A mesoderm-independent role for Nodal signaling in convergence &amp; extension gastrulation movements

Williams, Margot; Solnica‐Krezel, Lilianna

doi:10.1101/671164

Cited by 5 publications

(5 citation statements)

References 78 publications

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“…Furthermore, blocking Nodal receptor activity with SB505124 inhibits pescoid elongation ( Figure 4B). This is in line with recent work showing that Nodal signalling is important to drive convergence extension movements within animal caps [23].…”

supporting

confidence: 93%

Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Trivedi

Fulton

Attardi

et al. 2019

Preprint

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A fundamental question in developmental biology is how the early embryo breaks initial symmetry to establish the spatial coordinate system later important for the organisation of the embryonic body plan. In zebrafish, this is thought to depend on the inheritance of maternal mRNAs [1][2][3], cortical rotation to generate a dorsal pole of beta-catenin activity [4][5][6][7][8] and the release of Nodal signals from the yolk syncytial layer (YSL) [9][10][11][12]. Recent work aggregating mouse embryonic stem cells has shown that symmetry breaking can occur in the absence of extra-embryonic tissue [19,20]. To test whether this is also true in zebrafish, we separated embryonic cells from the yolk and allowed them to develop as aggregates. These aggregates break symmetry autonomously to form elongated structures with an anterior-posterior pattern. Extensive cell mixing shows that any pre-existing asymmetry is lost prior to the breaking morphological symmetry, revealing that the maternal pre-pattern is not strictly required for early embryo patterning. Following early signalling events after isolation of embryonic cells reveals that a pole of Nodal activity precedes and is required for elongation. The blocking of PCP-dependent convergence and extension movements disrupts the establishment of opposing poles of BMP and Wnt/TCF activity and the patterning of anterior-posterior neural tissue. These results lead us to suggest that convergence and extension plays a causal role in the establishment of morphogen gradients and pattern formation during zebrafish gastrulation.Our current understanding of pattern formation during early development relies heavily on the notion of opposing signalling gradients that set-up rudimentary body plans [17]. These gradients establish cell fates in space that in turn lead to the population specific cell behaviours that dictate the complex cell and tissue rearrangement of gastrulation and axial elongation. In zebrafish, opposing Nodal and BMP signalling gradients are thought to be necessary and su cient for the establishment of the body plan as shown by experiments in which deployment of such gradients in animal caps leads to the formation of a complete AP axis [13]. In addition to controlling cell fate assignments, a recent study has demonstrated that Nodal signalling is a key driver of convergence and extension movements and is su cient to generate these behaviours when expressed within zebrafish animal caps [14]. Furthermore, BMP levels have been shown to be important for controlling cell movements during both gastrulation [21] and posterior body elongation [22]. These observations raise the possibility that opposing BMP and nodal signalling gradients are upstream of both morphogenesis and patterning. However, the causal relationships of these processes are di cult to dissociate in situations where continuous external signalling sources are present, either from overexpression experiments or from the extra-embryonic signals present during early development. To follow how cells can develop and p...

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supporting

confidence: 93%

Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Trivedi

Fulton

Attardi

et al. 2019

Preprint

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“…In zebrafish, opposing Nodal and BMP signaling gradients are thought to be necessary and sufficient for the establishment of the body plan as shown by experiments in which deployment of such gradients in animal caps leads to the formation of a complete anterior-posterior (AP) axis [ 14 ]. In addition to controlling cell fate assignments, a recent study has demonstrated that Nodal signaling is a key driver of convergence and extension movements and is sufficient to generate these behaviors when expressed within zebrafish animal caps [ 15 ]. Furthermore, BMP levels have been shown to be important for controlling cell movements during both gastrulation [ 16 ] and posterior body elongation [ 13 ].…”

Section: Resultsmentioning

confidence: 99%

“…When large regions from the animal pole were taken, the remaining blastomere explant was defined as a small vegetal piece. Comparison of sizes by diameter at 5hpc were made using the Fiji line drawing tool and compared to similar explants at 1hpc in [ 3 ] and 2 somite stage [ 15 ].…”

Section: Methodsmentioning

confidence: 99%

Axis Specification in Zebrafish Is Robust to Cell Mixing and Reveals a Regulation of Pattern Formation by Morphogenesis

et al. 2020

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Summary A fundamental question in developmental biology is how the early embryo establishes the spatial coordinate system that is later important for the organization of the embryonic body plan. Although we know a lot about the signaling and gene-regulatory networks required for this process, much less is understood about how these can operate to pattern tissues in the context of the extensive cell movements that drive gastrulation. In zebrafish, germ layer specification depends on the inheritance of maternal mRNAs [ 1 , 2 , 3 ], cortical rotation to generate a dorsal pole of β-catenin activity [ 4 , 5 , 6 , 7 , 8 ], and the release of Nodal signals from the yolk syncytial layer (YSL) [ 9 , 10 , 11 , 12 ]. To determine whether germ layer specification is robust to altered cell-to-cell positioning, we separated embryonic cells from the yolk and allowed them to develop as spherical aggregates. These aggregates break symmetry autonomously to form elongated structures with an anterior-posterior pattern. Both forced reaggregation and endogenous cell mixing reveals how robust early axis specification is to spatial disruption of maternal pre-patterning. During these movements, a pole of Nodal signaling emerges that is required for explant elongation via the planar cell polarity (PCP) pathway. Blocking of PCP-dependent elongation disrupts the shaping of opposing poles of BMP and Wnt/TCF activity and the anterior-posterior patterning of neural tissue. These results lead us to suggest that embryo elongation plays a causal role in timing the exposure of cells to changes in BMP and Wnt signal activity during zebrafish gastrulation. Video Abstract

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“…Likewise, given the recent interest in studies of explanted tissues from zebrafish (e.g. (Williams and Solnica-Krezel, 2019;Xu et al, 2014), DIF-FRAC could also be readily applied to that powerful animal model.…”

Section: Discussionmentioning

confidence: 99%

A systematic, label-free method for identifying RNA-associated proteinsin vivoprovides insights into vertebrate ciliary beating

Drew

Lee

Cox

et al. 2020

Preprint

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Cell-type specific RNA-associated proteins (RAPs) are essential for development and homeostasis in animals. Despite a massive recent effort to systematically identify RAPs, we currently have few comprehensive rosters of cell-type specific RAPs in vertebrate tissues. Here, we demonstrate the feasibility of determining the RNA-interacting proteome of a defined vertebrate embryonic tissue using DIF-FRAC, a systematic and universal (i.e., label-free) method. Application of DIF-FRAC to cultured tissue explants of Xenopus mucociliary epithelium identified dozens of known RAPs as expected, but also several novel RAPs, including proteins related to assembly of the mitotic spindle and regulation of ciliary beating. In particular, we show that the inner dynein arm tether Cfap44 is an RNA-associated protein that localizes not only to axonemes, but also to liquid-like organelles in the cytoplasm called DynAPs. This result led us to discover that DynAPs are generally enriched for RNA. Together, these data provide a useful resource for a deeper understanding of mucociliary epithelia and demonstrate that DIF-FRAC will be broadly applicable for systematic identification of RAPs from embryonic tissues. Introduction:

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A mesoderm-independent role for Nodal signaling in convergence & extension gastrulation movements

Cited by 5 publications

References 78 publications

Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Axis Specification in Zebrafish Is Robust to Cell Mixing and Reveals a Regulation of Pattern Formation by Morphogenesis

A systematic, label-free method for identifying RNA-associated proteinsin vivoprovides insights into vertebrate ciliary beating

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