Dataset Information

Polarity Establishment and Maintenance in Ascidian Notochord.

ABSTRACT: Cell and tissue polarity due to the extracellular signaling and intracellular gene cascades, in turn, signals the directed cell behaviors and asymmetric tissue architectures that play a crucial role in organogenesis and embryogenesis. The notochord is a characteristic midline organ in chordate embryos that supports the body structure and produces positioning signaling. This review summarizes cellular and tissue-level polarities during notochord development in ascidians. At the early stage, planar cell polarity (PCP) is initialized, which drives cell convergence extension and migration to form a rod-like structure. Subsequently, the notochord undergoes a mesenchymal-epithelial transition, becoming an unusual epithelium in which cells have two opposing apical domains facing the extracellular lumen deposited between adjacent notochord cells controlled by apical-basal (AB) polarity. Cytoskeleton distribution is one of the main downstream events of cell polarity. Some cytoskeleton polarity patterns are a consequence of PCP: however, an additional polarized cytoskeleton, together with Rho signaling, might serve as a guide for correct AB polarity initiation in the notochord. In addition, the notochord's mechanical properties are associated with polarity establishment and transformation, which bridge signaling regulation and tissue mechanical properties that enable the coordinated organogenesis during embryo development.

SUBMITTER: Peng H

PROVIDER: S-EPMC7661463 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Polarity Establishment and Maintenance in Ascidian Notochord.

Peng Hongzhe H Qiao Runyu R Dong Bo B

Frontiers in cell and developmental biology 20201030

Cell and tissue polarity due to the extracellular signaling and intracellular gene cascades, in turn, signals the directed cell behaviors and asymmetric tissue architectures that play a crucial role in organogenesis and embryogenesis. The notochord is a characteristic midline organ in chordate embryos that supports the body structure and produces positioning signaling. This review summarizes cellular and tissue-level polarities during notochord development in ascidians. At the early stage, plana ...[more]

PMID: 33195278

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Project description:Background informationIn the embryos of various animals, the body elongates after gastrulation by morphogenetic movements involving convergent extension. The Wnt/PCP (planar cell polarity) pathway plays roles in this process, particularly mediolateral polarization and intercalation of the embryonic cells. In ascidians, several factors in this pathway, including Wnt5, have been identified and found to be involved in the intercalation process of notochord cells.ResultsIn the present study, the role of the Wnt5 genes, Hr-Wnt5alpha (Halocynthia roretzi Wnt5alpha) and Hr-Wnt5beta, in convergent extension was investigated in the ascidian H. roretzi by injecting antisense oligonucleotides and mRNAs into single precursor blastomeres of various tissues, including notochord, at the 64-cell stage. Hr-Wnt5alpha is expressed in developing notochord and was essential for notochord morphogenesis. Precise quantitative control of its expression level was crucial for proper cell intercalation. Overexpression of Wnt5 proteins in notochord and other tissues that surround the notochord indicated that Wnt5alpha plays a role within the notochord, and is unlikely to be the source of polarizing cues arising outside the notochord. Detailed mosaic analysis of the behaviour of individual notochord cells overexpressing Wnt5alpha indicated that a Wnt5alpha-manipulated cell does not affect the behaviour of neighbouring notochord cells, suggesting that Wnt5alpha works in a cell-autonomous manner. This is further supported by comparison of the results of Wnt5alpha and Dsh (Dishevelled) knockdown experiments. In addition, our results suggest that the Wnt/PCP pathway is also involved in mediolateral intercalation of cells of the ventral row of the nerve cord (floor plate) and the endodermal strand.ConclusionThe present study highlights the role of the Wnt5alpha signal in notochord convergent extension movements in ascidian embryos. Our results raise the novel possibility that Wnt5alpha functions in a cell-autonomous manner in activation of the Wnt/PCP pathway to polarize the protrusive activity that drives convergent extension.

Project description:BackgroundThe notochord is a defining feature of the chordate clade, and invertebrate chordates, such as tunicates, are uniquely suited for studies of this structure. Here we used a well-characterized set of 50 notochord genes known to be targets of the notochord-specific Brachyury transcription factor in one tunicate, Ciona intestinalis (Class Ascidiacea), to begin determining whether the same genetic toolkit is employed to build the notochord in another tunicate, Oikopleura dioica (Class Larvacea). We identified Oikopleura orthologs of the Ciona notochord genes, as well as lineage-specific duplicates for which we determined the phylogenetic relationships with related genes from other chordates, and we analyzed their expression patterns in Oikopleura embryos.ResultsOf the 50 Ciona notochord genes that were used as a reference, only 26 had clearly identifiable orthologs in Oikopleura. Two of these conserved genes appeared to have undergone Oikopleura- and/or tunicate-specific duplications, and one was present in three copies in Oikopleura, thus bringing the number of genes to test to 30. We were able to clone and test 28 of these genes. Thirteen of the 28 Oikopleura orthologs of Ciona notochord genes showed clear expression in all or in part of the Oikopleura notochord, seven were diffusely expressed throughout the tail, six were expressed in tissues other than the notochord, while two probes did not provide a detectable signal at any of the stages analyzed. One of the notochord genes identified, Oikopleura netrin, was found to be unevenly expressed in notochord cells, in a pattern reminiscent of that previously observed for one of the Oikopleura Hox genes.ConclusionsA surprisingly high number of Ciona notochord genes do not have apparent counterparts in Oikopleura, and only a fraction of the evolutionarily conserved genes show clear notochord expression. This suggests that Ciona and Oikopleura, despite the morphological similarities of their notochords, have developed rather divergent sets of notochord genes after their split from a common tunicate ancestor. This study demonstrates that comparisons between divergent tunicates can lead to insights into the basic complement of genes sufficient for notochord development, and elucidate the constraints that control its composition.

Dataset Information

Polarity Establishment and Maintenance in Ascidian Notochord.

Publications

Polarity Establishment and Maintenance in Ascidian Notochord.

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