Specialized progenitors and regeneration

Reddien, Peter W.

doi:10.1242/dev.080499

Cited by 99 publications

(97 citation statements)

References 59 publications

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“…Also, transient structures like the blastema are not always useful for comparative studies across distant taxa. Where blastemas can be characterized by a mass of cells clustering in the area of the wound after closure, leading to growth and regeneration into new organs or new body parts, it has been shown that the histological nature of this mass of cells is different in different regenerative structures (Shibata et al, 1999;Cebrià et al, 2002;Bosch et al, 2008;Kragl et al, 2009;Wenemoser and Reddien, 2010;Aboobaker, 2011;Reddien, 2013;Bely et al, 2014). Additionally in some epimorphic regenerative events, i.e., where local stimulation of cell proliferation precedes the development of the new part, there is a lack of structures that resemble a blastema, such as during the Ciona intestinalis siphon regeneration (Auger et al, 2010) or the whole body regeneration in colonial ascidians (Brown et al, 2009b).…”

Section: Resultsmentioning

confidence: 99%

Reconsidering regeneration in metazoans: an evo-devo approach

Tiozzo

Copley

2015

Front. Ecol. Evol.

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Regeneration of body structures is an ability widely but unevenly distributed amongst the animal kingdom. Understanding regenerative biology in metazoans means understanding the multiplicity of the cellular and molecular mechanisms that lead to the differentiation, morphogenesis and ultimately the development of a particular regenerating unit. In this manuscript we critically assess the evolutionary considerations suggesting that regeneration is an ancestral trait rather than a mechanism independently evolved in different taxa. As a general method to test evolutionary hypothesis on regeneration, we propose mechanistically dissecting the regenerative processes according to its conserved chronological steps: wound healing, mobilization of cell precursors and morphogenesis. We then suggest interpreting regenerative biology from an evo-devo perspective, proposing a possible theoretical framework and experimental approaches without necessarily invoking a common origin or only multiple losses of regenerative capabilities.

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Section: Resultsmentioning

confidence: 99%

Reconsidering regeneration in metazoans: an evo-devo approach

Tiozzo

Copley

2015

Front. Ecol. Evol.

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“…S4C; Table S1). Although we cannot specify the cell types that contribute to the gradient, we observed nuclear localization of β-CATENIN-1 in sub-epidermal muscular cells, which are the source of positional information cues (Witchley et al, 2013) and in proliferating cells, which correspond to neoblast and early progeny stem cells (Reddien, 2013) (Fig. S4D).…”

Section: Introductionmentioning

confidence: 95%

Localization of planarian β-CATENIN-1 reveals multiple roles during anterior-posterior regeneration and organogenesis

2016

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The β-catenin-dependent Wnt pathway exerts multiple contextdependent roles in embryonic and adult tissues. In planarians, β-catenin-1 is thought to specify posterior identities through the generation of an anteroposterior gradient. However, the existence of such a gradient has not been directly demonstrated. Here, we use a specific polyclonal antibody to demonstrate that nuclear β-CATENIN-1 exists as an anteroposterior gradient from the pre-pharyngeal region to the tail of the planarian Schmidtea polychroa. High levels in the posterior region steadily decrease towards the pre-pharyngeal region but then increase again in the head region. During regeneration, β-CATENIN-1 is nuclearized in both anterior and posterior blastemas, but the canonical WNT1 ligand only influences posterior nuclearization. Additionally, β-catenin-1 is required for proper anterior morphogenesis, consistent with the high levels of nuclear β-CATENIN-1 observed in this region. We further demonstrate that β-CATENIN-1 is abundant in developing and differentiated organs, and is particularly required for the specification of the germline. Altogether, our findings provide the first direct evidence of an anteroposterior nuclear β-CATENIN-1 gradient in adult planarians and uncover novel, context-dependent roles for β-catenin-1 during anterior regeneration and organogenesis.

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“…On the basis of elegant single cell transplantation studies in lethally irradiated planarians (Wagner et al, 2011), it has been estimated that less than 5% of the planarian stem cells are truly pluripotent (Rink, 2013). Therefore, we and others hypothesize that a fraction of the heterogeneous stem cell pool may be comprised of lineage-committed or specialized progenitor cells (Reddien, 2013). To fully understand the mechanisms underlying how neuronal diversity is maintained or reestablished in planarians it will be essential to define any neural precursor populations that may exist.…”

mentioning

confidence: 97%

Genome-wide analysis of the bHLH gene family in planarians identifies factors required for adult neurogenesis and neuronal regeneration

et al. 2013

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In contrast to most well-studied model organisms, planarians have a remarkable ability to completely regenerate a functional nervous system from a pluripotent stem cell population. Thus, planarians provide a powerful model to identify genes required for adult neurogenesis in vivo. We analyzed the basic helix-loop-helix (bHLH) family of transcription factors, many of which are crucial for nervous system development and have been implicated in human diseases. However, their potential roles in adult neurogenesis or central nervous system (CNS) function are not well understood. We identified 44 planarian bHLH homologs, determined their patterns of expression in the animal and assessed their functions using RNAi. We found nine bHLHs expressed in stem cells and neurons that are required for CNS regeneration. Our analyses revealed that homologs of coe, hes (hesl-3) and sim label progenitors in intact planarians, and following amputation we observed an enrichment of coe + and sim + progenitors near the wound site. RNAi knockdown of coe, hesl-3 or sim led to defects in CNS regeneration, including failure of the cephalic ganglia to properly pattern and a loss of expression of distinct neuronal subtype markers. Together, these data indicate that coe, hesl-3 and sim label neural progenitor cells, which serve to generate new neurons in uninjured or regenerating animals. Our study demonstrates that this model will be useful to investigate how stem cells interpret and respond to genetic and environmental cues in the CNS and to examine the role of bHLH transcription factors in adult tissue regeneration.

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Specialized progenitors and regeneration

Cited by 99 publications

References 59 publications

Reconsidering regeneration in metazoans: an evo-devo approach

Reconsidering regeneration in metazoans: an evo-devo approach

Localization of planarian β-CATENIN-1 reveals multiple roles during anterior-posterior regeneration and organogenesis

Genome-wide analysis of the bHLH gene family in planarians identifies factors required for adult neurogenesis and neuronal regeneration

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