ◽  
T. B. Roos

Previous studies have described the morphology, including the ultrastructure, of primordial germ cells (PGCs), and the cells with which they associate to form the gonadal ridge, in Xenopus laevis. In order to test their capacity for active movement we have studied single, isolated PGCs in vitro. Time-lapse studies of these cells reveal that they are motile, using broad cytoplasmic processes. The fact that these cells are very large and easy to manipulate in vitro makes them an attractive subject of study, particularly with respect to the mechanism of their movement and the surface phenomena which guide them to the site of the gonadal ridge.


Sign in / Sign up

Export Citation Format

Share Document