A Nodal-independent and tissue-intrinsic mechanism controls heart-looping chirality

Noël, Emily S.; Verhoeven, Manon C.; Lagendijk, Anne Karine; Tessadori, Federico; Smith, K. A.; Choorapoikayil, Suma; Hertog, Jeroen den; Bakkers, Jeroen

doi:10.1038/ncomms3754

Cited by 105 publications

(171 citation statements)

References 51 publications

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“…However, this seems unnecessary as mutants with no jog retain their ability to loop [62,63,[68][69][70]. Indeed, the heart tube in the absence of Nodal signalling shows D-loop in about 70% of embryos and this is maintained even after the heart tube is cultured ex vivo [67]. Therefore, looping of the heart is controlled by a Nodal-independent mechanism that seems to rely on intrinsic mechanical properties dependent on the actin cytoskeleton [67].…”

Section: Coexistence Of Different Types Of Asymmetries: Epithalamus Amentioning

confidence: 99%

“…Indeed, the heart tube in the absence of Nodal signalling shows D-loop in about 70% of embryos and this is maintained even after the heart tube is cultured ex vivo [67]. Therefore, looping of the heart is controlled by a Nodal-independent mechanism that seems to rely on intrinsic mechanical properties dependent on the actin cytoskeleton [67]. Interestingly, this asymmetry is reminiscent of the bi-stable system driving asymmetric PpO migration although, in the case of the cardiac tube, the asymmetry is directional and not antisymmetric as observed in the PpO.…”

Section: Coexistence Of Different Types Of Asymmetries: Epithalamus Amentioning

confidence: 99%

“…For example, the sided migration of the PpO in zebrafish [40,50], the clockwise rotation of the neural tube in ascidians [12,39] and the conversion of left-right into dorsoventral seen in the projections from the Hb to the interpeduncular nucleus of zebrafish [45]. Symmetrical Nodal (absent and bilateral) result in the lack of jog (symmetry) [65][66][67], thus suggesting a role of Nodal as asymmetry inducer in this particular aspect of heart asymmetry. Notably, symmetry in both cases is produced through different ontogenic pathways.…”

Section: Coexistence Of Different Types Of Asymmetries: Epithalamus Amentioning

confidence: 99%

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Nodal signalling and asymmetry of the nervous system

Signore

Palma

Concha

2016

Phil. Trans. R. Soc. B

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One contribution of 17 to a theme issue 'Provocative questions in left -right asymmetry'. The role of Nodal signalling in nervous system asymmetry is still poorly understood. Here, we review and discuss how asymmetric Nodal signalling controls the ontogeny of nervous system asymmetry using a comparative developmental perspective. A detailed analysis of asymmetry in ascidians and fishes reveals a critical context-dependency of Nodal function and emphasizes that bilaterally paired and midline-unpaired structures/organs behave as different entities. We propose a conceptual framework to dissect the developmental function of Nodal as asymmetry inducer and laterality modulator in the nervous system, which can be used to study other types of body and visceral organ asymmetries. Using insights from developmental biology, we also present novel evolutionary hypotheses on how Nodal led the evolution of directional asymmetry in the brain, with a particular focus on the epithalamus. We intend this paper to provide a synthesis on how Nodal signalling controls left-right asymmetry of the nervous system. This article is part of the themed issue 'Provocative questions in leftright asymmetry'.

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Section: Coexistence Of Different Types Of Asymmetries: Epithalamus Amentioning

confidence: 99%

Section: Coexistence Of Different Types Of Asymmetries: Epithalamus Amentioning

confidence: 99%

Section: Coexistence Of Different Types Of Asymmetries: Epithalamus Amentioning

confidence: 99%

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Nodal signalling and asymmetry of the nervous system

Signore

Palma

Concha

2016

Phil. Trans. R. Soc. B

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“…This has led to the conclusion that regional cell shape changes generate L/R organizer asymmetry which is in turn required for asymmetric fluid flow [251]. Moreover, dextral looping of the zebrafish heart seems to arise from a tissue intrinsic process that depends on actomyosin activity, which is enhanced by Nodal signaling [249]. The disruption of actin or myosin II activity, even in presence of asymmetric Nodal signaling, causes defects in organ laterality [249,252].…”

Section: Chiral Symmetry Breaking In Vertebratesmentioning

confidence: 99%

“…Notwithstanding the controversy which of the two models is correct, there is also ample evidence that cell-or tissue-intrinsic mechanisms using the actin cytoskeleton contribute to L/R patterning either through affecting patterning of the node [198] or by promoting organ chirality independently of Nodal signaling [249]. Specifically, Gros et al have argued that mesodermal nodal cells in the chick embryo do not have cilia and that the short cilia on endodermal nodal cells are unrelated to mesodermal motile cilia in mammals.…”

Section: Chiral Symmetry Breaking In Vertebratesmentioning

confidence: 99%

Cytoskeletal Symmetry Breaking and Chirality: From Reconstituted Systems to Animal Development

Pohl

2015

Symmetry

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Animal development relies on repeated symmetry breaking, e.g., during axial specification, gastrulation, nervous system lateralization, lumen formation, or organ coiling. It is crucial that asymmetry increases during these processes, since this will generate higher morphological and functional specialization. On one hand, cue-dependent symmetry breaking is used during these processes which is the consequence of developmental signaling. On the other hand, cells isolated from developing animals also undergo symmetry breaking in the absence of signaling cues. These spontaneously arising asymmetries are not well understood. However, an ever growing body of evidence suggests that these asymmetries can originate from spontaneous symmetry breaking and self-organization of molecular assemblies into polarized entities on mesoscopic scales. Recent discoveries will be highlighted and it will be discussed how actomyosin and microtubule networks serve as common biomechanical systems with inherent abilities to drive spontaneous symmetry breaking.

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Early Committed Clockwise Cell Chirality Upregulates Adipogenic Differentiation of Mesenchymal Stem Cells

Bao

Chu

et al. 2020

Adv. Biosys.

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determine the LR asymmetry in morphogenesis. [2] For example, chirality has been found in Xenopus egg cortex before fertilization, [1] and can be passed down to more differentiated cells that establish LR body axis of animal body plan, [7] organ distribution, [8-10] and epithelial movement that leads to axial torsion and overall handedness of hindgut. [11,12] For specialized adult cells derived from somatic tissue, footprints of cell chirality can still be seen by their ability of generating cellular torque, [6,13] migration with LR bias, [14-16] or forming specific alignment in the multicellular level. [15,17,18] Through cell-cell communication, the chiral behavior causes LR-biased cell assembly of multicellular structure [15] and regulates permeability of intercellular junctions. [19] Clearly, cell chirality can be manifested in diverse forms and coordinate different morphogenic dynamics, resulting in distinct forms of tissue and organ architecture. Actin cytoskeleton plays an important role in cell chirality. When cultured on micropatterned substrate, the accumulation of actomyosin stress fibers at micropattern boundary is essential to activate the LR bias in cell migration and orientation. [15,17] Molecular studies suggest helical motion of actin filament as the underlying mechanism for the chirality at cellular level. [20,21] Functioning as a built-in machinery, actomyosin cytoskeleton allows chiral nucleus rotation of single cell [21] and generation of cellular torque with rotational bias. [13] Through a series of amplification process, the actin chirality ultimately determines the symmetry breaking in early embryonic development, [1,7,22] cardiac looping, [4,8,23] and organ laterality [9] in vivo. To give rise to such diverse forms of cell chirality, cell differentiation should play a role. [13,15,17] Cell differentiation is a process coupling with chemical [24] and physical factors. [25-27] Based on variation of key proteins in cytoskeleton, [28] cytoskeleton can be changed at early stage of cell differentiation, as shown by upregulation of cytoskeletal contractility [29] and cell morphological features, which can even forecast the cell lineage fate. [28] It suggests that cytoskeletal components, particularly actin, may early respond to the induction of cell differentiation and then actively participate the signal cascades to engage cell fate. Evidences can be found by regulation of cell differentiation via changed cell shape and cell spreading by physical cues [30-38]

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A Nodal-independent and tissue-intrinsic mechanism controls heart-looping chirality

Cited by 105 publications

References 51 publications

Nodal signalling and asymmetry of the nervous system

Nodal signalling and asymmetry of the nervous system

Cytoskeletal Symmetry Breaking and Chirality: From Reconstituted Systems to Animal Development

Early Committed Clockwise Cell Chirality Upregulates Adipogenic Differentiation of Mesenchymal Stem Cells

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