Reversal of dorsoventral polarity in Xenopus laevis embryos by 180° rotation of the animal micromeres at the eight-cell stage

doi:10.1016/0012-1606(88)90304-1

Developmental Biology

Volume 128, Issue 2, August 1988, Pages 428-434

https://doi.org/10.1016/0012-1606(88)90304-1 Get rights and content

Abstract

The 180° rotation of the animal cell quartet at the 8-cell stage of Xenopus laevis embryos leads to a reversal of dorsoventral polarity in a majority of the embryos. Dorsal micromeres appear to instruct the macromeres in contact with them to initiate later steps in dorsal development. This inductive process is most apparent in the second half of the third cell cycle and is largely lost by the beginning of the fourth cell cycle.

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Cited by (21)

Pre-MBT patterning of early gene regulation in Xenopus: The role of the cortical rotation and mesoderm induction
1998, Mechanisms of Development
Patterning events that occur before the mid-blastula transition (MBT) and that organize the spatial pattern of gene expression in the animal hemisphere have been analyzed in Xenopus embryos. We present evidence that genes that play a role in dorsoventral specification display different modes of activation. Using early blastomere explants (16–128-cell stage) cultured until gastrula stages, we demonstrate by RT-PCR analysis that the expression of goosecoid (gsc), wnt-8 and brachyury (bra) is dependent on mesoderm induction. In contrast, nodal-related 3 (nr3) and siamois (sia) are expressed in a manner that is independent of mesoderm induction, however their spatially correct activation does require cortical rotation. The pattern of sia and nr3 expression reveals that the animal half of the 16-cell embryo is already distinctly polarized along the dorsoventral axis as a result of rearrangement of the egg structure during cortical rotation. Similar to the antagonistic activity between the ventral and the dorsal mesoderm, the ventral animal blastomeres can attenuate the expression of nr3 and sia in dorsal animal blastomeres. Our data suggest that no Nieuwkoop center activity at the blastula stage is required for the activation of nr3 and sia in vivo.
Neural Induction in Amphibians
1997, Current Topics in Developmental Biology
One of the most important processes during the early embryonic development is neural induction, resulting in the formation of the central nervous system. When a small area above the blastopore of an early amphibian gastrula is grafted to the prospective belly side of a host embryo, a complete secondary embryo is formed. This is true even after a renaissance of amphibian embryology, following the introduction of Xenopus luevis embryos as a favorite vertebrate model system, on one hand, and molecular techniques, on the other. In the past two years, insight into the processes of neural induction reached a new dimension. The action of neuralizing factors is discussed later in the chapter in the context of the new hypothesis of the neural default state of the ectoderm and the importance of the ventralizing factors. The disadvantage of Xenopus luevis and other amphibian species is that they could not be used for genetic studies because of their long generation times and their tetraploid genome. Therefore, the other model systems, Cuenorhabdifis, Drosophila, zebrafish, and mouse, were chosen. The molecular analysis of the processes leading to a large number of mutants in Drosophila and zebrafish has tremendously increased our knowledge about the early steps of embryogenesis.
A contact-dependent animal-to-vegetal signal biases neural lineages during Xenopus cleavage stages
1996, Developmental Biology
The central nervous system (CNS) of Xenopus is derived from three of four tiers of blastomeres of the 32-cell embryo, and each blastomere in these tiers produces a characteristic number of primary spinal neurons. The C-tier blastomeres constitute the boundary between those that contribute to the CNS (A-, B-, and C-tiers) and those that do not (D-tier). To test whether the neural lineages descended from the C-tier are established by intrinsic information or by cell–cell interactions, single B-tier blastomeres were deleted and the lineage of their C-tier neighbors mapped. The contributions of C-tier blastomeres to subdivisions of the CNS and to specific spinal neurons were significantly reduced. Contributions of these blastomeres to other tissues were mostly normal, indicating that those C-tier progeny that no longer contribute to CNS are distributed in small numbers throughout the rest of the clone. To test whether the changes in neural lineages after B-tier deletions were the result of the C-tier blastomere changing position, contacting new neighbors, or losing contact with inductive B-tier neighbors, intact embryos were transiently dissociated within their vitelline membranes at different time points prior to the midblastula transition. This treatment disrupted cell–cell contact, but not gap junction-mediated dye coupling or the positions of neighboring cells. C-tier CNS lineages were reduced as after deletion of the B-tier neighbor, suggesting that the neural fate of C-tier cells depends upon specific B-tier interactions. To determine whether these interactions occurred specifically between B-tier and C-tier neighbors, barriers were inserted transiently between individual B/C pairs; similar reductions in C-tier CNS lineages were observed. These data demonstrate that an animal-to-vegetal, contact-dependent signal passes from B-tier to C-tier blastomeres and is required for the normal C-tier contribution to the CNS. This cell–cell interaction occurs many hours before the onset of zygotic transcription or neural induction and may bias the field of cells that can respond to neural induction.
Determination of Xenopus cell lineage by maternal factors and cell interactions
1996, Current Topics in Developmental Biology
This chapter discusses the relative roles of maternally inherited components and epigenetic interactions in cell fate determination in Xenopus laevis embryos. In Xenopus, the determination of fate is a multistep process that begins with the polarization of the egg and the establishment of the embryonic dorsal-ventral axis is followed, by a number of signaling events, that regionalize the embryo, establish tissue types, and induce organ anlage, and finishes with late interactions that finalize cellular phenotype. Xenopus is an ideal vertebrate, in which to search for such molecules, because early embryos utilize stored maternal molecules and can be selected with nearly identical cleavage patterns, and thus any maternal localized determinants should be parcelled into separate identifiable lineages. It has become a very popular vertebrate model for the early developmental studies for a variety of reasons. Because the eggs are laid external to the female, they are accessible for manipulations throughout development. Xenopus embryos also pass from fertilization to tadpole stages very rapidly. It takes only about 30h of incubation, at room temperature, from fertilization to the first muscle twitches and hatching, from the vitelline membrane.
Three regions of the 32-cell embryo of Xenopus laevis essential for formation of a complete tadpole
1995, Developmental Biology
To examine the conditions of cell composition necessary for formation of a complete tadpole, defect embryos of 35 series were prepared by removing particular cells from 16- and 32-cell embryos of Xenopus laevis. These defect embryos were cultured and their development was examined. Formation of a complete tadpole did not require a special cell in the embryo, but did require cell combinations as follows: (1) A set of dorsal cells with a sufficient capacity to initiate axial structures. (2) Dorsal-most and ventral-most cells or dorsal-most and ventrolateral cells of the vegetal hemisphere. (3) The animal-most and vegetal-most tiers and either one of the upper-equatorial or the under-equatorial tiers. On the basis of these conditions, the minimal set of cells required for formation of a complete tadpole was determined. The minimal set included one dorsovegetal, two ventrovegetal, and eight animal cells in a lateral hemisphere of the 32-cell embryo. Forty percent of defect embryos with this minimal set developed into about quartersized but otherwise normal tadpoles. These tadpoles are the smallest complete tadpoles which have been experimentally obtained. The results of these experiments suggest that formation of a complete tadpole requires at the least cells in three different regions of the 32-cell embryo, that is, the animal, dorsovegetal, and ventrovegetal regions. The mechanism of pattern formation at the blastula stage is discussed, in consideration of the "three signal model" of mesoderm formation.
Spatial distribution of the capacity to initiate a secondary embryo in the 32-cell embryo ofXenopus laevis
1990, Developmental Biology
To examine the spatial distribution of dorsal determinants in the early embryos ofXenopus laevis, individual cells from the 32-cell embryo were transplanted into the same tier of the ventral side of a synchronous recipient. Their abilities to initiate a secondary embryo were measured by the incidence of secondary embryos and by the length of the secondary axis relative to the primary embryo. The ability was found to be localized in all cells (A1, B1, C1, and D1) of the dorsal most column and in the vegetal cells (C2 and D2) of the dorsolateral column. Transplanted C1 (subequatorial) cells caused the highest incidence of a secondary embryo and the average relative length of the secondary embryo was also greatest. Effectiveness decreased in the order: D1, B1, D2, C2, and A1. When these results were compared with Dale and Slack's fate map of the 32-cell embryo, it was concluded that the distribution of dorsal determinants is unique and does not coincide with the prospective regions for any tissues, though it is somewhat similar to the prospective region of dorsal endoderm or notochord. From these results it seems that dorsal determinants do not determine a particular tissue in an embryo but rather the “dorsal” region of an embryo.

View all citing articles on Scopus

^☆: This research was supported by the Italian Ministry of Education and by the Royal Netherlands Academy of Arts and Sciences.

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Full paperReversal of dorsoventral polarity in Xenopus laevis embryos by 180° rotation of the animal micromeres at the eight-cell stage☆

Abstract

Dev. Biol

Dev. Biol

Dev. Biol

Cell

Adv. Morphog

Dev. Biol

C. R. Soc. Biol. (Paris)

Recherches sur le déterminism de la symétrie bilatérale et dans l'oeuf de Amphibiens

Bull. Biol. France Belg

La rotation de symétrisation, facteur de la polarisation dorso-ventrale des ébauches primordiales, dans l'oeuf des Amphibiens

Arch. Anat. Microsc. Exp

The molecular basis of communication within the cell

Sci. Amer

The formation of the mesoderm in urodelean amphibians. V. First regional induction by the endoderm

Wilhelm Roux's Arch. Dev. Biol

Modification of the polarity following a 180° rotation of the four animal blastomeres at the 8-cell stage (Xenopus laevis D.)

Acta Embryol. Morphol. Exp

Communication in the eight-cell stage of Xenopus laevis development

A study using dye coupling

Devl. Biol

Une conception nouvelle des bases physiologiques de la morphogénès

Arch. Biol

Fate map for the 32-cell stage of Xenopus Laevis

Development

Mechanisms regulating pattern formation in the amphibian egg and early embryo

A reinvestigation of the role of the grey crescent in axis formation in Xenopus laevis

Nature (London)

The cleavage pattern of the axolotl egg studied by cinematography and cell counting

Wilhelm Roux's Arch. Dev. Biol

The ultrastructure of the dorsal yolk-free cytoplasm and the immediately surrounding cytoplasm in the symmetrized egg of Xenopus laevis

J. Embryol. Exp. Morphol

The development of animal cap cells in Xenopus: A measure of the start of animal cap competence to form mesoderm

Development

Full paper
Reversal of dorsoventral polarity in Xenopus laevis embryos by 180° rotation of the animal micromeres at the eight-cell stage☆