Editorial

11 pages, 5042 KiB

Open AccessEditorial

Introduction to the Study on Regeneration in Lizards as an Amniote Model of Organ Regeneration

by Lorenzo Alibardi

J. Dev. Biol. 2021, 9(4), 51; https://0-doi-org.brum.beds.ac.uk/10.3390/jdb9040051 - 22 Nov 2021

Cited by 1 | Viewed by 2961

Initial observations on the regeneration of the tail in lizards were recorded in brief notes by Aristotle over 2000 years ago, as reported in his book, History of Animals (cited from [...] Full article

(This article belongs to the Special Issue Lizards As Reptilian Models To Analyze Organ Regeneration in Amniotes)

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Research

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13 pages, 2329 KiB

Open AccessArticle

De Novo Transcriptome Sequencing and Analysis of Differential Gene Expression among Various Stages of Tail Regeneration in Hemidactylus flaviviridis

by Sonam Patel, Isha Ranadive, Pranav Buch, Kashmira Khaire and Suresh Balakrishnan

J. Dev. Biol. 2022, 10(2), 24; https://0-doi-org.brum.beds.ac.uk/10.3390/jdb10020024 - 14 Jun 2022

Cited by 6 | Viewed by 2026

Abstract

Across the animal kingdom, lizards are the only amniotes capable of regenerating their lost tail through epimorphosis. Of the many reptiles, the northern house gecko, Hemidactylus flaviviridis, is an excellent model system that is used for understanding the mechanism of epimorphic regeneration. [...] Read more.

Across the animal kingdom, lizards are the only amniotes capable of regenerating their lost tail through epimorphosis. Of the many reptiles, the northern house gecko, Hemidactylus flaviviridis, is an excellent model system that is used for understanding the mechanism of epimorphic regeneration. A stage-specific transcriptome profile was generated in the current study following an autotomized tail with the HiSeq2500 platform. The reads obtained from de novo sequencing were filtered and high-quality reads were considered for gene ontology (GO) annotation and pathway analysis. Millions of reads were recorded for each stage upon de novo assembly. Up and down-regulated transcripts were categorized for early blastema (EBL), blastema (BL) and differentiation (DF) stages compared to the normal tail (NT) by differential gene expression analysis. The transcripts from developmentally significant pathways such as FGF, Wnt, Shh and TGF-β/BMP were present during tail regeneration. Additionally, differential expression of transcripts was recorded from biological processes, namely inflammation, cell proliferation, apoptosis and cell migration. Overall, the study reveals the stage-wise transcriptome analysis in conjunction with cellular processes as well as molecular signaling pathways during lizard tail regeneration. The knowledge obtained from the data can be extrapolated to configure regenerative responses in other amniotes, including humans, upon loss of a complex organ. Full article

(This article belongs to the Special Issue Lizards As Reptilian Models To Analyze Organ Regeneration in Amniotes)

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22 pages, 8386 KiB

Open AccessArticle

Radial Glia and Neuronal-like Ependymal Cells Are Present within the Spinal Cord of the Trunk (Body) in the Leopard Gecko (Eublepharis macularius)

by Sarah V. Donato and Matthew K. Vickaryous

J. Dev. Biol. 2022, 10(2), 21; https://0-doi-org.brum.beds.ac.uk/10.3390/jdb10020021 - 01 Jun 2022

Cited by 1 | Viewed by 2759

Abstract

As is the case for many lizards, leopard geckos (Eublepharis macularius) can self-detach a portion of their tail to escape predation, and then regenerate a replacement complete with a spinal cord. Previous research has shown that endogenous populations of neural stem/progenitor [...] Read more.

As is the case for many lizards, leopard geckos (Eublepharis macularius) can self-detach a portion of their tail to escape predation, and then regenerate a replacement complete with a spinal cord. Previous research has shown that endogenous populations of neural stem/progenitor cells (NSPCs) reside within the spinal cord of the original tail. In response to tail loss, these NSPCs are activated and contribute to regeneration. Here, we investigate whether similar populations of NSPCs are found within the spinal cord of the trunk (body). Using a long-duration 5-bromo-2′-deoxyuridine pulse-chase experiment, we determined that a population of cells within the ependymal layer are label-retaining following a 20-week chase. Tail loss does not significantly alter rates of ependymal cell proliferation within the trunk spinal cord. Ependymal cells of the trunk spinal cord express SOX2 and represent at least two distinct cell populations: radial glial-like (glial fibrillary acidic protein- and Vimentin-expressing) cells; and neuronal-like (HuCD-expressing) cells. Taken together, these data demonstrate that NSPCs of the trunk spinal cord closely resemble those of the tail and support the use of the tail spinal cord as a less invasive proxy for body spinal cord injury investigations. Full article

(This article belongs to the Special Issue Lizards As Reptilian Models To Analyze Organ Regeneration in Amniotes)

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11 pages, 2030 KiB

Open AccessFeature PaperArticle

Lizard Blastema Organoid Model Recapitulates Regenerated Tail Chondrogenesis

by Ariel C. Vonk, Sarah C. Hasel-Kolossa, Gabriela A. Lopez, Megan L. Hudnall, Darian J. Gamble and Thomas P. Lozito

J. Dev. Biol. 2022, 10(1), 12; https://0-doi-org.brum.beds.ac.uk/10.3390/jdb10010012 - 10 Feb 2022

Cited by 3 | Viewed by 3561

Abstract

(1) Background: Lizard tail regeneration provides a unique model of blastema-based tissue regeneration for large-scale appendage replacement in amniotes. Green anole lizard (Anolis carolinensis) blastemas contain fibroblastic connective tissue cells (FCTCs), which respond to hedgehog signaling to create cartilage in vivo. However, [...] Read more.

(1) Background: Lizard tail regeneration provides a unique model of blastema-based tissue regeneration for large-scale appendage replacement in amniotes. Green anole lizard (Anolis carolinensis) blastemas contain fibroblastic connective tissue cells (FCTCs), which respond to hedgehog signaling to create cartilage in vivo. However, an in vitro model of the blastema has not previously been achieved in culture. (2) Methods: By testing two adapted tissue dissociation protocols and two optimized media formulations, lizard tail FCTCs were pelleted in vitro and grown in a micromass blastema organoid culture. Pellets were analyzed by histology and in situ hybridization for FCTC and cartilage markers alongside staged original and regenerating lizard tails. (3) Results: Using an optimized serum-free media and a trypsin- and collagenase II-based dissociation protocol, micromass blastema organoids were formed. Organoid cultures expressed FCTC marker CDH11 and produced cartilage in response to hedgehog signaling in vitro, mimicking in vivo blastema and tail regeneration. (4) Conclusions: Lizard tail blastema regeneration can be modeled in vitro using micromass organoid culture, recapitulating in vivo FCTC marker expression patterns and chondrogenic potential. Full article

(This article belongs to the Special Issue Lizards As Reptilian Models To Analyze Organ Regeneration in Amniotes)

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21 pages, 3458 KiB

Open AccessArticle

The Review of the Autotomy of Agamid Lizards with Considerations about the Types of Autotomy and Regeneration

by Natalia Borisovna Ananjeva, Dmitry Anatolyevich Gordeev and Dmitry Vyacheslavovich Korost

J. Dev. Biol. 2021, 9(3), 32; https://0-doi-org.brum.beds.ac.uk/10.3390/jdb9030032 - 16 Aug 2021

Cited by 5 | Viewed by 4383

Abstract

We present a review of the data on the intervertebral autotomy and regeneration of agamid lizards based on an analysis of information obtained over a 35-year period after the publication of thorough reviews (Arnold, 1984, 1988 and Bellairs, Bryant, 1985). It is supplemented [...] Read more.

We present a review of the data on the intervertebral autotomy and regeneration of agamid lizards based on an analysis of information obtained over a 35-year period after the publication of thorough reviews (Arnold, 1984, 1988 and Bellairs, Bryant, 1985). It is supplemented by our own studies of 869 specimens of agamid lizards (Sauria, Agamidae) stored in the herpetological collections of the Zoological Institute of the Russian Academy of Sciences (St. Petersburg, Russia) and the Zoological Museum of the Moscow State University (Moscow, Russia), represented by 31 species of 16 genera. The manifestations of the ability for autotomy and regeneration in phylogenetic lineages within the family—Leiolepidinae, Amphibolurinae, Agaminae, Draconinae—are considered. A comparative morphological analysis of the structure of the caudal vertebrae was carried out using the Computer Microtomography Methods (micro-CT) in the following ecomorphological types of agama: (1) with developed abilities to caudal autotomy and regeneration, (2) with the ability to caudal autotomy but without regeneration and (3) without the ability to autotomy. The phenomenon of intervertebral autotomy (urotomy) in snakes is considered too. Possible ways of evolution of the ability to caudal autotomy as a defense strategy against predators are discussed in the phylogenetic context. Full article

(This article belongs to the Special Issue Lizards As Reptilian Models To Analyze Organ Regeneration in Amniotes)

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Review

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21 pages, 7056 KiB

Open AccessFeature PaperReview

At What Cost? Trade-Offs and Influences on Energetic Investment in Tail Regeneration in Lizards Following Autotomy

by James I. Barr, Catherine A. Boisvert and Philip W. Bateman

J. Dev. Biol. 2021, 9(4), 53; https://0-doi-org.brum.beds.ac.uk/10.3390/jdb9040053 - 25 Nov 2021

Cited by 6 | Viewed by 4136

Abstract

Caudal autotomy, the ability to shed a portion of the tail, is a widespread defence strategy among lizards. Following caudal autotomy, and during regeneration, lizards face both short- and long-term costs associated with the physical loss of the tail and the energy required [...] Read more.

Caudal autotomy, the ability to shed a portion of the tail, is a widespread defence strategy among lizards. Following caudal autotomy, and during regeneration, lizards face both short- and long-term costs associated with the physical loss of the tail and the energy required for regeneration. As such, the speed at which the individual regenerates its tail (regeneration rate) should reflect the fitness priorities of the individual. However, multiple factors influence the regeneration rate in lizards, making inter-specific comparisons difficult and hindering broader scale investigations. We review regeneration rates for lizards and tuatara from the published literature, discuss how species’ fitness priorities and regeneration rates are influenced by specific, life history and environmental factors, and provide recommendations for future research. Regeneration rates varied extensively (0–4.3 mm/day) across the 56 species from 14 family groups. Species-specific factors, influencing regeneration rates, varied based on the type of fracture plane, age, sex, reproductive season, and longevity. Environmental factors including temperature, photoperiod, nutrition, and stress also affected regeneration rates, as did the method of autotomy induction, and the position of the tail also influenced regeneration rates for lizards. Additionally, regeneration could alter an individual’s behaviour, growth, and reproductive output, but this varied depending on the species. Full article

(This article belongs to the Special Issue Lizards As Reptilian Models To Analyze Organ Regeneration in Amniotes)

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8 pages, 234 KiB

Open AccessFeature PaperReview

Self-Control of Inflammation during Tail Regeneration of Lizards

by Bingqiang He, Honghua Song and Yongjun Wang

J. Dev. Biol. 2021, 9(4), 48; https://0-doi-org.brum.beds.ac.uk/10.3390/jdb9040048 - 02 Nov 2021

Cited by 7 | Viewed by 4339

Abstract

Lizards can spontaneously regenerate their lost tail without evoking excessive inflammation at the damaged site. In contrast, tissue/organ injury of its mammalian counterparts results in wound healing with a formation of a fibrotic scar due to uncontrolled activation of inflammatory responses. Unveiling the [...] Read more.

Lizards can spontaneously regenerate their lost tail without evoking excessive inflammation at the damaged site. In contrast, tissue/organ injury of its mammalian counterparts results in wound healing with a formation of a fibrotic scar due to uncontrolled activation of inflammatory responses. Unveiling the mechanism of self-limited inflammation occurring in the regeneration of a lizard tail will provide clues for a therapeutic alternative to tissue injury. The present review provides an overview of aspects of rapid wound healing and roles of antibacterial peptides, effects of leukocytes on the tail regeneration, self-blocking of the inflammatory activation in leukocytes, as well as inflammatory resistance of blastemal cells or immature somatic cells during lizard tail regeneration. These mechanistic insights of self-control of inflammation during lizard tail regeneration may lead in the future to the development of therapeutic strategies to fight injury-induced inflammation. Full article

(This article belongs to the Special Issue Lizards As Reptilian Models To Analyze Organ Regeneration in Amniotes)

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21 pages, 11019 KiB

Open AccessReview

Regeneration in Reptiles Generally and the New Zealand Tuatara in Particular as a Model to Analyse Organ Regrowth in Amniotes: A Review

by Lorenzo Alibardi and Victor Benno Meyer-Rochow

J. Dev. Biol. 2021, 9(3), 36; https://0-doi-org.brum.beds.ac.uk/10.3390/jdb9030036 - 30 Aug 2021

Cited by 7 | Viewed by 3662

Abstract

The ability to repair injuries among reptiles, i.e., ectothermic amniotes, is similar to that of mammals with some noteworthy exceptions. While large wounds in turtles and crocodilians are repaired through scarring, the reparative capacity involving the tail derives from a combined process of [...] Read more.

The ability to repair injuries among reptiles, i.e., ectothermic amniotes, is similar to that of mammals with some noteworthy exceptions. While large wounds in turtles and crocodilians are repaired through scarring, the reparative capacity involving the tail derives from a combined process of wound healing and somatic growth, the latter being continuous in reptiles. When the tail is injured in juvenile crocodilians, turtles and tortoises as well as the tuatara (Rhynchocephalia: Sphenodon punctatus, Gray 1842), the wound is repaired in these reptiles and some muscle and connective tissue and large amounts of cartilage are regenerated during normal growth. This process, here indicated as “regengrow”, can take years to produce tails with similar lengths of the originals and results in only apparently regenerated replacements. These new tails contain a cartilaginous axis and very small (turtle and crocodilians) to substantial (e.g., in tuatara) muscle mass, while most of the tail is formed by an irregular dense connective tissue containing numerous fat cells and sparse nerves. Tail regengrow in the tuatara is a long process that initially resembles that of lizards (the latter being part of the sister group Squamata within the Lepidosauria) with the formation of an axial ependymal tube isolated within a cartilaginous cylinder and surrounded by an irregular fat-rich connective tissue, some muscle bundles, and neogenic scales. Cell proliferation is active in the apical regenerative blastema, but much reduced cell proliferation continues in older regenerated tails, where it occurs mostly in the axial cartilage and scale epidermis of the new tail, but less commonly in the regenerated spinal cord, muscles, and connective tissues. The higher tissue regeneration of Sphenodon and other lepidosaurians provides useful information for attempts to improve organ regeneration in endothermic amniotes. Full article

(This article belongs to the Special Issue Lizards As Reptilian Models To Analyze Organ Regeneration in Amniotes)

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