scholarly journals An early global role for Axin is required for correct patterning of the anterior-posterior axis in the sea urchin embryo

Development ◽  
2021 ◽  
pp. dev.191197
Author(s):  
Hongyan Sun ◽  
ChiehFu Jeff Peng ◽  
Lingyu Wang ◽  
Honglin Feng ◽  
Athula H. Wikramanayake
Keyword(s):  
Functional Analysis ◽  
Sea Urchin ◽  
Function Analysis ◽  
Cleavage Stage ◽  
Cell Fates ◽  
Sea Urchin Embryo ◽  
Early Embryos ◽  
Gsk 3Β ◽  
Intracellular Inhibition ◽  
Anterior Posterior

Activation of Wnt/β-catenin (cWnt) signaling at the future posterior end of early bilaterian embryos is a highly conserved mechanism for establishing the anterior-posterior (AP) axis. Moreover, inhibition of cWnt at the anterior end is required for development of anterior structures in many deuterostome taxa. This phenomenon, which occurs around the time of gastrulation, has been fairly well characterized but the significance of intracellular inhibition of cWnt signaling in cleavage-stage deuterostome embryos for normal AP patterning is less well understood. To investigate this process in an invertebrate deuterostome we defined Axin function in early sea urchin embryos. Axin is ubiquitously expressed at relatively high levels in early embryos and functional analysis revealed that Axin suppresses posterior cell fates in anterior blastomeres by blocking ectopic cWnt activation in these cells. Structure-function analysis of sea urchin Axin demonstrated that only its GSK-3β-binding domain is required for cWnt inhibition. These observations and results in other deuterostomes suggest that Axin plays a critical conserved role in embryonic AP patterning by preventing cWnt activation in multipotent early blastomeres, thus protecting them from assuming ectopic cell fates.

scholarly journals A dual role for Axin in establishing the anterior-posterior axis in the early sea urchin embryo

2020 ◽  
Author(s):  
Hongyan Sun ◽  
ChiehFu Jeff Peng ◽  
Lingyu Wang ◽  
Honglin Feng ◽  
Athula H. Wikramanayake
Keyword(s):  
Gene Expression ◽  
Sea Urchin ◽  
Glycogen Synthase ◽  
Negative Regulator ◽  
Cell Surface Receptor ◽  
Ligand Complex ◽  
Sea Urchin Embryo ◽  
Early Embryos ◽  
Gsk 3Β ◽  
Anterior Posterior

AbstractThe activation of Wnt/β-catenin (cWnt) signaling at the future posterior end of early embryos is a highly conserved mechanism for initiating pattern formation along the anterior-posterior (AP) axis in bilaterians. Moreover, in many bilaterian taxa, in addition, to activation of cWnt signaling at the posterior end, inhibition of cWnt signaling at the anterior end is required for normal development of anterior structures. In most cases, inhibition of cWnt signaling at the anterior end occurs around gastrulation and it is typically mediated by secreted factors that block signal transduction through the cWnt cell surface receptor-ligand complex. This phenomenon has been fairly well characterized, but the emerging role for intracellular inhibition of cWnt signaling in future anterior blastomeres—in cleavage stage embryos—to regulate correct AP patterning is less well understood. To investigate this process in an invertebrate deuterostome embryo we studied the function of Axin, a critical negative regulator of cWnt signaling, during early sea urchin embryogenesis. Sea urchin Axin is ubiquitously expressed in early embryos and by the blastula stage the expression of the gene becomes restricted to the posterior end of the embryo. Strikingly, knockdown of Axin protein levels using antisense Axin morpholinos (MO) led to ectopic nuclearization of β-catenin and activation of endomesoderm gene expression in anterior blastomeres in early embryos. These embryos developed a severely posteriorized phenotype that could be fully rescued by co-injection of Axin MO with wild-type Axin mRNA. Axin is known to negatively regulate cWnt by its role in mediating β-catenin stability within the destruction complex. Consistent with this function overexpression of Axin by mRNA injection led to the downregulation of nuclear β-catenin, inhibition of endomesoderm specification and a strong anteriorization of embryos. Axin has several well-defined domains that regulate its interaction with β-catenin and the key regulators of the destruction complex, Adenomatous Polyposis Coli (APC), Glycogen Synthase Kinase 3β(GSK-3β), and Dishevelled (Dvl). Using Axin constructs with single deletions of the binding sites for these proteins we showed that only the GSK-3βbinding site on Axin is required for its inhibition of cWnt in the sea urchin embryo. Strikingly, overexpression of the GSK-3β-binding domain alone led to embryos with elevated levels of endomesoderm gene expression and a strongly posteriorized phenotype. These results indicated that Axin has a critical global role in inhibiting cWnt signaling in the early sea urchin embryo, and moreover, that the interaction of Axin with GSK-3βis critical for this inhibition. These results also add to the growing body of evidence that Axin plays a global function in suppressing cWnt signaling in early embryos and indicates that modulation of Axin function may be a critical early step during patterning of the AP axis during bilaterian development

Cell interactions and mesodermal cell fates in the sea urchin embryo

Development ◽  
1992 ◽  
Vol 116 (Supplement) ◽  
pp. 43-51 ◽  
Author(s):  
Charles A. Ettensohn
Keyword(s):  
Sea Urchin ◽  
Cell Interactions ◽  
Cell Labeling ◽  
Cell Fates ◽  
Mesodermal Cell ◽  
Sea Urchin Embryo ◽  
Present Information ◽  
Cell Type Specific ◽  
Mesenchyme Cells

Cell interactions during gastrulation play a key role in the determination of mesodermal cell fates in the sea urchin embryo. An interaction between primary and secondary mesenchyme cells (PMCs and SMCs, respectively), the two principal populations of mesodermal cells, regulates the expression of SMC fates. PMCs are committed early in cleavage to express a skeletogenic phenotype. During gastrulation, they transmit a signal that suppresses the skeletogenic potential of a subpopulation of SMCs and directs these cells into an alternative developmental pathway. This review summarizes present information concerning the cellular basis of the PMC-SMC interaction, as analyzed by cell transplantation and ablation experiments, fluorescent cell labeling methods and the use of cell type-specific molecular markers. The nature and stability of SMC fate switching, the timing of the PMC-SMC interaction and its quantitative characteristics, and the lineage, numbers and normal fate of the population of skeletogenic SMCs are discussed. Evidence is presented indicating that PMCs and SMCs come into direct filopodial contact during the late gastrula stage, when the signal is transmitted. Finally, evolutionary questions raised by these studies are briefly addressed.

scholarly journals Abnormal morphogenesis of sea urchin embryo induced by UV partial irradiation given at cleavage stage.

1983 ◽  
Vol 24 (3) ◽  
pp. 197-202 ◽  
Author(s):  
YOSHIHIRO AKIMOTO ◽  
TSUGIO SHIROYA ◽  
NOBUO EGAMI
Keyword(s):  
Sea Urchin ◽  
Cleavage Stage ◽  
Sea Urchin Embryo

Archenteron precursor cells can organize secondary axial structures in the sea urchin embryo

Development ◽  
1997 ◽  
Vol 124 (18) ◽  
pp. 3461-3470 ◽  
Author(s):  
H. Benink ◽  
G. Wray ◽  
J. Hardin
Keyword(s):  
Sea Urchin ◽  
Crucial Role ◽  
Model System ◽  
Mirror Image ◽  
Precursor Cells ◽  
Skeletal Patterning ◽  
Sea Urchin Embryo ◽  
Early Embryos ◽  
Cell Embryo ◽  
Local Cell

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.

scholarly journals β-Catenin is essential for patterning the maternally specified animal-vegetal axis in the sea urchin embryo

1998 ◽  
Vol 95 (16) ◽  
pp. 9343-9348 ◽  
Author(s):  
Athula H. Wikramanayake ◽  
Ling Huang ◽  
William H. Klein
Keyword(s):  
Sea Urchin ◽  
Molecular Mechanisms ◽  
Early Embryo ◽  
Cell Fates ◽  
Cell Stage ◽  
Signal Transduction Cascade ◽  
Sea Urchin Embryos ◽  
Sea Urchin Embryo ◽  
Vegetal Pole ◽  
Vegetal Cell

In sea urchin embryos, the animal-vegetal axis is specified during oogenesis. After fertilization, this axis is patterned to produce five distinct territories by the 60-cell stage. Territorial specification is thought to occur by a signal transduction cascade that is initiated by the large micromeres located at the vegetal pole. The molecular mechanisms that mediate the specification events along the animal–vegetal axis in sea urchin embryos are largely unknown. Nuclear β-catenin is seen in vegetal cells of the early embryo, suggesting that this protein plays a role in specifying vegetal cell fates. Here, we test this hypothesis and show that β-catenin is necessary for vegetal plate specification and is also sufficient for endoderm formation. In addition, we show that β-catenin has pronounced effects on animal blastomeres and is critical for specification of aboral ectoderm and for ectoderm patterning, presumably via a noncell-autonomous mechanism. These results support a model in which a Wnt-like signal released by vegetal cells patterns the early embryo along the animal–vegetal axis. Our results also reveal similarities between the sea urchin animal–vegetal axis and the vertebrate dorsal–ventral axis, suggesting that these axes share a common evolutionary origin.

Manipulating cell fates in the sea urchin embryo

1997 ◽  
Vol 31 (1-3) ◽  
pp. 21-29 ◽  
Author(s):  
WILLIAM H. KLEIN ◽  
CHAI-AN MAO ◽  
LIN GAN ◽  
CHIN-KAI CHUANG ◽  
ATHULA H. WIKRAMANAYAKE
Keyword(s):  
Sea Urchin ◽  
Cell Fates ◽  
Sea Urchin Embryo

The allocation of early blastomeres to the ectoderm and endoderm is variable in the sea urchin embryo

Development ◽  
1997 ◽  
Vol 124 (11) ◽  
pp. 2213-2223 ◽  
Author(s):  
C.Y. Logan ◽  
D.R. McClay
Keyword(s):  
Sea Urchin ◽  
Low Frequency ◽  
Initial Step ◽  
Cell Types ◽  
Lytechinus Variegatus ◽  
Cell Fates ◽  
Cell Stage ◽  
Sea Urchin Embryo

During sea urchin development, a tier-to-tier progression of cell signaling events is thought to segregate the early blastomeres to five different cell lineages by the 60-cell stage (E. H. Davidson, 1989, Development 105, 421–445). For example, the sixth equatorial cleavage produces two tiers of sister cells called ‘veg1′ and ‘veg2,’ which were projected by early studies to be allocated to the ectoderm and endoderm, respectively. Recent in vitro studies have proposed that the segregation of veg1 and veg2 cells to distinct fates involves signaling between the veg1 and veg2 tiers (O. Khaner and F. Wilt, 1991, Development 112, 881–890). However, fate-mapping studies on 60-cell stage embryos have not been performed with modern lineage tracers, and cell interactions between veg1 and veg2 cells have not been shown in vivo. Therefore, as an initial step towards examining how archenteron precursors are specified, a clonal analysis of veg1 and veg2 cells was performed using the lipophilic dye, DiI(C16), in the sea urchin species, Lytechinus variegatus. Both veg1 and veg2 descendants form archenteron tissues, revealing that the ectoderm and endoderm are not segregated at the sixth cleavage. Also, this division does not demarcate cell type boundaries within the endoderm, because both veg1 and veg2 descendants make an overlapping range of endodermal cell types. The allocation of veg1 cells to ectoderm and endoderm during cleavage is variable, as revealed by both the failure of veg1 descendants labeled at the eighth equatorial division to segregate predictably to either tissue and the large differences in the numbers of veg1 descendants that contribute to the ectoderm. Furthermore, DiI-labeled mesomeres of 32-cell stage embryos also contribute to the endoderm at a low frequency. These results show that the prospective archenteron is produced by a larger population of cleavage-stage blastomeres than believed previously. The segregation of veg1 cells to the ectoderm and endoderm occurs relatively late during development and is unpredictable, indicating that later cell position is more important than the early cleavage pattern in determining ectodermal and archenteron cell fates.

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