Model systems for regeneration: <i>Hydra</i>

Vogg, Matthias Christian; Galliot, Brigitte; Tsiairis, Charisios D.

doi:10.1242/dev.177212

Cited by 81 publications

(72 citation statements)

References 113 publications

(139 reference statements)

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“…This implies that the entire radial axis of the umbrella possesses the potential to form a manubrium, and that a control mechanism exists to prevent multiple manubria from forming. One explanation could be that Clytia manubrium has an organizing role, as is the case for the hypostome (mouth) of Hydra polyps (Bode, 2011;Meinhardt, 1993;Vogg et al, 2019), and provides an inhibitory signal that spreads through the umbrella and prevents the induction of additional manubria. We tested this hypothesis by grafting supernumerary manubria at different subumbrellar positions.…”

Section: Why Does Only One Manubrium Usually Regenerate?mentioning

confidence: 99%

“…The relative contributions of cell proliferation and tissue remodeling to the restoration of form vary widely among regenerating species. In the classic regeneration model Hydra, as in Clytia, body regeneration mainly involves remodeling and repatterning of existing tissues (Bode, 2003;Vogg et al, 2019). In contrast, cell proliferation plays a prominent role during regeneration of Nematostella and Hydractinia polyps (Amiel et al, 2015;Bradshaw et al, 2015;Passamaneck and Martindale, 2012).…”

Section: Distinct Cell Behaviors Coordinated In Time and Spacementioning

confidence: 99%

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Pattern regulation in a regenerating jellyfish

Sinigaglia

Péron

Eichelbrenner

et al. 2020

eLife

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Clytia hemisphaerica jellyfish, with their tetraradial symmetry, offer a novel paradigm for addressing patterning mechanisms during regeneration. Here we show that an interplay between mechanical forces, cell migration and proliferation allows jellyfish fragments to regain shape and functionality rapidly, notably by efficient restoration of the central feeding organ (manubrium). Fragmentation first triggers actomyosin-powered remodeling that restores body umbrella shape, causing radial smooth muscle fibers to converge around 'hubs' which serve as positional landmarks. Stabilization of these hubs, and associated expression of Wnt6, depends on the configuration of the adjoining muscle fiber 'spokes'. Stabilized hubs presage the site of the manubrium blastema, whose growth is Wnt/β-catenin dependent and fueled by both cell proliferation and long-range cell recruitment. Manubrium morphogenesis is modulated by its connections with the gastrovascular canal system. We conclude that body patterning in regenerating jellyfish emerges mainly from local interactions, triggered and directed by the remodeling process.

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Section: Why Does Only One Manubrium Usually Regenerate?mentioning

confidence: 99%

Section: Distinct Cell Behaviors Coordinated In Time and Spacementioning

confidence: 99%

Pattern regulation in a regenerating jellyfish

Sinigaglia

Péron

Eichelbrenner

et al. 2020

eLife

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“…These then polarize and transform into fully functional hydra 1 , albeit smaller than the adult consisting of about 100.000 cells. Hydra represents a well-known model organism for its remarkable regenerative properties 2 . Regrowth from a spheroid requires de-novo axis definition 3,4 .…”

Section: Introductionmentioning

confidence: 99%

Symmetry breaking andde-novoaxis formation inhydraspheroids: the microtubule cytoskeleton as a pivotal element

Sander

Pasula

Sander

et al. 2020

Preprint

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The establishment of polarity in cells and tissues is one of the first steps in multicellular development. The 'eternal embryo' hydra can completely regenerate from a disorganised cell cluster or a small fragment of tissue of about 10, 000 cells. During regeneration, the cells first form a hollow cell spheroid, which then undergoes de-novo symmetry breaking to irreversibly polarise. Here, we address the symmetry-related shape changes. Prior to axis establishment, the spherical aggregates of regenerating cells show highly coordinated mechanical oscillations on several timescales that are isotropic in space. There are transient periods of fluctuations in defined arbitrary directions, until these undergo a clearly identified irreversible transition to directed fluctuations along the future main axis of the regenerating hydra. Stabilised cytosolic actin structures disappear during the de-novo polarisation, while polymerised microtubules remain. Drugs that depolymerise actin filaments accelerate the symmetry breaking process, while drug-stabilised actin filaments prevent it. Nocodazole-depolymerised microtubules prevent symmetry breaking, but it can be rescued by the microtubule-stabilising drug paclitaxel at concentrations where microtubular structures start to reappear. We discuss the possibility that these mechanical fluctuations induce the orientation of the microtubules, which contribute to β -catenin nuclear translocation, to increase the organiserforming-potential of the cells. Our data suggest that in regenerating hydra spheroids, the biomechanical shape fluctuations are an integral part of the cooperative polarisation of the self-organising hydra, during which microtubules play a pivotal role.

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“…In the eighteenth century, Abraham Trembley (1719–1784) discovered regeneration in the hydra, which can recreate complete structures each time from bisected parts of the body 1 . Now, we know that some species from certain taxonomic groups, such as cnidarians, planarians, annelids and colonial ascidians, can undergo whole body regeneration and show no limitations of regeneration after recurrent fragmentations 2 – 5 . Among vertebrates, the concept of unlimited organ regeneration has been explored in several species.…”

Section: Introductionmentioning

confidence: 99%

Multiple cryoinjuries modulate the efficiency of zebrafish heart regeneration

Bise

Sallin

Pfefferli

et al. 2020

Sci Rep

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Zebrafish can regenerate their damaged hearts throughout their lifespan. It is, however, unknown, whether regeneration remains effective when challenged with successive cycles of cardiac damage in the same animals. Here, we assessed ventricular restoration after two, three and six cryoinjuries interspaced by recovery periods. Using transgenic cell-lineage tracing analysis, we demonstrated that the second cryoinjury damages the regenerated area from the preceding injury, validating the experimental approach. We identified that after multiple cryoinjuries, all hearts regrow a thickened myocardium, similarly to hearts after one cryoinjury. However, the efficiency of scar resorption decreased with the number of repeated cryoinjuries. After six cryoinjuries, all examined hearts failed to completely resolve the fibrotic tissue, demonstrating reduced myocardial restoration. This phenotype was associated with enhanced recruitment of neutrophils and decreased cardiomyocyte proliferation and dedifferentiation at the early regenerative phase. Furthermore, we found that each repeated cryoinjury increased the accumulation of collagen at the injury site. Our analysis demonstrates that the cardiac regenerative program can be successfully activated many times, despite a persisting scar in the wounded area. This finding provides a new perspective for regenerative therapies, aiming in stimulation of organ regeneration in the presence of fibrotic tissue in mammalian models and humans.

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Model systems for regeneration: Hydra

Abstract: Hydra as a model system for regeneration

Cited by 81 publications

References 113 publications

Pattern regulation in a regenerating jellyfish

Pattern regulation in a regenerating jellyfish

Symmetry breaking andde-novoaxis formation inhydraspheroids: the microtubule cytoskeleton as a pivotal element

Multiple cryoinjuries modulate the efficiency of zebrafish heart regeneration

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