Wnt ligands regulate the asymmetric divisions of neuronal progenitors in <i>C. elegans</i> embryos

Kaur, Shilpa; Mélénec, Pauline; Murgan, Sabrina; Bordet, Guillaume; Recouvreux, Pierre; Lenne, Pierre-François; Bertrand, Vincent

doi:10.1242/dev.183186

Cited by 13 publications

(20 citation statements)

References 49 publications

(78 reference statements)

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“…Thus, we propose that the Wnt signaling pathway has an instructive, rather than a permissive role on K-to-DVB Td, with WNT ligands acting as positional cues in this process, instructing which K daughter will cease to be a rectal cell. An analogous situation has been recently demonstrated in the SMDD/AIY asymmetric cell division during embryonic development (Kaur et al, 2020).…”

Section: Discussionsupporting

confidence: 70%

A natural transdifferentiation event involving mitosis is empowered by integrating signaling inputs with conserved plasticity factors

Riva

Hajdůšková

Gally

et al. 2021

Preprint

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SUMMARYTransdifferentiation, or direct cell reprogramming, is the direct conversion of one fully differentiated cell type into another. Whether core mechanisms are shared between different transdifferentiation events, which can occur naturally in presence or in absence of cell division, is unclear. Our lab has previously characterized the Y-to-PDA natural transdifferentiation in Caenorhabditis elegans, which occurs without cell division and requires orthologs of vertebrates’ reprogramming factors. In this study, focusing on another transdifferentiation process, the K rectal cell-to-DVB GABAergic neuron, we report that the Y-to-PDA reprogramming factor SEM-4/SALL, SOX-2, CEH-6/POU are required for K-to-DVB transdifferentiation to allow the erasure of the rectal identity. In addition, cell division is necessary but not sufficient for this transdifferentiation event while the Wnt signaling plays distinct functions during the process including the selection of the daughter cell with a different fate, loss of the rectal identity and imposition of the specific neuronal subtype identity. We provide evidence that both the Wnt signaling and Y-to-PDA reprogramming factor SEM-4/SALL, SOX-2, CEH-6/POU act in parallel for the rectal identity erasure. Our results further support a model where antagonistic activities of SOX-2 and POP-1 and decreasing SOX-2 levels over time provide a timer for the acquisition of the final identity. In addition, the different levels of SOX-2 provide a mechanism for the integration of Wnt opposite dedifferentiation and re-differentiation functions during K-to-DVB transdifferentiation.

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Section: Discussionsupporting

confidence: 70%

A natural transdifferentiation event involving mitosis is empowered by integrating signaling inputs with conserved plasticity factors

Riva

Hajdůšková

Gally

et al. 2021

Preprint

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“…Wnt ligands bind receptor Fzd, alongside co-receptors Lrp5 or Lrp6, ultimately leading to β-catenin-dependent transcription of target genes. In several systems ( Bertrand, 2016 ; Goldstein et al, 2006 ; Huang and Niehrs, 2014 ; Kaur et al, 2020 ; Sugioka et al, 2011 ; Walston et al, 2004 ), including mouse embryonic stem cells (ESCs) ( Habib et al, 2013 ), localised Wnts induce oriented asymmetric cell division (ACD).…”

Section: Introductionmentioning

confidence: 99%

Wnt- and glutamate-receptors orchestrate stem cell dynamics and asymmetric cell division

Junyent

Reeves

Szczerkowski

et al. 2021

eLife

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The Wnt-pathway is part of a signalling network that regulates many aspects of cell biology. Recently we discovered crosstalk between AMPA/Kainate-type ionotropic glutamate receptors (iGluRs) and the Wnt-pathway during the initial Wnt3a-interaction at the cytonemes of mouse embryonic stem cells (ESCs). Here, we demonstrate that this crosstalk persists throughout the Wnt3a-response in ESCs. Both AMPA- and Kainate-receptors regulate early Wnt3a-recruitment, dynamics on the cell membrane, and orientation of the spindle towards a Wnt3a-source at mitosis. AMPA-receptors specifically are required for segregating cell fate components during Wnt3a-mediated asymmetric cell division (ACD). Using Wnt-pathway component knockout lines, we determine that Wnt co-receptor Lrp6 has particular functionality over Lrp5 in cytoneme formation, and in facilitating ACD. Both Lrp5 and 6, alongside pathway effector β-catenin act in concert to mediate the positioning of the dynamic interaction with, and spindle orientation to, a localized Wnt3a-source. Wnt-iGluR crosstalk may prove pervasive throughout embryonic and adult stem cell signalling.

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“…For example, it has been established that for the endomesoderm precursor cell EMS or the larval blast cell T, Wnt ligands, secreted from a posterior source, control the division orientation and the asymmetry of daughter cell fates (Goldstein, Takeshita, Mizumoto, & Sawa, 2006). Interestingly, it has been recently observed that three Wnt ligands (CWN-1, CWN-2 and MOM-2), coming from the posterior of the embryo, regulate in an instructive manner the terminal asymmetric divisions of embryonic neuronal progenitors (Kaur et al, 2020). This illustrates the importance of intercellular signaling during neuronal development in C. elegans.…”

Section: Neuronal Specification: a Combination Of Lineage Inheritance And Intercellular Signalingmentioning

confidence: 99%

Neuronal specification in C. elegans: combining lineage inheritance with intercellular signaling

Barrière

Bertrand

2020

Journal of Neurogenetics

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The nervous system is composed of a high diversity of neuronal types. How this diversity is generated during development is a key question in neurobiology. Addressing this question is one of the reasons that led Sydney Brenner to develop the nematode C. elegans as a model organism. While there was initially a debate on whether the neuronal specification follows a 'European' model (determined by ancestry) or an 'American' model (determined by intercellular communication), several decades of research have established that the truth lies somewhere in between. Neurons are specified by the combination of transcription factors inherited from the ancestor cells and signaling between neighboring cells (especially Wnt and Notch signaling). This converges to the activation in newly generated postmitotic neurons of a specific set of terminal selector transcription factors that initiate and maintain the differentiation of the neuron. In this review we also discuss the evolution of these specification mechanisms in other nematodes and beyond.

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Wnt ligands regulate the asymmetric divisions of neuronal progenitors in C. elegans embryos

Cited by 13 publications

References 49 publications

A natural transdifferentiation event involving mitosis is empowered by integrating signaling inputs with conserved plasticity factors

A natural transdifferentiation event involving mitosis is empowered by integrating signaling inputs with conserved plasticity factors

Wnt- and glutamate-receptors orchestrate stem cell dynamics and asymmetric cell division

Neuronal specification in C. elegans: combining lineage inheritance with intercellular signaling

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