Antagonistic Self-Organizing Patterning Systems Control Maintenance and Regeneration of the Anteroposterior Axis in Planarians

Stückemann, Tom; Cleland, James; Werner, Steffen; Vu, Hanh Thi-Kim; Bayersdorf, Robert; Liu, Shang-Yun; Friedrich, Benjamin M.; Jülicher, Frank; Rink, Jochen C.

doi:10.1016/j.devcel.2016.12.024

Cited by 110 publications

(149 citation statements)

References 56 publications

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“…Interestingly, the expression of the cell autonomous antagonist of Wnt/b-catenin named naked cuticle in Drosophila (Nkd, seq61685) is graded apical to basal at all five positions ( Fig. 3), consistent with a graded regulation of Wnt signaling activity along the Hydra body axis as observed in the planarian worm S. mediterranea (Stuckemann et al, 2017).…”

Section: Genes Showing Modulated Expression At the Extremitiessupporting

confidence: 63%

Generic and context-dependent gene modulations duringHydrawhole body regeneration

Wenger

Buzgariu

Perruchoud

et al. 2019

Preprint

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The cnidarian Hydra is a classical model of whole-body regeneration. Historically, Hydra apical regeneration has received more attention than its basal counterpart, most studies considering these two regenerative processes independently. We present here a transcriptome-wide comparative analysis of apical and basal regeneration after decapitation and mid-gastric bisection, augmented with a characterization of positional and cell-type expression patterns in non-regenerating animals. The profiles of 25'637 Hydra transcripts are available on HydrATLAS (https://hydratlas.unige.ch), a web interface allowing a convenient access to each transcript profile. These data indicate that generic impulse-type modulations occur during the first four hours post-amputation, consistent with a similar integration of injury-related cues on both sides of the amputation plane. Initial divergences in gene regulations are observed in regenerating tips between four and eight hours post-amputation, followed by a dramatic transcriptomic reprogramming between eight and 16 hours when regulations become sustained. As expected, central components of apical patterning, Wnt3 and HyBra1, are among the earliest genes up-regulated during apical regeneration. During early basal regeneration, a BMP signaling ligand (BMP5-8c) and a potential BMP inhibitor (NBL1) are up-regulated, suggesting that BMP signaling is involved in the basal organizer, as supported by higher levels of phosphorylated Smad in the basal region and by the LiCl-induced extension of NBL1 expression. By contrast, upon ectopic activation of Wnt/b-catenin signaling, NBL1 is no longer expressed, basal differentiation is not maintained and basal regeneration is abolished. A tight cross-talk between Wnt/b-catenin apically and BMP signaling basally appears necessary for maintaining and regenerating Hydra anatomy.

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Section: Genes Showing Modulated Expression At the Extremitiessupporting

confidence: 63%

Generic and context-dependent gene modulations duringHydrawhole body regeneration

Wenger

Buzgariu

Perruchoud

et al. 2019

Preprint

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“…In self-organizing systems, ordered patterns emerge from an initially disordered and noisy environment. Selforganization has been invoked in embryonic development (3–9), regeneration (10, 11), and in the in vitro formation of complex structures such as the optic cup (12) and organoids (13, 14). To explore the role of self-organization in regeneration, we investigated the ability of planarians to completely regenerate missing organs.…”

mentioning

confidence: 99%

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

Atabay

LoCascio

Hoog

et al. 2018

Science

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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.

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“…First, it only requires the presence of a single morphogen (SI Appendix, Sec. 1.G) which could correspond to many practical situations where a pair of activator/inhibitor has not been clearly identified, for instance the role of Wnt in the antero-posterior pattern of planarians [41]. Second, it possesses spatial scaling properties regarding to its fundamental mode, as compared to a Turing instability.…”

Section: Turing-keller-segel Instabilitiesmentioning

confidence: 99%

Theory of mechano-chemical patterning in biphasic biological tissues

Recho

Hallou

Hannezo

2018

Preprint

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The formation of self-organized patterns is key to the morphogenesis of multicellular organisms, although a comprehensive theory of biological pattern formation is still lacking. Here, we propose a biologically realistic and unifying approach to emergent pattern formation. Our biphasic model of multicellular tissues incorporates turnover and transport of morphogens controlling cell differentiation and tissue mechanics in a single framework, where one tissue phase consists of a poroelastic network made of cells and the other is the extracellular fluid permeating between cells. While this model encompasses previous theories approximating tissues to inert monophasic media, such as Turing’s reaction-diffusion model, it overcomes some of their key limitations permitting pattern formation via any two-species biochemical kinetics thanks to mechanically induced cross-diffusion flows. Moreover, we unravel a qualitatively different advection-driven instability which allows for the formation of patterns with a single morphogen and which single mode pattern scales with tissue size. We discuss the potential relevance of these findings for tissue morphogenesis.

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Antagonistic Self-Organizing Patterning Systems Control Maintenance and Regeneration of the Anteroposterior Axis in Planarians

Cited by 110 publications

References 56 publications

Generic and context-dependent gene modulations duringHydrawhole body regeneration

Generic and context-dependent gene modulations duringHydrawhole body regeneration

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

Theory of mechano-chemical patterning in biphasic biological tissues

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