Early cellular interactions promote embryonic axis formation in Xenopus laevis

The correct distribution and activity of secreted signaling proteins called morphogens is required for many developmental processes. Nodal morphogens play critical roles in embryonic axis formation in many organisms. Models proposed to generate the Nodal gradient include diffusivity, ligand processing, and a temporal activation window. But how the Nodal morphogen gradient forms in vivo remains unclear. Here, we have measured in vivo for the first time, the binding affinity of Nodal ligands to their major cell surface receptor, Acvr2b, and to the Nodal inhibitor, Lefty, by fluorescence cross-correlation spectroscopy. We examined the diffusion coefficient of Nodal ligands and Lefty inhibitors in live zebrafish embryos by fluorescence correlation spectroscopy. We also investigated the contribution of ligand degradation to the Nodal gradient. We show that ligand clearance via degradation shapes the Nodal gradient and correlates with its signaling range. By computational simulations of gradient formation, we demonstrate that diffusivity, extra-cellular interactions, and selective ligand destruction collectively shape the Nodal morphogen gradient.

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A cytoplasmic determinant for dorsal axis formation in an early embryo of Xenopus laevis

Development ◽

10.1242/dev.110.4.1051 ◽

1990 ◽

Vol 110 (4) ◽

pp. 1051-1056 ◽

Cited By ~ 6

Author(s):

M. Yuge ◽

Y. Kobayakawa ◽

M. Fujisue ◽

K. Yamana

Keyword(s):

Xenopus Laevis ◽

Direct Evidence ◽

Early Embryo ◽

Dorsal Side ◽

Axis Formation ◽

Secondary Axis ◽

Dorsal Axis ◽

Cell Embryo ◽

Dorsal Cells ◽

Cytoplasmic Determinant

In Xenopus laevis, dorsal cells that arise at the future dorsal side of an early cleaving embryo have already acquired the ability to cause axis formation. Since the distribution of cytoplasmic components is markedly heterogeneous in an egg and embryo, it has been supposed that the dorsal cells are endowed with the activity to form axial structures by inheriting a unique cytoplasmic component or components localized in the dorsal region of an egg or embryo. However, there has been no direct evidence for this. To examine the activity of the cytoplasm of dorsal cells, we injected cytoplasm (dorsal cytoplasm) from dorsal vegetal cells of a Xenopus 16-cell embryo into ventral vegetal cells of a simultaneous recipient. The cytoplasm caused secondary axis formation in 42% of recipients. Histological examination revealed that well-developed secondary axes included notochord, as well as a neural tube and somites. However, injection of cytoplasm of ventral vegetal cells never caused secondary axis and most recipients became normal tailbud embryos. Furthermore, about two-thirds of ventral isolated halves injected with dorsal cytoplasm formed axial structures. These results show that dorsal, but not ventral, cytoplasm contains the component or components responsible for axis formation. This can be the first step towards identifying the molecular basis of dorsal axis formation.

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Switch-like behavior enables Wnt11 concentration specific response during dorso-ventral axis formation in Xenopus laevis

Journal of Theoretical Biology ◽

10.1016/j.jtbi.2017.06.027 ◽

2017 ◽

Vol 429 ◽

pp. 82-94 ◽

Cited By ~ 1

Author(s):

Jan Eric Sträng ◽

Rainer Schuler ◽

Michael Kühl ◽

Hans A. Kestler

Keyword(s):

Xenopus Laevis ◽

Axis Formation ◽

Specific Response

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Secondary embryonic axis formation by transplantation of D quadrant micromeres in an oligochaete annelid

Development ◽

10.1242/dev.055384 ◽

2010 ◽

Vol 138 (2) ◽

pp. 283-290 ◽

Cited By ~ 19

Author(s):

A. Nakamoto ◽

L. M. Nagy ◽

T. Shimizu

Keyword(s):

Embryonic Axis ◽

Axis Formation ◽

Oligochaete Annelid

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The correlation between patterns of dye transfer junctions and future developmental fate in Xenopus: u.v. irradiation and lithium treatment

Development ◽

10.1242/dev.105.4.747 ◽

1989 ◽

Vol 105 (4) ◽

pp. 747-752 ◽

Cited By ~ 1

Author(s):

D.J. Nagajski ◽

S.C. Guthrie ◽

C.C. Ford ◽

A.E. Warner

Keyword(s):

Lucifer Yellow ◽

Lithium Treatment ◽

Cell Communication ◽

Embryonic Axis ◽

Axis Formation ◽

Dye Transfer ◽

Cell Stage ◽

The Future ◽

Vegetal Pole ◽

Cell Embryo

The correlation between cell-to-cell communication junctions at the 32-cell stage and the subsequent embryonic axis has been examined in Xenopus laevis Disturbances of embryonic axis formation were u.v. irradiation at the vegetal pole before 0.6 in the which generates embryos with dorsal axial embryos were treated with 100mM-lithium chloride 32-cell stage, which generates embryos with ventral The cell-to-cell transfer of Lucifer Yellow was used junctional permeability. Injections were made into cells, lying in tiers 1 and 2 of the 32-cell embryo, relative to the future dorsoventral axis of the embryo on the basis of differences in pigmentation. The Yellow transfer in the future dorsal half of the compared with that in the future ventral half for u.v.-irradiated and Li-treated embryos. Injected subsequently scored for axial developmenf for transfer frequencies. In control embryos at the 32- Yellow transfer was both more frequent and more dorsal regions than in future ventral regions, as In embryos that had been u.v. irradiated before 0.6 in cycle, Lucifer transfer was the same in both light and the animal hemisphere and at the low level ventral regions in normal embryos. These embryos reductions in dorsal axial structures. Embryos the first cell cycle, when u.v. irradiation no longer cytoplasmic movements initiated at fertilization, dorsoventral difference in Lucifer Yellow transfer and normal dorsoventral polarity. Embryos exposed to

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Interactions between Wnt and Vg1 signalling pathways initiate primitive streak formation in the chick embryo

Development ◽

10.1242/dev.128.15.2915 ◽

2001 ◽

Vol 128 (15) ◽

pp. 2915-2927 ◽

Cited By ~ 6

Author(s):

Isaac Skromne ◽

Claudio D. Stern

Keyword(s):

Chick Embryo ◽

Marginal Zone ◽

Primitive Streak ◽

Embryonic Axis ◽

Normal Embryo ◽

Signalling Pathways ◽

Axis Formation ◽

Distinct Region ◽

Wnt Pathways ◽

Area Pellucida

The posterior marginal zone (PMZ) of the chick embryo has Nieuwkoop centre-like properties: when transplanted to another part of the marginal zone, it induces a complete embryonic axis, without making a cellular contribution to the induced structures. However, when the PMZ is removed, the embryo can initiate axis formation from another part of the remaining marginal zone. Chick Vg1 can mimic the axis-inducing ability of the PMZ, but only when misexpressed somewhere within the marginal zone. We have investigated the properties that define the marginal zone as a distinct region. We show that the competence of the marginal zone to initiate ectopic primitive streak formation in response to cVg1 is dependent on Wnt activity. First, within the Wnt family, only Wnt8C is expressed in the marginal zone, in a gradient decreasing from posterior to anterior. Second, misexpression of Wnt1 in the area pellucida enables this region to form a primitive streak in response to cVg1. Third, the Wnt antagonists Crescent and Dkk-1 block the primitive streak-inducing ability of cVg1 in the marginal zone. These findings suggest that Wnt activity defines the marginal zone and allows cVg1 to induce an axis. We also present data suggesting some additional complexity: first, the Vg1 and Wnt pathways appear to regulate the expression of downstream components of each other’s pathway; and second, misexpression of different Wnt antagonists suggests that different classes of Wnts may cooperate with each other to regulate axis formation in the normal embryo.

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