Zebrafish—a Model System for Developmental Biology II

Special Issue Editor

1. Center for Developmental Biology and Regenerative Medicine, Seattle Children’s Research Institute, 1900 9th Avenue, Seattle, WA 98101, USA
2. Division of Cardiology, Department of Pediatrics, University of Washington, Seattle, WA 98105, USA
Interests: zebrafish developmental biology and genetics; skeletal muscle development and disease; heart development; homeodomain transcription factors
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Special Issue Information

Dear Colleagues,

Following a very successful first run, we are pleased to announce the launch of a second edition of the Special Issue on Zebrafish—A Model System for Developmental Biology II.

The birth of zebrafish (Danio rerio) research is, for many of us, linked to the historic publication of George Streisinger and colleagues (Nature 1981;291:293–296). This work detailed the development of zebrafish genetic procedures and clonal lines. It was followed by a series of seminal papers on zebrafish developmental staging and cell lineage studies by Charles Kimmel and colleagues (for example, Dev Dyn 1995;203:253–310) and forward genetic screens for zebrafish mutants by the Nüsslein-Volhard, Driever, and Fishman labs (published in Development 1996;193:1–481). These studies established many of the standards for the use of zebrafish as a model organism for developmental genetics research. Zebrafish is used today in many diverse branches of research from basic to biomedical and applied research. In the field of developmental biology, zebrafish has been critical in identifying the components of many signalling pathways, the mechanisms behind gastrulation movements and neuronal migration, and the genetic and morphogenetic basis of the development of organs such as the heart, brain, liver, and skeleton. This Special Issue will focus on the latest advances in basic research made possible by the use of zebrafish. We invite contributions, reviews, or research papers that focus on this field of research.

Dr. Lisa Maves
Guest Editor

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Keywords

  • zebrafish
  • gastrulation
  • neurogenesis
  • ciliogenesis
  • skeletal development
  • chondrogenesis
  • heart development
  • angiogenesis
  • myogenesis

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Published Papers (7 papers)

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Research

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21 pages, 7620 KiB  
Article
Regionalized Protein Localization Domains in the Zebrafish Hair Cell Kinocilium
by Timothy Erickson, William Paul Biggers III, Kevin Williams, Shyanne E. Butland and Alexandra Venuto
J. Dev. Biol. 2023, 11(2), 28; https://doi.org/10.3390/jdb11020028 - 16 Jun 2023
Cited by 1 | Viewed by 2479
Abstract
Sensory hair cells are the receptors for auditory, vestibular, and lateral line sensory organs in vertebrates. These cells are distinguished by “hair”-like projections from their apical surface collectively known as the hair bundle. Along with the staircase arrangement of the actin-filled stereocilia, the [...] Read more.
Sensory hair cells are the receptors for auditory, vestibular, and lateral line sensory organs in vertebrates. These cells are distinguished by “hair”-like projections from their apical surface collectively known as the hair bundle. Along with the staircase arrangement of the actin-filled stereocilia, the hair bundle features a single, non-motile, true cilium called the kinocilium. The kinocilium plays an important role in bundle development and the mechanics of sensory detection. To understand more about kinocilial development and structure, we performed a transcriptomic analysis of zebrafish hair cells to identify cilia-associated genes that have yet to be characterized in hair cells. In this study, we focused on three such genes—ankef1a, odf3l2a, and saxo2—because human or mouse orthologs are either associated with sensorineural hearing loss or are located near uncharacterized deafness loci. We made transgenic fish that express fluorescently tagged versions of their proteins, demonstrating their localization to the kinocilia of zebrafish hair cells. Furthermore, we found that Ankef1a, Odf3l2a, and Saxo2 exhibit distinct localization patterns along the length of the kinocilium and within the cell body. Lastly, we have reported a novel overexpression phenotype of Saxo2. Overall, these results suggest that the hair cell kinocilium in zebrafish is regionalized along its proximal-distal axis and set the groundwork to understand more about the roles of these kinocilial proteins in hair cells. Full article
(This article belongs to the Special Issue Zebrafish—a Model System for Developmental Biology II)
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12 pages, 2538 KiB  
Communication
Comparison of Pronase versus Manual Dechorionation of Zebrafish Embryos for Small Molecule Treatments
by Eva H. Hasegawa, Gist H. Farr III and Lisa Maves
J. Dev. Biol. 2023, 11(2), 16; https://doi.org/10.3390/jdb11020016 - 28 Mar 2023
Cited by 3 | Viewed by 4152
Abstract
Zebrafish are a powerful animal model for small molecule screening. Small molecule treatments of zebrafish embryos usually require that the chorion, an acellular envelope enclosing the embryo, is removed in order for chemical compounds to access the embryo from the bath medium. For [...] Read more.
Zebrafish are a powerful animal model for small molecule screening. Small molecule treatments of zebrafish embryos usually require that the chorion, an acellular envelope enclosing the embryo, is removed in order for chemical compounds to access the embryo from the bath medium. For large-scale studies requiring hundreds of embryos, manual dechorionation, using forceps, can be a time-consuming and limiting process. Pronase is a non-specific protease that is widely used as an enzymatic alternative for dechorionating zebrafish embryos. However, whether pronase treatments alter the effects of subsequent small molecule treatments has not been addressed. Here, we provide a detailed protocol for large-scale pronase dechorionation of zebrafish embryos. We tested whether pronase treatment can influence the efficacy of drug treatments in zebrafish embryos. We used a zebrafish model for Duchenne muscular dystrophy (DMD) to investigate whether the efficacies of trichostatin-A (TSA) or salermide + oxamflatin, small molecule inhibitors known to ameliorate the zebrafish dmd muscle degeneration phenotype, are significantly altered when embryos are treated with pronase versus manual dechorionation. We also tested the effects of pronase on the ability of the anthracycline cancer drug doxorubicin to induce cardiotoxicity in zebrafish embryos. When comparing pronase- versus forceps-dechorionated embryos used in these small molecule treatments, we found no appreciable effects of pronase on animal survival or on the effects of the small molecules. The significant difference that was detected was a small improvement in the ability of salermide + oxamflatin to ameliorate the dmd phenotype in pronase-treated embryos when compared with manual dechorionation. Our study supports the use of pronase treatment as a dechorionation method for zebrafish drug screening experiments. Full article
(This article belongs to the Special Issue Zebrafish—a Model System for Developmental Biology II)
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19 pages, 10150 KiB  
Article
Zebrafish Model of Stickler Syndrome Suggests a Role for Col2a1a in the Neural Crest during Early Eye Development
by Antionette L. Williams and Brenda L. Bohnsack
J. Dev. Biol. 2022, 10(4), 42; https://doi.org/10.3390/jdb10040042 - 1 Oct 2022
Cited by 4 | Viewed by 2863
Abstract
Most cases of Stickler syndrome are due to autosomal-dominant COL2A1 gene mutations leading to abnormal type II collagen. Ocular findings include axial eye lengthening with vitreal degeneration and early-onset glaucoma, which can result in vision loss. Although COL2A1 is a major player in [...] Read more.
Most cases of Stickler syndrome are due to autosomal-dominant COL2A1 gene mutations leading to abnormal type II collagen. Ocular findings include axial eye lengthening with vitreal degeneration and early-onset glaucoma, which can result in vision loss. Although COL2A1 is a major player in cartilage and bone formation, its specific role in eye development remains elusive. We investigated the role of Col2a1a in neural crest migration and differentiation during early zebrafish eye development. In situ hybridization, immunofluorescence, live imaging, exogenous treatments [10 μM diethylaminobenzaldehyde (DEAB), 100 nM all-trans retinoic acid (RA) and 1–3% ethanol (ETOH)] and morpholino oligonucleotide (MO) injections were used to analyze wildtype Casper (roy−/−;nacre−/−), TgBAC(col2a1a::EGFP), Tg(sox10::EGFP) and Tg(foxd3::EGFP) embryos. Col2a1a colocalized with Foxd3- and Sox10-positive cells in the anterior segment and neural crest-derived jaw. Col2a1a expression was regulated by RA and inhibited by 3% ETOH. Furthermore, MO knockdown of Col2a1a delayed jaw formation and disrupted the ocular anterior segment neural crest migration of Sox10-positive cells. Interestingly, human COL2A1 protein rescued the MO effects. Altogether, these results suggest that Col2a1a is a downstream target of RA in the cranial neural crest and is required for both craniofacial and eye development. Full article
(This article belongs to the Special Issue Zebrafish—a Model System for Developmental Biology II)
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36 pages, 6497 KiB  
Article
Zebrafish Paralogs brd2a and brd2b Are Needed for Proper Circulatory, Excretory and Central Nervous System Formation and Act as Genetic Antagonists during Development
by Gregory L. Branigan, Kelly S. Olsen, Isabella Burda, Matthew W. Haemmerle, Jason Ho, Alexandra Venuto, Nicholas D. D’Antonio, Ian E. Briggs and Angela J. DiBenedetto
J. Dev. Biol. 2021, 9(4), 46; https://doi.org/10.3390/jdb9040046 - 31 Oct 2021
Cited by 2 | Viewed by 3622
Abstract
Brd2 belongs to the BET family of epigenetic transcriptional co-regulators that act as adaptor-scaffolds for the assembly of chromatin-modifying complexes and other factors at target gene promoters. Brd2 is a protooncogene and candidate gene for juvenile myoclonic epilepsy in humans, a homeobox gene [...] Read more.
Brd2 belongs to the BET family of epigenetic transcriptional co-regulators that act as adaptor-scaffolds for the assembly of chromatin-modifying complexes and other factors at target gene promoters. Brd2 is a protooncogene and candidate gene for juvenile myoclonic epilepsy in humans, a homeobox gene regulator in Drosophila, and a maternal-zygotic factor and cell death modulator that is necessary for normal development of the vertebrate central nervous system (CNS). As two copies of Brd2 exist in zebrafish, we use antisense morpholino knockdown to probe the role of paralog Brd2b, as a comparative study to Brd2a, the ortholog of human Brd2. A deficiency in either paralog results in excess cell death and dysmorphology of the CNS, whereas only Brd2b deficiency leads to loss of circulation and occlusion of the pronephric duct. Co-knockdown of both paralogs suppresses single morphant defects, while co-injection of morpholinos with paralogous RNA enhances them, suggesting novel genetic interaction with functional antagonism. Brd2 diversification includes paralog-specific RNA variants, a distinct localization of maternal factors, and shared and unique spatiotemporal expression, providing unique insight into the evolution and potential functions of this gene. Full article
(This article belongs to the Special Issue Zebrafish—a Model System for Developmental Biology II)
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Review

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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 10 | Viewed by 3417
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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21 pages, 2885 KiB  
Review
Two Modulators of Skeletal Development: BMPs and Proteoglycans
by Elham Koosha and B. Frank Eames
J. Dev. Biol. 2022, 10(2), 15; https://doi.org/10.3390/jdb10020015 - 6 Apr 2022
Cited by 11 | Viewed by 4125
Abstract
During embryogenesis, skeletal development is tightly regulated by locally secreted growth factors that interact with proteoglycans (PGs) in the extracellular matrix (ECM). Bone morphogenetic proteins (BMPs) are multifunctional growth factors that play critical roles in cartilage maturation and bone formation. BMP signals are [...] Read more.
During embryogenesis, skeletal development is tightly regulated by locally secreted growth factors that interact with proteoglycans (PGs) in the extracellular matrix (ECM). Bone morphogenetic proteins (BMPs) are multifunctional growth factors that play critical roles in cartilage maturation and bone formation. BMP signals are transduced from plasma membrane receptors to the nucleus through both canonical Smad and noncanonical p38 mitogen-activated protein kinase (MAPK) pathways. BMP signalling is modulated by a variety of endogenous and exogenous molecular mechanisms at different spatiotemporal levels and in both positive and negative manners. As an endogenous example, BMPs undergo extracellular regulation by PGs, which generally regulate the efficiency of ligand-receptor binding. BMP signalling can also be exogenously perturbed by a group of small molecule antagonists, such as dorsomorphin and its derivatives, that selectively bind to and inhibit the intracellular kinase domain of BMP type I receptors. In this review, we present a current understanding of BMPs and PGs functions in cartilage maturation and osteoblast differentiation, highlighting BMP–PG interactions. We also discuss the identification of highly selective small-molecule BMP receptor type I inhibitors. This review aims to shed light on the importance of BMP signalling and PGs in cartilage maturation and bone formation. Full article
(This article belongs to the Special Issue Zebrafish—a Model System for Developmental Biology II)
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15 pages, 1199 KiB  
Review
Advances in Cardiac Development and Regeneration Using Zebrafish as a Model System for High-Throughput Research
by Nicholas Francoeur and Rwik Sen
J. Dev. Biol. 2021, 9(4), 40; https://doi.org/10.3390/jdb9040040 - 25 Sep 2021
Cited by 4 | Viewed by 5301
Abstract
Heart disease is the leading cause of death in the United States and worldwide. Understanding the molecular mechanisms of cardiac development and regeneration will improve diagnostic and therapeutic interventions against heart disease. In this direction, zebrafish is an excellent model because several processes [...] Read more.
Heart disease is the leading cause of death in the United States and worldwide. Understanding the molecular mechanisms of cardiac development and regeneration will improve diagnostic and therapeutic interventions against heart disease. In this direction, zebrafish is an excellent model because several processes of zebrafish heart development are largely conserved in humans, and zebrafish has several advantages as a model organism. Zebrafish transcriptomic profiles undergo alterations during different stages of cardiac development and regeneration which are revealed by RNA-sequencing. ChIP-sequencing has detected genome-wide occupancy of histone post-translational modifications that epigenetically regulate gene expression and identified a locus with enhancer-like characteristics. ATAC-sequencing has identified active enhancers in cardiac progenitor cells during early developmental stages which overlap with occupancy of histone modifications of active transcription as determined by ChIP-sequencing. CRISPR-mediated editing of the zebrafish genome shows how chromatin modifiers and DNA-binding proteins regulate heart development, in association with crucial signaling pathways. Hence, more studies in this direction are essential to improve human health because they answer fundamental questions on cardiac development and regeneration, their differences, and why zebrafish hearts regenerate upon injury, unlike humans. This review focuses on some of the latest studies using state-of-the-art technology enabled by the elegant yet simple zebrafish. Full article
(This article belongs to the Special Issue Zebrafish—a Model System for Developmental Biology II)
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