Reconsidering regeneration in metazoans: an evo-devo approach

Tiozzo, Stefano; Copley, Richard R.

doi:10.3389/fevo.2015.00067

Cited by 57 publications

(85 citation statements)

References 155 publications

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“…While regeneration phenomena are widespread among metazoans, the regenerative capacity varies considerably within a given phylum and at the organ/tissue levels within an organism (Bely and Nyberg, 2010; Tiozzo and Copley, 2015). Although still quite variable within the phylum, cnidarians in general exhibit tremendous tissue plasticity and regeneration abilities (Figure 6).…”

Section: Muscle Plasticity and Regeneration In Cnidariansmentioning

confidence: 99%

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Leclère

Röttinger

2017

Front. Cell Dev. Biol.

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The ability to perform muscle contractions is one of the most important and distinctive features of eumetazoans. As the sister group to bilaterians, cnidarians (sea anemones, corals, jellyfish, and hydroids) hold an informative phylogenetic position for understanding muscle evolution. Here, we review current knowledge on muscle function, diversity, development, regeneration and evolution in cnidarians. Cnidarian muscles are involved in various activities, such as feeding, escape, locomotion and defense, in close association with the nervous system. This variety is reflected in the large diversity of muscle organizations found in Cnidaria. Smooth epithelial muscle is thought to be the most common type, and is inferred to be the ancestral muscle type for Cnidaria, while striated muscle fibers and non-epithelial myocytes would have been convergently acquired within Cnidaria. Current knowledge of cnidarian muscle development and its regeneration is limited. While orthologs of myogenic regulatory factors such as MyoD have yet to be found in cnidarian genomes, striated muscle formation potentially involves well-conserved myogenic genes, such as twist and mef2. Although satellite cells have yet to be identified in cnidarians, muscle plasticity (e.g., de- and re-differentiation, fiber repolarization) in a regenerative context and its potential role during regeneration has started to be addressed in a few cnidarian systems. The development of novel tools to study those organisms has created new opportunities to investigate in depth the development and regeneration of cnidarian muscle cells and how they contribute to the regenerative process.

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Section: Muscle Plasticity and Regeneration In Cnidariansmentioning

confidence: 99%

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Leclère

Röttinger

2017

Front. Cell Dev. Biol.

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“…salamanders) and non-regenerating vertebrates (Seifert et al, 2012). Regeneration is likely to be an ancestral animal trait that utilizes many of the molecular mechanisms of development, thus implying evolutionary loss of this trait in some lineages (Bely and Nyberg, 2010;Morgan, 1901;Tiozzo and Copley, 2015). By identifying points of evolutionary conservation and divergence in the molecular mechanisms underlying regeneration, progress can be made toward illuminating how different species can accomplish the same task in vastly different ways.…”

Section: Introductionmentioning

confidence: 99%

A microRNA-mRNA expression network during oral siphon regeneration in Ciona

et al. 2017

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Here we present a parallel study of mRNA and microRNA expression during oral siphon (OS) regeneration in Ciona robusta, and the derived network of their interactions. In the process of identifying 248 mRNAs and 15 microRNAs as differentially expressed, we also identified 57 novel microRNAs, several of which are among the most highly differentially expressed. Analysis of functional categories identified enriched transcripts related to stress responses and apoptosis at the wound healing stage, signaling pathways including Wnt and TGFβ during early regrowth, and negative regulation of extracellular proteases in late stage regeneration. Consistent with the expression results, we found that inhibition of TGFβ signaling blocked OS regeneration. A correlation network was subsequently inferred for all predicted microRNA-mRNA target pairs expressed during regeneration. Network-based clustering associated transcripts into 22 non-overlapping groups, the functional analysis of which showed enrichment of stress response, signaling pathway and extracellular protease categories that could be related to specific microRNAs. Predicted targets of the miR-9 cluster suggest a role in regulating differentiation and the proliferative state of neural progenitors through regulation of the cytoskeleton and cell cycle.

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“…Regenerative ability in the animal kingdom exists along a spectrum, ranging from mammals, where regenerative potential only exists within limited timeframes and types of tissue, to animals like the hydra, capable of regenerating their entire body plan from a single cell (Birnbaum & Alvarado, ; Brockes & Kumar, ; Tanaka & Reddien, ; Tiozzo & Copley, ). In the middle of this range sit the anuran amphibians, the class of amphibians including frogs and toads that lose their tail during metamorphosis.…”

Section: Introductionmentioning

confidence: 99%

Recovery of the Xenopus laevis heart from ROS‐induced stress utilizes conserved pathways of cardiac regeneration

Jewhurst

McLaughlin

2019

Dev Growth Differ

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Urodele amphibians and some fish are capable of regenerating up to a quarter of their heart tissue after cardiac injury. While many anuran amphibians like Xenopus laevis are not capable of such feats, they are able to repair lesser levels of cardiac damage, such as that caused by oxidative stress, to a far greater degree than mammals. Using an optogenetic stress induction model that utilizes the protein KillerRed, we have investigated the extent to which mechanisms of cardiac regeneration are conserved during the restoration of normal heart morphology post oxidative stress in X. laevis tadpoles. We focused particularly on the processes of cardiomyocyte proliferation and dedifferentiation, as well as the pathways that facilitate the regulation of these processes. The cardiac response to KillerRed‐induced injury in X. laevis tadpole hearts consists of a phase dominated by indicators of cardiac stress, followed by a repair‐like phase with characteristics similar to mechanisms of cardiac regeneration in urodeles and fish. In the latter phase, we found markers associated with partial dedifferentiation and cardiomyocyte proliferation in the injured tadpole heart, which, unlike in regenerating hearts, are not dependent on Notch or retinoic acid signaling. Ultimately, the X. laevis cardiac response to KillerRed‐induced oxidative stress shares characteristics with both mammalian and urodele/fish repair mechanisms, but is nonetheless a unique form of recovery, occupying an intermediate place on the spectrum of cardiac regenerative ability. An understanding of how Xenopus repairs cardiac damage can help bridge the gap between mammals and urodeles and contribute to new methods of treating heart disease.

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Reconsidering regeneration in metazoans: an evo-devo approach

Cited by 57 publications

References 155 publications

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

Diversity of Cnidarian Muscles: Function, Anatomy, Development and Regeneration

A microRNA-mRNA expression network during oral siphon regeneration in Ciona

Recovery of the Xenopus laevis heart from ROS‐induced stress utilizes conserved pathways of cardiac regeneration

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