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Development of the Skin in Vertebrates
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Development of the Skin in Vertebrates

A special issue of Journal of Developmental Biology (ISSN 2221-3759).

Deadline for manuscript submissions: closed (30 July 2023) | Viewed by 34522

Special Issue Editor

Prof. Dr. Lorenzo Alibardi

E-Mail Website
Guest Editor
Comparative Histolab and Department of Biology, University of Bologna, Via Selmi 3, 40126 Bologna, Italy
Interests: skin development in all vertebrates, especially reptiles AND nervous; organ regeneration in vertebrates, especially reptiles and amphibians
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

The integument of vertebrates is a complex and large organ positioned at the interface with the environment, be that aquatic or terrestrial. Specific characteristics have evolved from piscine to land vertebrates in the epidermis and dermis. During development, a series of successive transformations of the epidermis and dermis have occurred in different vertebrates, in particular, during the transition from water to land. In fish, and most amphibians, keratinization is the prevalent form of the terminal differentiation of keratinocytes, whereas a variable process of cornification takes place in amniotes; this varies in intensity in different integument appendages, such as scales, feathers, hair, claws, horns, etc. Additionally, specific receptors are differentiated in the skin of anamniotes (fish and amphibians) and amniotes (sauropsids and mammals). In the dermis and hypodermis of different vertebrates, a variable collection of fibroblasts, chromatophores, immune cells and other cell types accumulate, allowing for specific functions.

The Journal of Developmental Biology invites researchers working in the field of the developmental biology of the skin of anamniotes and amniotes to contribute articles in order to form an updated collection of information that describes the development and transformation of the integument of vertebrates in relation to their environment and lifestyle. This Special Issue, after some historical and general considerations on the “comparative dermatology of vertebrates”, introduces papers illustrating the development and general structure of the skin of fish, amphibians, and various amniotes.

Dr. Lorenzo Alibardi
Guest Editor

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Journal of Developmental Biology is an international peer-reviewed open access quarterly journal published by MDPI.

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Keywords

  • vertebrates
  • skin
  • development
  • evolution
  • land adaptation

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Related Special Issue

Published Papers (11 papers)

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Editorial

Jump to: Research, Review

2 pages, 166 KiB  
Editorial
Introduction to the Development of Skin in Vertebrates
by Lorenzo Alibardi
J. Dev. Biol. 2023, 11(1), 7; https://doi.org/10.3390/jdb11010007 - 31 Jan 2023
Viewed by 2401
Abstract
The integument of vertebrates is a complex and large organ positioned at the interface with the aquatic or terrestrial environment, and is derived from the embryonic ectoderm (epidermis) and mesoderm (dermis and hypodermis) [...] Full article
(This article belongs to the Special Issue Development of the Skin in Vertebrates)

Research

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11 pages, 4213 KiB  
Article
Impact of Stem Cells on Reparative Regeneration in Abdominal and Dorsal Skin in the Rat
by Evgeniya Kananykhina, Andrey Elchaninov and Galina Bolshakova
J. Dev. Biol. 2024, 12(1), 6; https://doi.org/10.3390/jdb12010006 - 27 Jan 2024
Viewed by 2040
Abstract
A characteristic feature of repair processes in mammals is the formation of scar tissue at the site of injury, which is designed to quickly prevent contact between the internal environment of the organism and the external environment. Despite this general pattern, different organs [...] Read more.
A characteristic feature of repair processes in mammals is the formation of scar tissue at the site of injury, which is designed to quickly prevent contact between the internal environment of the organism and the external environment. Despite this general pattern, different organs differ in the degree of severity of scar changes in response to injury. One of the areas in which regeneration after wounding leads to the formation of a structure close to the original one is the abdominal skin of laboratory rats. Finding out the reasons for such a phenomenon is essential for the development of ways to stimulate full regeneration. The model of skin wound healing in the abdominal region of laboratory animals was reproduced in this work. It was found that the wound surface is completely epithelialized on the abdomen by 20 days, while on the back—by 30 days. The qPCR method revealed higher expression of marker genes of skin stem cells (Sox9, Lgr6, Gli1, Lrig1) in the intact skin of the abdomen compared to the back, which corresponded to a greater number of hairs with which stem cells are associated on the abdomen compared to the back. Considering that some stem cell populations are associated with hair, it can be suggested that one of the factors in faster regeneration of abdominal skin in the rat is the greater number of stem cells in this area. Full article
(This article belongs to the Special Issue Development of the Skin in Vertebrates)
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15 pages, 3860 KiB  
Article
Immunolocalization of Some Epidermal Proteins and Glycoproteins in the Growing Skin of the Australian Lungfish (Neoceratodus forsteri)
by Lorenzo Alibardi
J. Dev. Biol. 2023, 11(3), 35; https://doi.org/10.3390/jdb11030035 - 14 Aug 2023
Viewed by 1681
Abstract
Here we report the immunolocalization of mucin, nestin, elastin and three glycoproteins involved in tissue mineralization in small and large juveniles of Neoceratodus forsteri. Both small and larger juvenile epidermis are mucogenic and contain a diffuse immunolabeling for nestin. Sparse PCNA-labeled cells, [...] Read more.
Here we report the immunolocalization of mucin, nestin, elastin and three glycoproteins involved in tissue mineralization in small and large juveniles of Neoceratodus forsteri. Both small and larger juvenile epidermis are mucogenic and contain a diffuse immunolabeling for nestin. Sparse PCNA-labeled cells, indicating proliferation, are found in basal and suprabasal epidermal layers. No scales are formed in small juveniles but are present in a 5 cm long juvenile and in larger juveniles. Elastin and a mineralizing matrix are localized underneath the basement membrane of the tail epidermis where lepidotriches are forming. The latter appears as “circular bodies” in cross sections and are made of elongated cells surrounding a central amorphous area containing collagen and elastin-like proteins that undergo calcification as evidenced using the von Kossa staining. However, the first calcification sites are the coniform teeth of the small juveniles of 2–3 cm in length. In the superficial dermis of juveniles (16–26 cm in length) where scales are formed, the spinulated outer bony layer (squamulin) of the elasmoid scales contains osteonectin, alkaline phosphatase, osteopontin, and calcium deposits that are instead absent in the underlying layer of elasmodin. In particular, these glycoproteins are localized along the scale margin in juveniles where scales grow, as indicated by the presence of PCNA-labeled cells (proliferating). These observations suggest a continuous deposition of new bone during the growth of the scales, possibly under the action of these mineralizing glycoproteins, like in the endoskeleton of terrestrial vertebrates. Full article
(This article belongs to the Special Issue Development of the Skin in Vertebrates)
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14 pages, 4103 KiB  
Article
Molecular and Cellular Characterization of Avian Reticulate Scales Implies the Evo–Devo Novelty of Skin Appendages in Foot Sole
by Tzu-Yu Liu, Michael W. Hughes, Hao-Ven Wang, Wei-Cheng Yang, Cheng-Ming Chuong and Ping Wu
J. Dev. Biol. 2023, 11(3), 30; https://doi.org/10.3390/jdb11030030 - 3 Jul 2023
Cited by 2 | Viewed by 2322
Abstract
Among amniotic skin appendages, avian feathers and mammalian hairs protect their stem cells in specialized niches, located in the collar bulge and hair bulge, respectively. In chickens and alligators, label retaining cells (LRCs), which are putative stem cells, are distributed in the hinge [...] Read more.
Among amniotic skin appendages, avian feathers and mammalian hairs protect their stem cells in specialized niches, located in the collar bulge and hair bulge, respectively. In chickens and alligators, label retaining cells (LRCs), which are putative stem cells, are distributed in the hinge regions of both avian scutate scales and reptilian overlapping scales. These LRCs take part in scale regeneration. However, it is unknown whether other types of scales, for example, symmetrically shaped reticulate scales, have a similar way of preserving their stem cells. In particular, the foot sole represents a special interface between animal feet and external environments, with heavy mechanical loading. This is different from scutate-scale-covered metatarsal feet that function as protection. Avian reticulate scales on foot soles display specialized characteristics in development. They do not have a placode stage and lack β-keratin expression. Here, we explore the molecular and cellular characteristics of avian reticulate scales. RNAscope analysis reveals different molecular profiles during surface and hinge determination compared with scutate scales. Furthermore, reticulate scales express Keratin 15 (K15) sporadically in both surface- and hinge-region basal layer cells, and LRCs are not localized. Upon wounding, the reticulate scale region undergoes repair but does not regenerate. Our results suggest that successful skin appendage regeneration requires localized stem cell niches to guide regeneration. Full article
(This article belongs to the Special Issue Development of the Skin in Vertebrates)
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15 pages, 8158 KiB  
Article
Osteoderm Development during the Regeneration Process in Eurylepis taeniolata Blyth, 1854 (Scincidae, Sauria, Squamata)
by Gennady O. Cherepanov, Dmitry A. Gordeev, Daniel A. Melnikov and Natalia B. Ananjeva
J. Dev. Biol. 2023, 11(2), 22; https://doi.org/10.3390/jdb11020022 - 24 May 2023
Cited by 4 | Viewed by 2216
Abstract
Osteoderms are bony structures that develop within the dermal layer of the skin in vertebrates and are very often found in different lizard families. Lizard osteoderms are diverse in topography, morphology, and microstructure. Of particular interest are the compound osteoderms of skinks, which [...] Read more.
Osteoderms are bony structures that develop within the dermal layer of the skin in vertebrates and are very often found in different lizard families. Lizard osteoderms are diverse in topography, morphology, and microstructure. Of particular interest are the compound osteoderms of skinks, which are a complex of several bone elements known as osteodermites. We present new data on the development and regeneration of compound osteoderms based on the results of a histological and Computed Microtomography (micro-CT) study of a scincid lizard: Eurylepis taeniolata. The specimens studied are stored in the herpetological collections of the Saint-Petersburg State University and Zoological Institute of the Russian Academy of Sciences located in St. Petersburg, Russia. The topography of osteoderms in the integuments of the original tail area and its regenerated part was studied. A comparative histological description of the original and regenerated osteoderms of Eurylepis taeniolata is presented for the first time. The first description of the development of compound osteoderm microstructure in the process of caudal regeneration is also presented. Full article
(This article belongs to the Special Issue Development of the Skin in Vertebrates)
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13 pages, 4230 KiB  
Article
Heme Oxygenase-1 Is Upregulated during Differentiation of Keratinocytes but Its Expression Is Dispensable for Cornification of Murine Epidermis
by Marta Surbek, Supawadee Sukseree, Attila Placido Sachslehner, Dragan Copic, Bahar Golabi, Ionela Mariana Nagelreiter, Erwin Tschachler and Leopold Eckhart
J. Dev. Biol. 2023, 11(1), 12; https://doi.org/10.3390/jdb11010012 - 10 Mar 2023
Cited by 3 | Viewed by 2684
Abstract
The epidermal barrier of mammals is initially formed during embryonic development and continuously regenerated by the differentiation and cornification of keratinocytes in postnatal life. Cornification is associated with the breakdown of organelles and other cell components by mechanisms which are only incompletely understood. [...] Read more.
The epidermal barrier of mammals is initially formed during embryonic development and continuously regenerated by the differentiation and cornification of keratinocytes in postnatal life. Cornification is associated with the breakdown of organelles and other cell components by mechanisms which are only incompletely understood. Here, we investigated whether heme oxygenase 1 (HO-1), which converts heme into biliverdin, ferrous iron and carbon monoxide, is required for normal cornification of epidermal keratinocytes. We show that HO-1 is transcriptionally upregulated during the terminal differentiation of human keratinocytes in vitro and in vivo. Immunohistochemistry demonstrated expression of HO-1 in the granular layer of the epidermis where keratinocytes undergo cornification. Next, we deleted the Hmox1 gene, which encodes HO-1, by crossing Hmox1-floxed and K14-Cre mice. The epidermis and isolated keratinocytes of the resulting Hmox1f/f K14-Cre mice lacked HO-1 expression. The genetic inactivation of HO-1 did not impair the expression of keratinocyte differentiation markers, loricrin and filaggrin. Likewise, the transglutaminase activity and formation of the stratum corneum were not altered in Hmox1f/f K14-Cre mice, suggesting that HO-1 is dispensable for epidermal cornification. The genetically modified mice generated in this study may be useful for future investigations of the potential roles of epidermal HO-1 in iron metabolism and responses to oxidative stress. Full article
(This article belongs to the Special Issue Development of the Skin in Vertebrates)
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Review

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11 pages, 1410 KiB  
Review
Epidermal Barrier Development via Corneoptosis: A Unique Form of Cell Death in Stratum Granulosum Cells
by Takeshi Matsui
J. Dev. Biol. 2023, 11(4), 43; https://doi.org/10.3390/jdb11040043 - 30 Nov 2023
Cited by 10 | Viewed by 2898
Abstract
Epidermal development is responsible for the formation of the outermost layer of the skin, the epidermis. The establishment of the epidermal barrier is a critical aspect of mammalian development. Proper formation of the epidermis, which is composed of stratified squamous epithelial cells, is [...] Read more.
Epidermal development is responsible for the formation of the outermost layer of the skin, the epidermis. The establishment of the epidermal barrier is a critical aspect of mammalian development. Proper formation of the epidermis, which is composed of stratified squamous epithelial cells, is essential for the survival of terrestrial vertebrates because it acts as a crucial protective barrier against external threats such as pathogens, toxins, and physical trauma. In mammals, epidermal development begins from the embryonic surface ectoderm, which gives rise to the basal layer of the epidermis. This layer undergoes a series of complex processes that lead to the formation of subsequent layers, including the stratum intermedium, stratum spinosum, stratum granulosum, and stratum corneum. The stratum corneum, which is the topmost layer of the epidermis, is formed by corneoptosis, a specialized form of cell death. This process involves the transformation of epidermal keratinocytes in the granular layer into flattened dead cells, which constitute the protective barrier. In this review, we focus on the intricate mechanisms that drive the development and establishment of the mammalian epidermis to gain insight into the complex processes that govern this vital biological system. Full article
(This article belongs to the Special Issue Development of the Skin in Vertebrates)
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23 pages, 3748 KiB  
Review
Evo Devo of the Vertebrates Integument
by Danielle Dhouailly
J. Dev. Biol. 2023, 11(2), 25; https://doi.org/10.3390/jdb11020025 - 5 Jun 2023
Cited by 11 | Viewed by 3982
Abstract
All living jawed vertebrates possess teeth or did so ancestrally. Integumental surface also includes the cornea. Conversely, no other anatomical feature differentiates the clades so readily as skin appendages do, multicellular glands in amphibians, hair follicle/gland complexes in mammals, feathers in birds, and [...] Read more.
All living jawed vertebrates possess teeth or did so ancestrally. Integumental surface also includes the cornea. Conversely, no other anatomical feature differentiates the clades so readily as skin appendages do, multicellular glands in amphibians, hair follicle/gland complexes in mammals, feathers in birds, and the different types of scales. Tooth-like scales are characteristic of chondrichthyans, while mineralized dermal scales are characteristic of bony fishes. Corneous epidermal scales might have appeared twice, in squamates, and on feet in avian lineages, but posteriorly to feathers. In contrast to the other skin appendages, the origin of multicellular glands of amphibians has never been addressed. In the seventies, pioneering dermal–epidermal recombination between chick, mouse and lizard embryos showed that: (1) the clade type of the appendage is determined by the epidermis; (2) their morphogenesis requires two groups of dermal messages, first for primordia formation, second for appendage final architecture; (3) the early messages were conserved during amniotes evolution. Molecular biology studies that have identified the involved pathways, extending those data to teeth and dermal scales, suggest that the different vertebrate skin appendages evolved in parallel from a shared placode/dermal cells unit, present in a common toothed ancestor, c.a. 420 mya. Full article
(This article belongs to the Special Issue Development of the Skin in Vertebrates)
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15 pages, 3629 KiB  
Review
The Complex Bridge between Aquatic and Terrestrial Life: Skin Changes during Development of Amphibians
by Esra Akat Çömden, Melodi Yenmiş and Berna Çakır
J. Dev. Biol. 2023, 11(1), 6; https://doi.org/10.3390/jdb11010006 - 30 Jan 2023
Cited by 17 | Viewed by 6723
Abstract
Amphibian skin is a particularly complex organ that is primarily responsible for respiration, osmoregulation, thermoregulation, defense, water absorption, and communication. The skin, as well as many other organs in the amphibian body, has undergone the most extensive rearrangement in the adaptation from water [...] Read more.
Amphibian skin is a particularly complex organ that is primarily responsible for respiration, osmoregulation, thermoregulation, defense, water absorption, and communication. The skin, as well as many other organs in the amphibian body, has undergone the most extensive rearrangement in the adaptation from water to land. Structural and physiological features of skin in amphibians are presented within this review. We aim to procure extensive and updated information on the evolutionary history of amphibians and their transition from water to land—that is, the changes seen in their skin from the larval stages to adulthood from the points of morphology, physiology, and immunology. Full article
(This article belongs to the Special Issue Development of the Skin in Vertebrates)
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12 pages, 1690 KiB  
Review
The Story of the Finest Armor: Developmental Aspects of Reptile Skin
by Melodi Yenmiş and Dinçer Ayaz
J. Dev. Biol. 2023, 11(1), 5; https://doi.org/10.3390/jdb11010005 - 28 Jan 2023
Cited by 6 | Viewed by 3686
Abstract
The reptile skin is a barrier against water loss and pathogens and an armor for mechanical damages. The integument of reptiles consists of two main layers: the epidermis and the dermis. The epidermis, the hard cover of the body which has an armor-like [...] Read more.
The reptile skin is a barrier against water loss and pathogens and an armor for mechanical damages. The integument of reptiles consists of two main layers: the epidermis and the dermis. The epidermis, the hard cover of the body which has an armor-like role, varies among extant reptiles in terms of structural aspects such as thickness, hardness or the kinds of appendages it constitutes. The reptile epithelial cells of the epidermis (keratinocytes) are composed of two main proteins: intermediate filament keratins (IFKs) and corneous beta proteins (CBPs). The outer horny layer of the epidermis, stratum corneum, is constituted of keratinocytes by means of terminal differentiation or cornification which is a result of the protein interactions where CBPs associate with and coat the initial scaffold of IFKs. Reptiles were able to colonize the terrestrial environment due to the changes in these epidermal structures, which led to various cornified epidermal appendages such as scales and scutes, a beak, claws or setae. Developmental and structural aspects of the epidermal CBPs as well as their shared chromosomal locus (EDC) indicate an ancestral origin that gave rise to the finest armor of reptilians. Full article
(This article belongs to the Special Issue Development of the Skin in Vertebrates)
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18 pages, 27753 KiB  
Review
The Periodic Replacement of Adhesive Setae in Pad Lamellae of Climbing Lizards Is Driven by Patterns of Corneous Layer Growth
by Lorenzo Alibardi
J. Dev. Biol. 2023, 11(1), 3; https://doi.org/10.3390/jdb11010003 - 30 Dec 2022
Cited by 5 | Viewed by 2379
Abstract
The adhesive digital pads in some gecko and anoline lizards are continuously utilized for movements on vertical surfaces that may determine wear and a decrease of adhesion efficiency. The pads are formed by lamellae bearing adhesive setae that are worn out following frequent [...] Read more.
The adhesive digital pads in some gecko and anoline lizards are continuously utilized for movements on vertical surfaces that may determine wear and a decrease of adhesion efficiency. The pads are formed by lamellae bearing adhesive setae that are worn out following frequent usage and are replaced by new inner setae that maintain an efficient adhesion. Whether the extensive usage of adhesive setae determines a higher shedding frequency in the digital pads with respect to other body regions remains unknown. Setae replacement has been analyzed in embryos and adult lizards using autoradiography and 5BrdU-immunohistochemistry. The observation strongly suggests that during development and epidermal renewal in adult lamellae, there is a shifting of the outer setae toward the apex of the lamella. This movement is likely derived from the continuous addition of proteins in the beta- and alpha-layers sustaining the outer setae while the inner setae are forming. Ultrastructural and in situ hybridization studies indicate that the thin outer beta- and alpha-layers still contain mRNAs and ribosomes that may contribute to the continuous production of corneous beta proteins (CBPs) and keratins for the growth of the free margin at the apex of the lamella. This process determines the apical shifting and release of the old setae, while the new inner setae formed underneath becomes the new outer setae. Full article
(This article belongs to the Special Issue Development of the Skin in Vertebrates)
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