Senescence-induced cellular reprogramming drives cnidarian whole-body regeneration

Salinas‐Saavedra, Miguel; Febrimarsa, Febrimarsa; Krasovec, Gabriel; Horkan, Helen R.; Baxevanis, Andreas D.; Frank, Uri

doi:10.1016/j.celrep.2023.112687

Cited by 15 publications

(8 citation statements)

References 39 publications

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“…In this case, gastrodermal gland cells appear to dedifferentiate into i-cells [ 69 ], while gastrodermal digestive cells transdifferentiate into epidermal epitheliomuscular cells [ 70 ]. Moreover, a recent report using Hydractinia has shown that, when the hypostome is isolated from the body, cellular reprogramming triggered by cell senescence occurs in somatic cells, which convert into pluripotent Piwi1 + i-cells [ 71 ]. Although these reports support the possibility that dedifferentiation produces pluri/multipotent stem cells after isolation from the body, it is also possible that RSPCs are derived from their descendant cell types.…”

Section: Discussionmentioning

confidence: 99%

Distinct stem-like cell populations facilitate functional regeneration of the Cladonema medusa tentacle

Fujita,

Takahashi,

Kumano

et al. 2023

PLoS Biol

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Blastema formation is a crucial process that provides a cellular source for regenerating tissues and organs. While bilaterians have diversified blastema formation methods, its mechanisms in non-bilaterians remain poorly understood. Cnidarian jellyfish, or medusae, represent early-branching metazoans that exhibit complex morphology and possess defined appendage structures highlighted by tentacles with stinging cells (nematocytes). Here, we investigate the mechanisms of tentacle regeneration, using the hydrozoan jellyfish Cladonema pacificum. We show that proliferative cells accumulate at the tentacle amputation site and form a blastema composed of cells with stem cell morphology. Nucleoside pulse-chase experiments indicate that most repair-specific proliferative cells (RSPCs) in the blastema are distinct from resident stem cells. We further demonstrate that resident stem cells control nematogenesis and tentacle elongation during both homeostasis and regeneration as homeostatic stem cells, while RSPCs preferentially differentiate into epithelial cells in the newly formed tentacle, analogous to lineage-restricted stem/progenitor cells observed in salamander limbs. Taken together, our findings propose a regeneration mechanism that utilizes both resident homeostatic stem cells (RHSCs) and RSPCs, which in conjunction efficiently enable functional appendage regeneration, and provide novel insight into the diversification of blastema formation across animal evolution.

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Section: Discussionmentioning

confidence: 99%

Distinct stem-like cell populations facilitate functional regeneration of the Cladonema medusa tentacle

Fujita,

Takahashi,

Kumano

et al. 2023

PLoS Biol

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show abstract

“…In this case, gastrodermal gland cells appear to dedifferentiate into i-cells [67], while gastrodermal digestive cells transdifferentiate into epidermal epitheliomuscular cells [68]. Moreover, a recent report using Hydractinia has shown that, when the hypostome is isolated from the body, cellular reprogramming triggered by cell senescence occurs in somatic cells, which convert into pluripotent Piwi1 + i-cells [69]. Although these reports support the possibility that dedifferentiation produces pluri/multipotent stem cells after isolation from the body, it is also possible that RSPCs are derived from their descendant cell types.…”

Section: Discussionmentioning

confidence: 99%

Distinct stem-like cell populations facilitate functional regeneration of theCladonemamedusa tentacle

Fujita

Kuranaga

Miura

et al. 2022

Preprint

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Blastema formation is a crucial process that provides a cellular source for regenerating tissues and organs. While bilaterians have diversified blastema formation methods, its mechanisms in non-bilaterians remain poorly understood. Cnidarian jellyfish, or medusae, represent early-branching metazoans that exhibit complex morphology and possess defined appendage structures highlighted by tentacles with stinging cells (nematocytes). Here we investigate the mechanisms of tentacle regeneration, using the hydrozoan jellyfish Cladonema pacificum. We show that proliferative cells accumulate at the tentacle amputation site and form a blastema composed of cells with stem-like cell morphology. Lineage tracing experiments indicate that repair-specific proliferative cells in the blastema are distinct from resident stem-like cells. We further demonstrate that resident stem-like cells control nematogenesis and tentacle elongation during both homeostasis and regeneration, while repair-specific proliferative cells preferentially differentiate into epithelial cells in the newly formed tentacle, analogous to lineage-restricted stem/progenitor cells observed in salamander limbs. Taken together, our findings reveal a regeneration mechanism that utilizes both resident stem-like cells and repair-specific proliferative cells, which in conjunction efficiently enable functional appendage regeneration, and provide novel insight into the diversification of blastema formation across animal evolution.

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“…All sgRNAs were incubated together (500 ng/µl) with recombinant Cas9 (1 μg/μl; IDT, Cat. #1074181) for fifteen minutes prior to injection as described in 16 .…”

Section: Methodsmentioning

confidence: 99%

“…DNA was extracted as described in 16 . A two-step PCR approach was used to amplify genomic fragments.…”

Section: Methodsmentioning

confidence: 99%

A positive feedback loop between germ cells and gonads induces and maintains cnidarian sexual reproduction

Curantz,

Doody,

Horkan

et al. 2024

Preprint

Self Cite

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The fertile gonad includes cells of two distinct developmental origins: the somatic mesoderm and the germline. How somatic and germ cells interact to develop and maintain fertility is not well understood. Here, using grafting experiments and transgenic reporter animals, we find that a specific part of the gonad-the germinal zone-acts as a sexual organizer to induce and maintain de novo germ cells and somatic gonads in non-sexual tissue in the cnidarian Hydractinia symbiolongicarpus. We further show that germ cells express a novel member of the BMP family (Gonadless, Gls) that induces somatic gonad morphogenesis. Loss of Gls resulted in animals lacking somatic gonadal structures but having few, non-proliferative germ cells. We propose a model according to which a small number of primary germ cells drive gonad development though Gls morphogen secretion. The germinal zone in the newly formed gonad, in turn, provides positive feedback to induce secondary germ cells by activating Tfap2 (the master regulator of germ cell fate) in resident pluripotent stem cells. De novo induction of germ cells by gonads in adult life is absent in bilaterians with a sequestered germline. However, the contribution of germ cell signaling to the patterning of somatic gonadal tissue, as observed in Hydractinia, may be a general animal feature.

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Senescence-induced cellular reprogramming drives cnidarian whole-body regeneration

Cited by 15 publications

References 39 publications

Distinct stem-like cell populations facilitate functional regeneration of the Cladonema medusa tentacle

Distinct stem-like cell populations facilitate functional regeneration of the Cladonema medusa tentacle

Distinct stem-like cell populations facilitate functional regeneration of theCladonemamedusa tentacle

A positive feedback loop between germ cells and gonads induces and maintains cnidarian sexual reproduction

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