Wnt, Ptk7, and FGFRL expression gradients control trunk positional identity in planarian regeneration

Lander, Rachel M.; Petersen, Christian P.

doi:10.7554/elife.12850

Cited by 69 publications

(97 citation statements)

References 51 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This observation supports the hypothesis that the wnt1 ligand, secreted by the newly formed posterior organizer, is the morphogen that sustains nuclear translocation of β-CATENIN-1 at the posterior pole during regeneration (Adell et al, 2009;Petersen and Reddien, 2009b). Later on, the nested expression of the other posterior Wnt ligands would control the re-establishment and maintenance of the gradient (Hayashi et al, 2011;Lander and Petersen, 2016;März et al, 2013;Scimone et al, 2016;Sureda-Gómez et al, 2015) (Fig. 6A).…”

Section: A Gradient Of β-Catenin-1 Along the Ap Axissupporting

confidence: 78%

“…In recent years, functional characterization of the key elements of the canonical Wnt pathway suggested that the morphogenetic role of the wnt ligands secreted by a posterior organizing center could generate a gradient of nuclear β-CATENIN-1 responsible for the specification and maintenance of the planarian AP axis (Adell et al, 2009 and Reddien, 2009b;Scimone et al, 2016;Sureda-Gómez et al, 2015). The nested expression of several Wnt ligands (wnt1, wnt11-1, wnt11-2 and wnt11-5) in the pharyngeal and tail region of the planarian body, and the expression of Wnt inhibitors (notum and sFRP) in the anterior tip of the head gave support to the gradient hypothesis Gurley et al, 2010;Lander and Petersen, 2016;Petersen and Reddien, 2011;Scimone et al, 2016;Sureda-Gómez et al, 2015). Additionally, inhibition of these posterior Wnt ligands leads to 'tail-less' or 'two-headed' planarians, as does the inhibition of β-catenin-1 itself (Adell et al, 2009;Gurley et al, 2010;Petersen and Reddien, 2009b;Sureda-Gómez et al, 2015).…”

Section: A Gradient Of β-Catenin-1 Along the Ap Axismentioning

confidence: 84%

“…Moreover, it is known that several Wnt ligands are expressed posteriorly, whereas inhibitors (e.g. notum and sFRP) localize to the anterior pole, and their inhibition leads to anteriorized or posteriorized phenotypes, respectively (Adell et al, 2009;Gurley et al, 2010;Lander and Petersen, 2016;Reddien, 2009b, 2011;Scimone et al, 2016;Sureda-Gómez et al, 2015). Interestingly, recent reports have suggested that β-catenin-1 exerts additional roles in eye and brain patterning (Hill and Petersen, 2015;Owen et al, 2015), which is consistent with the ubiquitous mRNA expression of β-catenin-1 (Gurley et al, 2008;Iglesias et al, 2008;Petersen and Reddien, 2008).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

2016

View full text Add to dashboard Cite

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.

show abstract

Section: A Gradient Of β-Catenin-1 Along the Ap Axissupporting

confidence: 78%

Section: A Gradient Of β-Catenin-1 Along the Ap Axismentioning

confidence: 84%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

2016

View full text Add to dashboard Cite

show abstract

“…Inhibition of multiple PCGs (such as bmp4, wntP-2 , and ndl-3 ) by RNA interference (RNAi) causes patterning phenotypes, such as ectopic heads, pharynges, or eyes (23–26). After amputation, PCG expression domains are rapidly re-established in muscle (in a matter of 2–3 days).…”

Section: Transient Discordance Between Anatomy and Positional Informamentioning

confidence: 99%

Self-organization and progenitor targeting generate stable patterns in planarian regeneration

Atabay

LoCascio

Hoog

et al. 2018

Science

View full text Add to dashboard Cite

During animal regeneration cells must organize into discrete and functional systems. We show that self-organization, along with patterning cues, govern progenitor behavior in planarian regeneration. Surgical paradigms allowed manipulation of planarian eye regeneration in predictable locations and numbers, generating alternative stable neuroanatomical states for wild-type animals with multiple functional ectopic eyes. We utilized animals with multiple ectopic eyes and eye transplantation to demonstrate that broad progenitor specification, combined with self-organization, allows anatomy maintenance during regeneration. We propose a model for regenerative progenitors involving (i) migratory targeting cues, (ii) self-organization into existing or regenerating eyes, and (iii) a broad zone, associated with coarse progenitor specification, in which eyes can be targeted by progenitors. These three properties help explain how tissues can be organized during regeneration.

show abstract

“…Colorimetric (NBT/BCIP) or fluorescence in situ hybridizations were performed as described (Lander and Petersen, 2016) after fixation in 4% formaldehyde and bleaching (Pearson et al, 2009) using blocking solution containing 10% horse serum and western blot blocking reagent (Roche) (King and Newmark, 2013). Digoxigenin-or fluorescein-labeled riboprobes were synthesized as described (Pearson et al, 2009) For immunostainings, animals were fixed in Carnoy's solution as described (Hill and Petersen, 2015), using tyramide amplification to detect labeling with rabbit anti-phospho-ser10 Histone H3 (1:3000, Cell Signaling D2C8, lot 3377S) or Alexa Fluor 586-conjugated goat anti-mouse IgG (Invitrogen A11031, lot 822389) to detect labeling with mouse antisynapsin (1:50, anti-SYNORF1, Developmental Studies Hybridoma Bank clone 3C11).…”

Section: In Situ Hybridization and Immunostainingmentioning

confidence: 99%

Integrin suppresses neurogenesis and regulates brain tissue assembly in planarian regeneration

Bonar

Petersen

2017

Development

View full text Add to dashboard Cite

Animals capable of adult regeneration require specific signaling to control injury-induced cell proliferation, specification and patterning, but comparatively little is known about how the regeneration blastema assembles differentiating cells into well-structured functional tissues. Using the planarian Schmidtea mediterranea as a model, we identify β1-integrin as a crucial regulator of blastema architecture. β1-integrin(RNAi) animals formed small head blastemas with severe tissue disorganization, including ectopic neural spheroids containing differentiated neurons normally found in distinct organs. By mimicking aspects of normal brain architecture but without normal cell-type regionalization, these spheroids bore a resemblance to mammalian tissue organoids synthesized in vitro. We identified one of four planarian integrin-alpha subunits inhibition of which phenocopied these effects, suggesting that a specific receptor controls brain organization through regeneration. Neoblast stem cells and progenitor cells were mislocalized in β1-integrin(RNAi) animals without significantly altered body-wide patterning. Furthermore, tissue disorganization phenotypes were most pronounced in animals undergoing brain regeneration and not homeostatic maintenance or regeneration-induced remodeling of the brain. These results suggest that integrin signaling ensures proper progenitor recruitment after injury, enabling the generation of largescale tissue organization within the regeneration blastema.

show abstract

Wnt, Ptk7, and FGFRL expression gradients control trunk positional identity in planarian regeneration

Cited by 69 publications

References 51 publications

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

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

Self-organization and progenitor targeting generate stable patterns in planarian regeneration

Integrin suppresses neurogenesis and regulates brain tissue assembly in planarian regeneration

Contact Info

Product

Resources

About