Distinct mechanisms determine organ left‐right asymmetry patterning in an uncoupled way

Huang, Sizhou; Xu, Wenming; Su, Bingyin; Luo, Lingfei

doi:10.1002/bies.201300128

Cited by 6 publications

(7 citation statements)

References 123 publications

(214 reference statements)

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“…In vertebrates, organ laterality is thought to be determined by the LR body axis established by Nodal cassette gene expressions, which is distinct from the mechanisms reported for Drosophila ( Huang et al, 2014 ; Yoshiba and Hamada, 2014 ). However, a recent study revealed that LR asymmetry formation in the zebrafish heart does not depend on nodal gene expression ( Noël et al, 2013 ).…”

Section: Discussionmentioning

confidence: 81%

“…The nodal flow breaks the LR symmetry and eventually induces left-side-specific gene expressions, including Nodal , Lefty , and Pitx-2 , the so-called nodal cassette genes ( Nonaka et al, 2002 ; Nonaka et al, 1998 ; Okada and Hirokawa, 1999 ). In addition to nodal flow, various other mechanisms are used in different vertebrates, but they also ultimately lead to the left-side-specific expressions of nodal cassette genes ( Levin, 2005 ), which influence the LR asymmetric morphology and positioning of internal organs ( Huang et al, 2014 ; Yoshiba and Hamada, 2014 ). However, it was recently reported that the LR asymmetric looping of the zebrafish heart develops by a tissue-intrinsic mechanism, independent of nodal ( Noël et al, 2013 ).…”

Section: Introductionmentioning

confidence: 99%

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Chiral cell sliding drives left-right asymmetric organ twisting

Inaki

Hatori

Nakazawa

et al. 2018

eLife

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Polarized epithelial morphogenesis is an essential process in animal development. While this process is mostly attributed to directional cell intercalation, it can also be induced by other mechanisms. Using live-imaging analysis and a three-dimensional vertex model, we identified ‘cell sliding,’ a novel mechanism driving epithelial morphogenesis, in which cells directionally change their position relative to their subjacent (posterior) neighbors by sliding in one direction. In Drosophila embryonic hindgut, an initial left-right (LR) asymmetry of the cell shape (cell chirality in three dimensions), which occurs intrinsically before tissue deformation, is converted through LR asymmetric cell sliding into a directional axial twisting of the epithelial tube. In a Drosophila inversion mutant showing inverted cell chirality and hindgut rotation, cell sliding occurs in the opposite direction to that in wild-type. Unlike directional cell intercalation, cell sliding does not require junctional remodeling. Cell sliding may also be involved in other cases of LR-polarized epithelial morphogenesis.

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Section: Discussionmentioning

confidence: 81%

Section: Introductionmentioning

confidence: 99%

Chiral cell sliding drives left-right asymmetric organ twisting

Inaki

Hatori

Nakazawa

et al. 2018

eLife

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“…In vertebrates, later LR morphogenesis (such as the position and morphology of internal organs) is influenced by an established body LR axis, which is achieved by Nodal signalling [55,56]. In addition, Nodal-independent LR-asymmetric organ morphogenesis was recently reported in a vertebrate.…”

Section: Discussionmentioning

confidence: 99%

Cell chirality: its origin and roles in left–right asymmetric development

Inaki

Liu

Matsuno

2016

Phil. Trans. R. Soc. B

154

147

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An item is chiral if it cannot be superimposed on its mirror image. Most biological molecules are chiral. The homochirality of amino acids ensures that proteins are chiral, which is essential for their functions. Chirality also occurs at the whole-cell level, which was first studied mostly in ciliates, single-celled protozoans. Ciliates show chirality in their cortical structures, which is not determined by genetics, but by ‘cortical inheritance’. These studies suggested that molecular chirality directs whole-cell chirality. Intriguingly, chirality in cellular structures and functions is also found in metazoans. In Drosophila, intrinsic cell chirality is observed in various left–right (LR) asymmetric tissues, and appears to be responsible for their LR asymmetric morphogenesis. In other invertebrates, such as snails and Caenorhabditis elegans, blastomere chirality is responsible for subsequent LR asymmetric development. Various cultured cells of vertebrates also show intrinsic chirality in their cellular behaviours and intracellular structural dynamics. Thus, cell chirality may be a general property of eukaryotic cells. In Drosophila, cell chirality drives the LR asymmetric development of individual organs, without establishing the LR axis of the whole embryo. Considering that organ-intrinsic LR asymmetry is also reported in vertebrates, this mechanism may contribute to LR asymmetric development across phyla.This article is part of the themed issue ‘Provocative questions in left–right asymmetry’.

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“…5). Our early studies also found this kind of phenotype 38, 51. Here, we wanted to know, in the embryos injected with aplnra MO, whether the liver LR patterning was also defective in the embryos with a reversed heart loop.…”

Section: Discussionmentioning

confidence: 94%

Aplnra/b Sequentially Regulate Organ Left-Right Patterning via Distinct Mechanisms

et al. 2019

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The G protein-coupled receptor APJ/Aplnr has been widely reported to be involved in heart and vascular development and disease, but whether it contributes to organ left-right patterning is largely unknown. Here, we show that in zebrafish, aplnra/b coordinates organ LR patterning in an apela/apln ligand-dependent manner using distinct mechanisms at different stages. During gastrulation and early somitogenesis, aplnra/b loss of function results in heart and liver LR asymmetry defects, accompanied by disturbed KV/cilia morphogenesis and disrupted left-sided Nodal/spaw expression in the LPM. In this process, only aplnra loss of function results in KV/cilia morphogenesis defect. In addition, only apela works as the early endogenous ligand to regulate KV morphogenesis, which then contributes to left-sided Nodal/spaw expression and subsequent organ LR patterning. The aplnra-apela cascade regulates KV morphogenesis by enhancing the expression of foxj1a , but not fgf8 or dnh9 , during KV development. At the late somite stage, both aplnra and aplnrb contribute to the expression of lft1 in the trunk midline but do not regulate KV formation, and this role is possibly mediated by both endogenous ligands, apela and apln . In conclusion, our study is the first to identify a role for aplnra/b and their endogenous ligands apela/apln in LR patterning, and it clarifies the distinct roles of aplnra-apela and aplnra/b-apela/apln in orchestrating organ LR patterning.

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Distinct mechanisms determine organ left‐right asymmetry patterning in an uncoupled way

Cited by 6 publications

References 123 publications

Chiral cell sliding drives left-right asymmetric organ twisting

Chiral cell sliding drives left-right asymmetric organ twisting

Cell chirality: its origin and roles in left–right asymmetric development

Aplnra/b Sequentially Regulate Organ Left-Right Patterning via Distinct Mechanisms

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