Tail Bud Progenitor Activity Relies on a Network Comprising Gdf11, Lin28, and Hox13 Genes

Aires, Rita; Lemos, Luisa de; Nóvoa, Ana; Jurberg, Arnon Dias; Mascrez, Bénédicte; Duboule, Denis; Mallo, Moisés

doi:10.1016/j.devcel.2018.12.004

Cited by 88 publications

(138 citation statements)

References 71 publications

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“…Our study suggests that Lin28a expression dynamics control the timing of somitogenesis termination, as the number of caudal vertebrae increased when Lin28a was induced by Dox administration at both E8.5 and E9.5 (Figure E). During the preparation of this manuscript, Aires et al and Robinton et al reported that the Lin28/ let‐7 pathway controls caudal body axis elongation, which is consistent with our observation. Robinton et al showed that Lin28a overexpression in neuromesodermal lineages increases the duration, but not the rate, of somitogenesis.…”

Section: Discussionsupporting

confidence: 91%

Temporal regulation of Lin28a during mammalian neurulation contributes to neonatal body size control

Miyazawa

Muramatsu

Makino

et al. 2019

Developmental Dynamics

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Background The timing of developmental events is tightly regulated along a time axis for normal development. Although the RNA‐binding protein Lin28a plays a crucial role in the regulation of developmental timing in Caenorhabditis elegans, how the timing of Lin28a expression affects the rate and/or duration of developmental events during mammalian development remains to be addressed. Results In this study, we discovered that the timing and the duration of Lin28a expression affect embryonic growth. During the neurulation stage of mouse development, endogenous Lin28a levels start to drop. When Lin28a expression was maintained transiently using the inducible tetracycline‐regulated gene expression (Tet‐ON) system [doxycycline (Dox)‐inducible Lin28a transgenic (iLin28a Tg) mice] with Dox administration at E8.5 and E9.5, it resulted in neonatal lethality, increased body weight (organomegaly), and an increased number of caudal vertebrae at birth. On the other hand, Lin28a induction only at E8.5 caused neonatal lethality and organomegaly, but did not affect the caudal vertebra number. Of note, although Dox treatment before or after neurulation still caused neonatal lethality, it neither caused organomegaly nor the increased caudal vertebra number in iLin28a Tg neonates. Conclusions Temporal regulation of Lin28a expression during neurulation affects developmental events such as cessation of axial elongation and embryonic growth in mice.

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Section: Discussionsupporting

confidence: 91%

Temporal regulation of Lin28a during mammalian neurulation contributes to neonatal body size control

Miyazawa

Muramatsu

Makino

et al. 2019

Developmental Dynamics

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“…Importantly, however, only by explicitly including termination of elongation and patterning in these models will the true evolutionary diversity in vertebral formulas be accounted for . This would further entail the control to balance segmentation speed and progenitor pool size, as well as incorporating the temporal and spatial effects of an axial Hox code on progenitor proliferation and somite identity . Intriguingly, either modulations in the speed of the segmentation clock or, alternatively, changing the duration of progenitor pool persistence have been shown to alter the eventual number of segments in the vertebral column of different species …”

Section: Positional Information Directional Growth and The Periodicmentioning

confidence: 99%

“…[115][116][117][118] Intriguingly, either modulations in the speed of the segmentation clock or, alternatively, changing the duration of progenitor pool persistence have been shown to alter the eventual number of segments in the vertebral column of different species. 114,115…”

Section: Vertebrate Primary Body Axis Segmentation: Repetitive Pattmentioning

confidence: 99%

A sense of place, many times over ‐ pattern formation and evolution of repetitive morphological structures

Grall

Tschopp

2019

Developmental Dynamics

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Fifty years ago, Lewis Wolpert introduced the concept of “positional information” to explain how patterns form in a multicellular embryonic field. Using morphogen gradients, whose continuous distributions of positional values are discretized via thresholds into distinct cellular states, he provided, at the theoretical level, an elegant solution to the “French Flag problem.” In the intervening years, many experimental studies have lent support to Wolpert's ideas. However, the embryonic patterning of highly repetitive morphological structures, as often occurring in nature, can reveal limitations in the strict implementation of his initial theory, given the number of distinct threshold values that would have to be specified. Here, we review how positional information is complemented to circumvent these inadequacies, to accommodate tissue growth and pattern periodicity. In particular, we focus on functional anatomical assemblies composed of such structures, like the vertebrate spine or tetrapod digits, where the resulting segmented architecture is intrinsically linked to periodic pattern formation and unidirectional growth. These systems integrate positional information and growth with additional patterning cues that, we suggest, increase robustness and evolvability. We discuss different experimental and theoretical models to study such patterning systems, and how the underlying processes are modulated over evolutionary timescales to enable morphological diversification.

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“…Interestingly, it should be also noted that tb-EMT functional and molecular 5 characteristics are more akin to those described for the transitions involved in 6 metastatic processes than to the typical developmental EMTs (e.g. gastrulation) 7 The TgfbRI stop/+ line was generated by CRISPR/Cas9, inserting the 28 DNA obtained from yolk sacs or tail biopsies from embryos or mice, respectively, as 6 previously described (Aires et al, 2019). The primers used for genotyping are 7 specified in table 1.…”

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confidence: 99%

“…Experiments involving animals carried out in the Oeiras laboratory the majority underlying paraxial mesoderm, the different tissue pieces were pooled 25 and after 5 min at 37ºC in 0.05% trypsin/EDTA, they were placed in neutralization 26 In Situ Hybridization and sectioning. Whole-mount in situ hybridization was 1 performed as previously described (Aires et al, 2019). Post-stained embryos were 2 included in a mixture of 0.45% gelatin (Merck), 27% bovine serum albumin (Roche), 3 18% sucrose (Sigma) in PBS that was then jellified with 1.75% glutaraldehyde 4 (Biochem chemopharma) and sectioned at 20 µm with a vibratome (Leica).…”

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confidence: 99%

A TgfβRI/Snai1-dependent developmental module at the core of vertebrate axial elongation

Dias

Lozovska

Wymeersch

et al. 2020

Preprint

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Formation of the vertebrate postcranial body axis follows two sequential but distinct phases. The first phase generates pre-sacral structures (the so-called primary body) through the activity of the primitive streak (PS) on axial progenitors within the epiblast. The embryo then switches to generate the secondary body (post-sacral structures), which depends on axial progenitors in the tail bud. Here we show that the mammalian tail bud is generated through an independent developmental module, concurrent but functionally different to that generating the primary body. This module is triggered by convergent TgfβRI and Snai1 activities that promote an incomplete epithelial to mesenchymal transition (EMT) on a subset of epiblast axial progenitors. This EMT is functionally different to that coordinated by the PS, as it does not lead to mesodermal differentiation but brings axial progenitors into a transitory state, keeping their progenitor activity to drive further axial body extension.

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Tail Bud Progenitor Activity Relies on a Network Comprising Gdf11, Lin28, and Hox13 Genes

Cited by 88 publications

References 71 publications

Temporal regulation of Lin28a during mammalian neurulation contributes to neonatal body size control

Temporal regulation of Lin28a during mammalian neurulation contributes to neonatal body size control

A sense of place, many times over ‐ pattern formation and evolution of repetitive morphological structures

A TgfβRI/Snai1-dependent developmental module at the core of vertebrate axial elongation

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