High cell‐autonomy of the anterior endomesoderm viewed in blastomere fate shift during regulative development in the isolated right halves of four‐cell stage <i><scp>X</scp>enopus</i> embryos

Koga, Minoru; Nakashima, Takuro; Matsuo, Shintaro; Takeya, Ryu; Sumimoto, Hideki; Sakai, Masao; Kageura, H.

doi:10.1111/j.1440-169x.2012.01372.x

Cited by 4 publications

(2 citation statements)

References 46 publications

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“…Bilaterian animals require the early definition of two asymmetric, perpendicular axes for correct development. The process of axial differentiation in the embryo is controlled by two main mechanisms: the action of maternal determinants transmitted to specific blastomeres, and cellular interactions mediated by various signaling molecules ( Koga et al, 2012 ). Understanding the specific molecular determinants of these processes remains an important question in developmental biology.…”

Section: Introductionmentioning

confidence: 99%

Molecular asymmetry in the 8-cell stage Xenopus tropicalis embryo described by single blastomere transcript sequencing

Domenico

Owens

Grant

et al. 2015

Developmental Biology

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Correct development of the vertebrate body plan requires the early definition of two asymmetric, perpendicular axes. The first axis is established during oocyte maturation, and the second is established by symmetry breaking shortly after fertilization. The physical processes generating the second asymmetric, or dorsal–ventral, axis are well understood, but the specific molecular determinants, presumed to be maternal gene products, are poorly characterized. Whilst enrichment of maternal mRNAs at the animal and vegetal poles in both the oocyte and the early embryo has been studied, little is known about the distribution of maternal mRNAs along either the dorsal–ventral or left–right axes during the early cleavage stages. Here we report an unbiased analysis of the distribution of maternal mRNA on all axes of the Xenopus tropicalis 8-cell stage embryo, based on sequencing of single blastomeres whose positions within the embryo are known. Analysis of pooled data from complete sets of blastomeres from four embryos has identified 908 mRNAs enriched in either the animal or vegetal blastomeres, of which 793 are not previously reported as enriched. In contrast, we find no evidence for asymmetric distribution along either the dorsal–ventral or left–right axes. We confirm that animal pole enrichment is on average distinctly lower than vegetal pole enrichment, and that considerable variation is found between reported enrichment levels in different studies. We use publicly available data to show that there is a significant association between genes with human disease annotation and enrichment at the animal pole. Mutations in the human ortholog of the most animally enriched novel gene, Slc35d1, are causative for Schneckenbecken dysplasia, and we show that a similar phenotype is produced by depletion of the orthologous protein in Xenopus embryos.

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Section: Introductionmentioning

confidence: 99%

Molecular asymmetry in the 8-cell stage Xenopus tropicalis embryo described by single blastomere transcript sequencing

Domenico

Owens

Grant

et al. 2015

Developmental Biology

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“…A good fate map has been produced for Xenopus , 165 , 166 and subsequent experiments have revealed that only dorsal blastomeres, and more specifically the regions corresponding to the dorsal marginal zone, contribute to the GRP 167 , 168 . Further analyses indicate that only the cilia on the left side of the midline are required for flow at the GRP 169 ; thus, only injections targeted to the left dorsal blastomere should influence LR patterning via alterations in ciliary flow.…”

Section: Introductionmentioning

confidence: 99%

It’s never too early to get it Right

Vandenberg

Lemire

Levin

2013

Communicative & Integrative Biology

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For centuries, scientists and physicians have been captivated by the consistent left-right (LR) asymmetry of the heart, viscera, and brain. A recent study implicated tubulin proteins in establishing laterality in several experimental models, including asymmetric chemosensory receptor expression in C. elegans neurons, polarization of HL-60 human neutrophil-like cells in culture, and asymmetric organ placement in Xenopus. The same mutations that randomized asymmetry in these diverse systems also affect chirality in Arabidopsis, revealing a remarkable conservation of symmetry-breaking mechanisms among kingdoms. In Xenopus, tubulin mutants only affected LR patterning very early, suggesting that this axis is established shortly after fertilization. This addendum summarizes and extends the knowledge of the cytoskeleton’s role in the patterning of the LR axis. Results from many species suggest a conserved role for the cytoskeleton as the initiator of asymmetry, and indicate that symmetry is first broken during early embryogenesis by an intracellular process.

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Patterning and morphogenesis of the intricate but stereotyped oikoplastic epidermis of the appendicularian, Oikopleura dioica

Kishi

Hayashi

Onuma

et al. 2017

Developmental Biology

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Mechanisms for morphogenetic processes that generate complex patterns in a reproducible manner remain elusive. Live imaging provides a powerful tool to record cell behaviors. The appendicularian, Oikopleura dioica, is a planktonic tunicate that has a rapid developmental speed, small number of cells (less than 3500 cells in a juvenile), and a transparent body. The trunk epidermis, called the oikoplastic epithelium (OE), has elaborate cellular arrangements showing a complex pattern to secrete so-called "house" made of extracellular components. The OE is characterized by invariant number, size, and shape of the monolayer epithelial cells. Pattern formation is achieved during 5h of larval development without growth of the body, making this a suitable system for live imaging of a two-dimensional (2D) sheet. First, we subdivided the OE and defined several domains by cellular resolution, and systematically gave names to the constituent cells, since there is no variation among individuals. Time-lapse imaging of the epidermal cells revealed region-specific pattern formation processes. Each identified domain served as a compartment into which distribution of descendant cells of founder cells is restricted. Regulation of orientation, timing, and the number of rounds of cell divisions, but not cell death and migration, was a critical mechanism for determination of final cell arrangement and size. In addition, displacement of epithelial sheet plates was observed in the Eisen domain. Stem-cell-like cell divisions, whereby large mother stem cells generate a chain of small daughter cells, were involved in formation of the Nasse region and ventral sensory organ. These are the first examples of this kind of stem-cell-like cell division in deuterostomes. Furthermore, labeling of the left or right blastomere of the two-cell-stage embryo, which roughly gives rise to the left or right side of the body, respectively, revealed that the boundary of the descendant cells does not match with the midline of the trunk epidermis. Left and right descendants largely invade into the opposite side in an invariant way, suggesting the possibility that specification of the OE cell identities may occur later in development, most probably around hatching, and depending on cell position in the OE epithelial sheet. These detailed descriptions of OE patterning processes provide basic and essential information to analyze further cell behaviors in the generation of elaborate and intricate but stereotyped 2D cellular patterns in this advantageous model system for developmental and cell biological studies in chordates.

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High cell‐autonomy of the anterior endomesoderm viewed in blastomere fate shift during regulative development in the isolated right halves of four‐cell stage Xenopus embryos

Cited by 4 publications

References 46 publications

Molecular asymmetry in the 8-cell stage Xenopus tropicalis embryo described by single blastomere transcript sequencing

Molecular asymmetry in the 8-cell stage Xenopus tropicalis embryo described by single blastomere transcript sequencing

It’s never too early to get it Right

Patterning and morphogenesis of the intricate but stereotyped oikoplastic epidermis of the appendicularian, Oikopleura dioica

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