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J. Dev. Biol., Volume 11, Issue 1 (March 2023) – 14 articles

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18 pages, 6588 KiB  
Review
Principles of Zebrafish Nephron Segment Development
by Thanh Khoa Nguyen, Madeline Petrikas, Brooke E. Chambers and Rebecca A. Wingert
J. Dev. Biol. 2023, 11(1), 14; https://doi.org/10.3390/jdb11010014 - 18 Mar 2023
Cited by 7 | Viewed by 2741
Abstract
Nephrons are the functional units which comprise the kidney. Each nephron contains a number of physiologically unique populations of specialized epithelial cells that are organized into discrete domains known as segments. The principles of nephron segment development have been the subject of many [...] Read more.
Nephrons are the functional units which comprise the kidney. Each nephron contains a number of physiologically unique populations of specialized epithelial cells that are organized into discrete domains known as segments. The principles of nephron segment development have been the subject of many studies in recent years. Understanding the mechanisms of nephrogenesis has enormous potential to expand our knowledge about the basis of congenital anomalies of the kidney and urinary tract (CAKUT), and to contribute to ongoing regenerative medicine efforts aimed at identifying renal repair mechanisms and generating replacement kidney tissue. The study of the zebrafish embryonic kidney, or pronephros, provides many opportunities to identify the genes and signaling pathways that control nephron segment development. Here, we describe recent advances of nephron segment patterning and differentiation in the zebrafish, with a focus on distal segment formation. Full article
(This article belongs to the Special Issue Zebrafish—a Model System for Developmental Biology II)
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14 pages, 2889 KiB  
Article
COMMD10 Is Essential for Neural Plate Development during Embryogenesis
by Khanh P. Phan, Panayiotis Pelargos, Alla V. Tsytsykova, Erdyni N. Tsitsikov, Graham Wiley, Chuang Li, Melissa Bebak and Ian F. Dunn
J. Dev. Biol. 2023, 11(1), 13; https://doi.org/10.3390/jdb11010013 - 16 Mar 2023
Viewed by 1802
Abstract
The COMMD (copper metabolism MURR1 domain containing) family includes ten structurally conserved proteins (COMMD1 to COMMD10) in eukaryotic multicellular organisms that are involved in a diverse array of cellular and physiological processes, including endosomal trafficking, copper homeostasis, and cholesterol metabolism, among others. To [...] Read more.
The COMMD (copper metabolism MURR1 domain containing) family includes ten structurally conserved proteins (COMMD1 to COMMD10) in eukaryotic multicellular organisms that are involved in a diverse array of cellular and physiological processes, including endosomal trafficking, copper homeostasis, and cholesterol metabolism, among others. To understand the role of COMMD10 in embryonic development, we used Commd10Tg(Vav1-icre)A2Kio/J mice, where the Vav1-cre transgene is integrated into an intron of the Commd10 gene, creating a functional knockout of Commd10 in homozygous mice. Breeding heterozygous mice produced no COMMD10-deficient (Commd10Null) offspring, suggesting that COMMD10 is required for embryogenesis. Analysis of Commd10Null embryos demonstrated that they displayed stalled development by embryonic day 8.5 (E8.5). Transcriptome analysis revealed that numerous neural crest-specific gene markers had lower expression in mutant versus wild-type (WT) embryos. Specifically, Commd10Null embryos displayed significantly lower expression levels of a number of transcription factors, including a major regulator of the neural crest, Sox10. Moreover, several cytokines/growth factors involved in early embryonic neurogenesis were also lower in mutant embryos. On the other hand, Commd10Null embryos demonstrated higher expression of genes involved in tissue remodeling and regression processes. Taken together, our findings show that Commd10Null embryos die by day E8.5 due to COMMD10-dependent neural crest failure, revealing a new and critical role for COMMD10 in neural development. Full article
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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 1935
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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3 pages, 174 KiB  
Editorial
Scientific Papers by Developmental Biologists in Japan
by Hideyo Ohuchi and Tsutomu Nohno
J. Dev. Biol. 2023, 11(1), 11; https://doi.org/10.3390/jdb11010011 - 10 Mar 2023
Viewed by 1118
Abstract
We have assembled ten interesting manuscripts submitted by developmental biologists in Japan [...] Full article
(This article belongs to the Special Issue Scientific Papers by Developmental Biologists in Japan)
16 pages, 2398 KiB  
Article
In Vitro Comparison of Sex-Specific Splicing Efficiencies of fem Pre-mRNA under Monoallelic and Heteroallelic Conditions of csd, a Master Sex-Determining Gene in the Honeybee
by Yukihiro Suzuki, Takafumi Yamada and Masataka G. Suzuki
J. Dev. Biol. 2023, 11(1), 10; https://doi.org/10.3390/jdb11010010 - 10 Mar 2023
Cited by 1 | Viewed by 1626
Abstract
The sexual fate of honeybees is determined by the complementary sex determination (CSD) model: heterozygosity at a single locus (the CSD locus) determines femaleness, while hemizygosity or homozygosity at the CSD locus determines maleness. The csd gene encodes a splicing factor that regulates [...] Read more.
The sexual fate of honeybees is determined by the complementary sex determination (CSD) model: heterozygosity at a single locus (the CSD locus) determines femaleness, while hemizygosity or homozygosity at the CSD locus determines maleness. The csd gene encodes a splicing factor that regulates sex-specific splicing of the downstream target gene feminizer (fem), which is required for femaleness. The female mode of fem splicing occurs only when csd is present in the heteroallelic condition. To gain insights into how Csd proteins are only activated under the heterozygous allelic composition, we developed an in vitro assay system to evaluate the activity of Csd proteins. Consistent with the CSD model, the co-expression of two csd alleles, both of which lack splicing activity under the single-allele condition, restored the splicing activity that governs the female mode of fem splicing. RNA immunoprecipitation quantitative PCR analyses demonstrated that the CSD protein was specifically enriched in several exonic regions in the fem pre-mRNA, and enrichment in exons 3a and 5 was significantly greater under the heterozygous allelic composition than the single-allelic condition. However, in most cases csd expression under the monoallelic condition was capable of inducing the female mode of fem splicing contrary to the conventional CSD model. In contrast, repression of the male mode of fem splicing was predominant under heteroallelic conditions. These results were reproduced by real-time PCR of endogenous fem expression in female and male pupae. These findings strongly suggest that the heteroallelic composition of csd may be more important for the repression of the male splicing mode than for the induction of the female splicing mode of the fem gene. Full article
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26 pages, 3394 KiB  
Review
Modeling Podocyte Ontogeny and Podocytopathies with the Zebrafish
by Bridgette E. Drummond, Wesley S. Ercanbrack and Rebecca A. Wingert
J. Dev. Biol. 2023, 11(1), 9; https://doi.org/10.3390/jdb11010009 - 20 Feb 2023
Cited by 5 | Viewed by 4009
Abstract
Podocytes are exquisitely fashioned kidney cells that serve an essential role in the process of blood filtration. Congenital malformation or damage to podocytes has dire consequences and initiates a cascade of pathological changes leading to renal disease states known as podocytopathies. In addition, [...] Read more.
Podocytes are exquisitely fashioned kidney cells that serve an essential role in the process of blood filtration. Congenital malformation or damage to podocytes has dire consequences and initiates a cascade of pathological changes leading to renal disease states known as podocytopathies. In addition, animal models have been integral to discovering the molecular pathways that direct the development of podocytes. In this review, we explore how researchers have used the zebrafish to illuminate new insights about the processes of podocyte ontogeny, model podocytopathies, and create opportunities to discover future therapies. Full article
(This article belongs to the Special Issue 2022 Feature Papers by JDB’s Editorial Board Members)
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16 pages, 6428 KiB  
Article
Neurogenin 2 and Neuronal Differentiation 1 Control Proper Development of the Chick Trigeminal Ganglion and Its Nerve Branches
by Parinaz Bina, Margaret A. Hines, Johena Sanyal and Lisa A. Taneyhill
J. Dev. Biol. 2023, 11(1), 8; https://doi.org/10.3390/jdb11010008 - 19 Feb 2023
Viewed by 1892
Abstract
The trigeminal ganglion contains the cell bodies of sensory neurons comprising cranial nerve V, which relays information related to pain, touch, and temperature from the face and head to the brain. Like other cranial ganglia, the trigeminal ganglion is composed of neuronal derivatives [...] Read more.
The trigeminal ganglion contains the cell bodies of sensory neurons comprising cranial nerve V, which relays information related to pain, touch, and temperature from the face and head to the brain. Like other cranial ganglia, the trigeminal ganglion is composed of neuronal derivatives of two critical embryonic cell types, neural crest and placode cells. Neurogenesis within the cranial ganglia is promoted by Neurogenin 2 (Neurog2), which is expressed in trigeminal placode cells and their neuronal derivatives, and transcriptionally activates neuronal differentiation genes such as Neuronal Differentiation 1 (NeuroD1). Little is known, however, about the role of Neurog2 and NeuroD1 during chick trigeminal gangliogenesis. To address this, we depleted Neurog2 and NeuroD1 from trigeminal placode cells with morpholinos and demonstrated that Neurog2 and NeuroD1 influence trigeminal ganglion development. While knockdown of both Neurog2 and NeuroD1 affected innervation of the eye, Neurog2 and NeuroD1 had opposite effects on ophthalmic nerve branch organization. Taken together, our results highlight, for the first time, functional roles for Neurog2 and NeuroD1 during chick trigeminal gangliogenesis. These studies shed new light on the molecular mechanisms underlying trigeminal ganglion formation and may also provide insight into general cranial gangliogenesis and diseases of the peripheral nervous system. Full article
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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 1647
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)
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 6 | Viewed by 4104
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 3 | Viewed by 2513
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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2 pages, 278 KiB  
Editorial
Acknowledgment to the Reviewers of Journal of Developmental Biology in 2022
by JDB Editorial Office
J. Dev. Biol. 2023, 11(1), 4; https://doi.org/10.3390/jdb11010004 - 17 Jan 2023
Viewed by 1001
Abstract
High-quality academic publishing is built on rigorous peer review [...] Full article
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 3 | Viewed by 1619
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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15 pages, 2913 KiB  
Article
Roles for the RNA-Binding Protein Caper in Reproductive Output in Drosophila melanogaster
by Erika J. Tixtha, Meg K. Super, M. Brandon Titus, Jeremy M. Bono and Eugenia C. Olesnicky
J. Dev. Biol. 2023, 11(1), 2; https://doi.org/10.3390/jdb11010002 - 23 Dec 2022
Viewed by 2185
Abstract
RNA binding proteins (RBPs) play a fundamental role in the post-transcriptional regulation of gene expression within the germline and nervous system. This is underscored by the prevalence of mutations within RBP-encoding genes being implicated in infertility and neurological disease. We previously described roles [...] Read more.
RNA binding proteins (RBPs) play a fundamental role in the post-transcriptional regulation of gene expression within the germline and nervous system. This is underscored by the prevalence of mutations within RBP-encoding genes being implicated in infertility and neurological disease. We previously described roles for the highly conserved RBP Caper in neurite morphogenesis in the Drosophila larval peripheral system and in locomotor behavior. However, caper function has not been investigated outside the nervous system, although it is widely expressed in many different tissue types during embryogenesis. Here, we describe novel roles for Caper in fertility and mating behavior. We find that Caper is expressed in ovarian follicles throughout oogenesis but is dispensable for proper patterning of the egg chamber. Additionally, reduced caper function, through either a genetic lesion or RNA interference-mediated knockdown of caper in the female germline, results in females laying significantly fewer eggs than their control counterparts. Moreover, this phenotype is exacerbated with age. caper dysfunction also results in partial embryonic and larval lethality. Given that caper is highly conserved across metazoa, these findings may also be relevant to vertebrates. Full article
(This article belongs to the Special Issue Feature Papers in Journal of Developmental Biology II)
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17 pages, 1665 KiB  
Review
Advances in Understanding the Genetic Mechanisms of Zebrafish Renal Multiciliated Cell Development
by Hannah M. Wesselman, Thanh Khoa Nguyen, Joseph M. Chambers, Bridgette E. Drummond and Rebecca A. Wingert
J. Dev. Biol. 2023, 11(1), 1; https://doi.org/10.3390/jdb11010001 - 21 Dec 2022
Cited by 7 | Viewed by 2770
Abstract
Cilia are microtubule-based organelles that project from the cell surface. In humans and other vertebrates, possession of a single cilium structure enables an assortment of cellular processes ranging from mechanosensation to fluid propulsion and locomotion. Interestingly, cells can possess a single cilium or [...] Read more.
Cilia are microtubule-based organelles that project from the cell surface. In humans and other vertebrates, possession of a single cilium structure enables an assortment of cellular processes ranging from mechanosensation to fluid propulsion and locomotion. Interestingly, cells can possess a single cilium or many more, where so-called multiciliated cells (MCCs) possess apical membrane complexes with several dozen or even hundreds of motile cilia that beat in a coordinated fashion. Development of MCCs is, therefore, integral to control fluid flow and/or cellular movement in various physiological processes. As such, MCC dysfunction is associated with numerous pathological states. Understanding MCC ontogeny can be used to address congenital birth defects as well as acquired disease conditions. Today, researchers used both in vitro and in vivo experimental models to address our knowledge gaps about MCC specification and differentiation. In this review, we summarize recent discoveries from our lab and others that have illuminated new insights regarding the genetic pathways that direct MCC ontogeny in the embryonic kidney using the power of the zebrafish animal model. Full article
(This article belongs to the Special Issue Cilia in Development)
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