The dorsal involuting marginal zone stiffens anisotropically during its convergent extension in the gastrula of Xenopus laevis

Development ◽  
1995 ◽  
Vol 121 (10) ◽  
pp. 3131-3140 ◽  
Author(s):  
S.W. Moore ◽  
R.E. Keller ◽  
M.A. Koehl

Physically, the course of morphogenesis is determined by the distribution and timing of force production in the embryo and by the mechanical properties of the tissues on which these forces act. We have miniaturized a standard materials-testing procedure (the stress-relaxation test) to measure the viscoelastic properties of the dorsal involuting marginal zone, prechordal mesoderm, and vegetal endoderm of Xenopus laevis embryos during gastrulation. We focused on the involuting marginal zone, because it undergoes convergent extension (an important and wide-spread morphogenetic process) and drives involution, blastopore closure and elongation of the embryonic axis. We show that the involuting marginal zone stiffens during gastrulation, stiffening is a special property of this region rather than a general property of the whole embryo, stiffening is greater along the anteroposterior axis than the mediolateral axis and changes in the cytoskeleton or extracellular matrix are necessary for stiffening, although changes in cell-cell adhesions or cell-matrix adhesions are not ruled out. These findings provide a baseline of data on which future experiments can be designed and make specific, testable predictions about the roles of the cytoskeleton, extracellular matrix and intercellular adhesion in convergent extension, as well as predictions about the morphogenetic role of convergent extension in early development.

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.


2020 ◽  
Author(s):  
Anneke D. Kakebeen ◽  
Robert Huebner ◽  
Asako Shindo ◽  
Kujin Kwon ◽  
Taejoon Kwon ◽  
...  

AbstractExplanted tissues from vertebrate embryos reliably develop in culture and have provided essential paradigms for understanding embryogenesis, from early embryological investigations of induction, to the extensive study of Xenopus animal caps, to the current studies of mammalian gastruloids. Cultured explants of the Xenopus dorsal marginal zone (“Keller” explants) serve as a central paradigm for studies of convergent extension cell movements, yet we know little about the global patterns of gene expression in these explants. In an effort to more thoroughly develop this important model system, we provide here a time-resolved bulk transcriptome for developing Keller explants.


Development ◽  
1988 ◽  
Vol 102 (4) ◽  
pp. 677-686 ◽  
Author(s):  
C.M. Regen ◽  
R.A. Steinhardt

The discovery that lithium treatment at blastula stages can induce axis formation suggested that it might act by respecifying the cytoplasmic rearrangement-generated dorsoventral pattern, so that ventral cells behave like their dorsal counterparts. We have studied the effects of Li+ treatment on the spatial layout of the cell-group movements of gastrulation to see whether this is the case. We find that involution of the chordamesoderm and associated archenteron roof is retarded by Li+, an effect which does not suggest dorsal respecification. However, in both migration of the leading edge mesoderm and convergent extension of the marginal zone, ventral regions clearly do show dorsal-type movement. Because of this, and because of examples where disruption of involution and effects on axis differentiation do not correlate, we propose that failure of involution represents a distinct effect of Li+ involving disruption of mechanical relationships at the blastopore. Thus archenteron formation poorly reflects the dorsoventral pattern. Extension of sandwich explants of the ventral marginal zone is proposed as a reliable quantitative assay for alterations to the dorsoventral pattern.


2018 ◽  
Author(s):  
Glen D. Hirsh ◽  
Bette J. Dzamba ◽  
Pooja R. Sonavane ◽  
David R. Shook ◽  
Claire M. Allen ◽  
...  

AbstractShaping an embryo requires tissue-scale cell rearrangements known as morphogenetic events. These force-dependent processes require cells to adhere to their neighbors, through cadherin-catenin complexes, and to their extracellular matrix substrates, through integrin-based focal contacts. Integrin receptors are not only important for attachment to the extracellular matrix, but also for its fibrillar assembly. Fibrillogenesis requires actomyosin contractility, regulated in part by cadherin-catenin complexes. One such catenin, plakoglobin, mediates the attachment of actin stress fibers to cadherin cytoplasmic tails through its interactions with actin-binding proteins. In Xenopus gastrulae, plakoglobin has been identified as an essential member in the force-induced collective migration of the mesendoderm tissue. In the current study, we have further characterized the role of plakoglobin in two additional morphogenetic processes, epiboly and convergent extension. Plakoglobin-deficient tadpoles are 40% shorter and gastrulae contain notochords that are 60% wider than stage-matched controls, indicating convergent extension defects. The radially intercalating ectoderm of morphant animal caps is nearly twice as thick as controls. Furthermore, morphant embryos exhibit a failure to assemble a fibronectin matrix at the notochord-somite-boundary or along the blastocoel roof. The loss of the fibronectin matrix, while not due to changes in overall patterning, is a result of a failure to assemble the soluble dimers into long fibrils. The force of attachment to a cadherin or fibronectin substrate is reduced in plakoglobin morphants, indicating defects in adhesion to both cadherin and fibronectin. These data suggest that plakoglobin regulates morphogenesis and fibronectin assembly through cell-cell and cell-matrix adhesion.


2008 ◽  
Vol 182 (6) ◽  
pp. 1073-1082 ◽  
Author(s):  
Gun-Hwa Kim ◽  
Jung-Hyun Her ◽  
Jin-Kwan Han

The single-pass transmembrane protein Ryk (atypical receptor related tyrosine kinase) functions as a Wnt receptor. However, Ryk's correlation with Wnt/Frizzled (Fz) signaling is poorly understood. Here, we report that Ryk regulates Xenopus laevis convergent extension (CE) movements via the β-arrestin 2 (βarr2)-dependent endocytic process triggered by noncanonical Wnt signaling. During X. laevis gastrulation, βarr2-mediated endocytosis of Fz7 and dishevelled (Dvl/Dsh) actually occurs in the dorsal marginal zone tissues, which actively participate in noncanonical Wnt signaling. Noncanonical Wnt11/Fz7-mediated endocytosis of Dsh requires the cell-membrane protein Ryk. Ryk interacts with both Wnt11 and βarr2, cooperates with Fz7 to mediate Wnt11-stimulated endocytosis of Dsh, and signals the noncanonical Wnt pathway in CE movements. Conversely, depletion of Ryk and Wnt11 prevents Dsh endocytosis in dorsal marginal zone tissues. Our study suggests that Ryk functions as an essential regulator for noncanonical Wnt/Fz-mediated endocytosis in the regulation of X. laevis CE movements.


Development ◽  
1999 ◽  
Vol 126 (3) ◽  
pp. 423-434 ◽  
Author(s):  
M.C. Lane ◽  
W.C. Smith

The marginal zone in Xenopus laevis is proposed to be patterned with dorsal mesoderm situated near the upper blastoporal lip and ventral mesoderm near the lower blastoporal lip. We determined the origins of the ventralmost mesoderm, primitive blood, and show it arises from all vegetal blastomeres at the 32-cell stage, including blastomere C1, a progenitor of Spemann's organizer. This demonstrates that cells located at the upper blastoporal lip become ventral mesoderm, not solely dorsal mesoderm as previously believed. Reassessment of extant fate maps shows dorsal mesoderm and dorsal endoderm descend from the animal region of the marginal zone, whereas ventral mesoderm descends from the vegetal region of the marginal zone, and ventral endoderm descends from cells located vegetal of the bottle cells. Thus, the orientation of the dorsal-ventral axis of the mesoderm and endoderm is rotated 90(degrees) from its current portrayal in fate maps. This reassessment leads us to propose revisions in the nomenclature of the marginal zone and the orientation of the axes in pre-gastrula Xenopus embryos.


2002 ◽  
Vol 4 (1) ◽  
pp. 1-24 ◽  
Author(s):  
Josephine Clare Adams

The adhesion of cells to their surrounding extracellular matrix has vital roles in embryonic development, inflammatory responses, wound healing and adult tissue homeostasis. Cells attach to extracellular matrix by specific cell-surface receptors, of which the integrins and transmembrane proteoglycans are major representatives. The engagement of adhesion receptors triggers assembly of functional matrix contacts, in which bound matrix components, adhesion receptors and associated intracellular cytoskeletal and signalling molecules form large, localised multiprotein complexes. This review discusses the functional categories of matrix contacts, examples of the biological roles of matrix contacts in normal physiology, and examples of the ways in which abnormalities of matrix contacts are associated with major human diseases.


Development ◽  
1987 ◽  
Vol 100 (2) ◽  
pp. 279-295 ◽  
Author(s):  
L. Dale ◽  
J.M. Slack

We have further analysed the roles of mesoderm induction and dorsalization in the formation of a regionally specified mesoderm in early embryos of Xenopus laevis. First, we have examined the regional specificity of mesoderm induction by isolating single blastomeres from the vegetalmost tier of the 32-cell embryo and combining each with a lineage-labelled (FDA) animal blastomere tier. Whereas dorsovegetal (D1) blastomeres induce ‘dorsal-type’ mesoderm (notochord and muscle), laterovegetal and ventrovegetal blastomeres (D2–4) induce either ‘intermediate-type’ (muscle, mesothelium, mesenchyme and blood) or ‘ventral-type’ (mesothelium, mesenchyme and blood) mesoderm. No significant difference in inductive specificity between blastomeres D2, 3 and 4 could be detected. We also show that laterovegetal and ventrovegetal blastomeres from early cleavage stages can have a dorsal inductive potency partially activated by operative procedures, resulting in the induction of intermediate-type mesoderm. Second, we have determined the state of specification of ventral blastomeres by isolating and culturing them in vitro between the 4-cell stage and the early gastrula stage. The majority of isolates from the ventral half of the embryo gave extreme ventral types of differentiation at all stages tested. Although a minority of cases formed intermediate-type and dorsal-type mesoderms we believe these to result from either errors in our assessment of the prospective DV axis or from an enhancement, provoked by microsurgery, of some dorsal inductive specificity. The results of induction and isolation experiments suggest that only two states of specification exist in the mesoderm of the pregastrula embryo, a dorsal type and a ventral type. Finally we have made a comprehensive series of combinations between different regions of the marginal zone using FDA to distinguish the components. We show that, in combination with dorsal-type mesoderm, ventral-type mesoderm becomes dorsalized to the level of intermediate-type mesoderm. Dorsal-type mesoderm is not ventralized in these combinations. Dorsalizing activity is confined to a restricted sector of the dorsal marginal zone, it is wider than the prospective notochord and seems to be graded from a high point at the dorsal midline. The results of these experiments strengthen the case for the three-signal model proposed previously, i.e. dorsal and ventral mesoderm inductions followed by dorsalization, as the simplest explanation capable of accounting for regional specification within the mesoderm of early Xenopus embryos.


Sign in / Sign up

Export Citation Format

Share Document