María Jimena Mosna , Federico J. Garde , Marcelo G. Stinson , Candela D. Pastore , Abel L. Carcagno
{"title":"The chorioallantoic membrane (CAM) model: From its origins in developmental biology to its role in cancer research","authors":"María Jimena Mosna , Federico J. Garde , Marcelo G. Stinson , Candela D. Pastore , Abel L. Carcagno","doi":"10.1016/j.ydbio.2024.12.007","DOIUrl":"10.1016/j.ydbio.2024.12.007","url":null,"abstract":"<div><div>Over the past century, the chick embryo model, historically employed for research in developmental biology, has become a valuable tool for cancer research. The characteristics of the chick chorioallantoic membrane (CAM) make it a convenient model for the study of cancer, leading to the establishment of the CAM assay as an alternative to traditional <em>in vivo</em> cancer models. In this review we will explore the characteristics of the CAM that make it suitable for cancer research, as well as its consolidation as a versatile platform in this field. We will put particular emphasis on describing the key features that make this model an important asset for studying the hallmarks of cancer and for testing a wide variety of therapeutic strategies for its treatment, and which make it a suitable host for patient-derived xenografts (PDX). Additionally, we will examine the wide spectrum of methodological approaches available to study these subjects, highlighting some innovative cases. Finally, we will discuss the advantages and disadvantages of the chick CAM as a model for cancer research and how we can improve this model to its full potential.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"519 ","pages":"Pages 79-95"},"PeriodicalIF":2.5,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142853047","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Aniket Kshirsagar , Rachel Ronan , Ana Lúcia Rebelo , Siobhan McMahon , Abhay Pandit , Gerhard Schlosser
{"title":"Quantitative proteomics of regenerating and non-regenerating spinal cords in Xenopus","authors":"Aniket Kshirsagar , Rachel Ronan , Ana Lúcia Rebelo , Siobhan McMahon , Abhay Pandit , Gerhard Schlosser","doi":"10.1016/j.ydbio.2024.12.009","DOIUrl":"10.1016/j.ydbio.2024.12.009","url":null,"abstract":"<div><div>Spinal cord injury in humans is a life-changing condition with no effective treatment. However, many non-mammalian vertebrates can fully regenerate their spinal cord after injury. Frogs such as <em>Xenopus</em> can regenerate the spinal cord at larval stages, but lose this capacity at metamorphosis. This makes them ideal models to elucidate molecular pathways underlying regenerative capacity by comparing responses to spinal cord injury in regenerative (R) and non-regenerative (NR) stages of the same species. Here we use quantitative proteomics with Isobaric Tags for Relative and Absolute Quantification (iTRAQ) followed by Ingenuity Pathway Analysis (IPA) to identify functions and pathways that were differentially regulated after spinal cord injury between R and NR stages in <em>Xenopus laevis</em>. We find that many embryonic pathways of neuronal development are re-activated following SCI at the R but not at the NR stage. This is accompanied by the upregulation of regulatory proteins controlling transcription and translation at the R stage, but their downregulation at the NR stage. Conversely, lipid hydrolysis and uptake as well as mitochondrial oxidative phosphorylation is downregulated at the R, but upregulated at the NR stage. Taken together this suggests that dysregulation of lipid homeostasis and augmentation of oxidative stress play a key role in the loss of regenerative capacity of the spinal cord after metamorphosis. In identifying new factors regulating regenerative capacity in the vertebrate spinal cord, our findings suggest new potential therapeutic targets for promoting neural repair in the injured adult mammalian spinal cord.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"519 ","pages":"Pages 65-78"},"PeriodicalIF":2.5,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142852974","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Elkhan Yusifov , Martina Schaettin , Alexandre Dumoulin , Ruxandra Bachmann-Gagescu , Esther T. Stoeckli
{"title":"The primary cilium gene CPLANE1 is required for peripheral nervous system development","authors":"Elkhan Yusifov , Martina Schaettin , Alexandre Dumoulin , Ruxandra Bachmann-Gagescu , Esther T. Stoeckli","doi":"10.1016/j.ydbio.2024.12.008","DOIUrl":"10.1016/j.ydbio.2024.12.008","url":null,"abstract":"<div><div>Ciliopathies are a group of neurodevelopmental disorders characterized by the dysfunction of the primary cilium. This small protrusion from most cells of our body serves as a signaling hub for cell-to-cell communication during development. Cell proliferation, differentiation, migration, and neural circuit formation have been demonstrated to depend on functional primary cilia. In the context of ciliopathies, the focus has been on the development of the central nervous system, while the peripheral nervous system has not been studied in depth. In line with phenotypes seen in patients, the absence of a functional primary cilium was shown to affect the migration of cranial and vagal neural crest cells, which contribute to the development of craniofacial features and the heart, respectively. We show here that the ciliopathy gene Cplane1 is required for the development of the peripheral nervous system. Loss of Cplane1 function in chicken embryos induces defects in dorsal root ganglia, which vary in size and fail to localize symmetrically along the spinal cord. These defects may help to understand the alteration in somatosensory perceptions described in some ciliopathy patients.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"519 ","pages":"Pages 106-121"},"PeriodicalIF":2.5,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142853128","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The search to understand the development of the chicken immune system: Differences in expression of MHC class I loci and waves of thymocytes as evolutionary relics?","authors":"Samer Halabi, Nicolas Rocos, Jim Kaufman","doi":"10.1016/j.ydbio.2024.12.006","DOIUrl":"10.1016/j.ydbio.2024.12.006","url":null,"abstract":"<div><div>Chickens are renowned as a model for embryogenesis but have also been responsible for crucial advances in virology, cancer research and immunology. However, chickens are best known as a major source of animal protein for human nutrition, with roughly 80 billion chickens alive each year supplying meat and eggs, the vast majority part of a global poultry industry. As a result, avian immunology been studied intensively for over 60 years, and it has become clear that a major genetic locus in chickens determining resistance to infectious disease and response to vaccines is the major histocompatibility complex (MHC). Compared to typical mammals, the chicken MHC is compact and simple, with only two classical class I genes. A dominantly-expressed class I gene, BF2, is the major ligand for cytotoxic T lymphocytes (CTLs), while the other locus, BF1, is much less well-expressed, lacking in some MHC haplotypes, and is a ligand for natural killer (NK) cells. Cell surface class I expression in neonatal chicks is far less than in adults, and one possibility is that BF2 is not well-expressed early in ontogeny. A precedent is found for amphibians: the single classical class I molecule is not expressed in tadpoles of <em>Xenopus</em> frogs, although non-polymorphic (and thus non-classical) class I molecules from the XNC locus are expressed, which are recognised for immune defence by non-canonical NKT lymphocytes. Indeed, three waves of different T cells are produced by the <em>Xenopus</em> thymus: in tadpoles, during metamorphosis and finally as adults. Three waves of thymic emigrants are also found for chickens, and reasoning by analogy, it may be that the waves of thymocytes and the expression of class I molecules during ontogeny of chickens are evolutionary relics. As well as scientific interest in the ontogeny of MHC class I expression and appearance of peripheral T cells, there are potential practical implications, given the importance of vaccination in ovo and in day-old chicks for the poultry industry.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"519 ","pages":"Pages 38-45"},"PeriodicalIF":2.5,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142853271","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Carla Caniçais , Daniel Sobral , Sara Vasconcelos , Mariana Cunha , Alice Pinto , Joana Mesquita Guimarães , Fátima Santos , Alberto Barros , Sofia Dória , C. Joana Marques
{"title":"Transcriptomic analysis and epigenetic regulators in human oocytes at different stages of oocyte meiotic maturation","authors":"Carla Caniçais , Daniel Sobral , Sara Vasconcelos , Mariana Cunha , Alice Pinto , Joana Mesquita Guimarães , Fátima Santos , Alberto Barros , Sofia Dória , C. Joana Marques","doi":"10.1016/j.ydbio.2024.12.004","DOIUrl":"10.1016/j.ydbio.2024.12.004","url":null,"abstract":"<div><div>Human oocytes are highly specialized cells with the capacity to store and regulate mRNAs during oocyte maturation, in preparation for post-fertilization steps.</div><div>Here we performed single-oocyte transcriptomic analysis of human oocytes in three meitoic maturation stages – Germinal Vesicle (GV; n = 6), Metaphase I (MI; n = 6) and Metaphase II (MII; n = 7).</div><div>Single-oocyte transcriptomic analysis revealed that the total number of expressed genes progressively decreased from GV to MII stages, with 9660 genes being transcribed in GV, 8734 in MI and 5889 in MII. The same tendency was observed for the number of uniquely expressed genes, with 1328 uniquely expressed genes in GV, 401 in MI and 72 in MII. GO analysis of the uniquely expressed genes showed distinct terms in GV oocytes such as transferase activity, organonitrogen compound metabolic process and ncRNA processing. Analysis of Differentially Expressed Genes (DEGs) between the three maturation stages revealed 1165 DEGs between GV and MII oocytes, with 635 being upregulated and 528 downregulated, 42 DEGs between GV and MI, with 38 being upregulated and 4 downregulated, and no significant changes in gene expression between MI and MII oocytes. Comprehensive analysis of epigenetic regulators showed high expression of several histone-modifying enzymes, namely deacetylases, acetylases, lysine demethylases and methyltransferases, and DNA methylation regulators, namely the maintenance methyltransferase <em>DNMT1</em> and its co-regulators <em>DPPA3</em> and <em>UHRF1</em>. Some of these epigenetic regulators were differentially expressed between maturation stages, namely <em>SIRT3</em>, <em>SIRT6</em>, <em>KDM3AP1</em>, <em>KMT2E</em>, <em>DNMT1</em>, <em>DPPA3</em> and the <em>MEST</em> and <em>RASGRF1</em> imprinted genes.</div><div>Our study contributes with important information on the transcriptional landscape of human oocytes in different stages of meiotic maturation, providing important insights into candidate biomarkers of human oocyte quality.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"519 ","pages":"Pages 55-64"},"PeriodicalIF":2.5,"publicationDate":"2024-12-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142834407","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Carol Readhead , Simon Mahler , Zhenyu Dong , Yuki Sato , Changhuei Yang , Marianne E. Bronner
{"title":"Automated non-invasive laser speckle imaging of the chick heart rate and extraembryonic blood vessels and their response to Nifedipine and Amlodipine drugs","authors":"Carol Readhead , Simon Mahler , Zhenyu Dong , Yuki Sato , Changhuei Yang , Marianne E. Bronner","doi":"10.1016/j.ydbio.2024.12.005","DOIUrl":"10.1016/j.ydbio.2024.12.005","url":null,"abstract":"<div><div>Using our recently developed laser speckle contrast imaging (LSCI) to visualize blood vessels and monitor blood flow noninvasively, we test the utility of the developing chick heart as a functional model for drug screening. To this end, we examined the effects of antihypertensive agents Nifedipine and Amlodipine, belonging to the L-type calcium channel antagonist family, on blood flow visualized noninvasively through the intact shell. Guided by the live view mode, the drugs were injected through the shell and ventral to HH16-19 chick embryos. Our results show a significant reduction in the chick's heart rate, blood flow, and vascular size within 5–20 min after Nifedipine or Amlodipine injection. For moderate Nifedipine concentrations, these parameters returned to initial values within 2–3 h. Nifedipine showed a rapid reduction in heart rate and blood flow dynamics at a concentration ten times lower than Amlodipine. These findings show that our LSCI system can monitor and distinguish the chick heart's response to injected drugs from the same family. This serves as proof-of-concept, paving the way for a rapid, cost-effective, and quantitative test system for screening drugs that affect the cardiovascular system of live chick embryos. Live noninvasive imaging may also provide insights into the development and functioning of the vertebrate heart.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"519 ","pages":"Pages 46-54"},"PeriodicalIF":2.5,"publicationDate":"2024-12-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142827911","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Congenital heart defects differ following left versus right avian cardiac neural crest ablation","authors":"Tatiana Solovieva, Marianne E. Bronner","doi":"10.1016/j.ydbio.2024.12.003","DOIUrl":"10.1016/j.ydbio.2024.12.003","url":null,"abstract":"<div><div>The cardiac neural crest is critical for the normal development of the heart, as its surgical ablation in the chick recapitulates common human congenital heart defects such as ‘Common Arterial Trunk’ and ‘Double Outlet Right Ventricle’ (DORV). While left-right asymmetry is known to be important for heart development, little is known about potential asymmetric differences between right and left cardiac neural folds with respect to heart development. Here, through surgical ablation of either left or right cardiac neural crest, we find that right ablation results in more varied and more severe heart defects. Embryos with Common Arterial Trunk and with missing arteries occurred in right-ablated embryos but were not observed in left-ablated embryos; moreover, embryos with DORV and with misalignment of the arteries were more prevalent following right versus left cardiac crest ablation. In addition, survival of right-ablated embryos was lower than left-ablated embryos. Together, these data raise the intriguing possibility that there may be differences in left versus right cardiac neural crest during heart development.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"519 ","pages":"Pages 30-37"},"PeriodicalIF":2.5,"publicationDate":"2024-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142817559","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Development and functions of the area opaca of the chick embryo","authors":"Hyung Chul Lee , Yara Fadaili , Claudio D. Stern","doi":"10.1016/j.ydbio.2024.12.002","DOIUrl":"10.1016/j.ydbio.2024.12.002","url":null,"abstract":"<div><div>Before radial symmetry-breaking of the blastoderm, the chick embryo is distinctly divided into a central area pellucida and a surrounding region, the area opaca. In this review, we focus on the area opaca and its functions. First, we survey current knowledge about how the area opaca is formed during the intrauterine period and how it sets up its initial tissue structure. With the formation of a vascularized mesoderm layer, the area opaca becomes subdivided into an inner area vasculosa and an outer area vitellina, which contribute to the development of extraembryonic membranes: the yolk sac and chorion. Second, we review the various functions of the area opaca during development including supplying nutrients, driving the expansion of the embryo by a specialized population of edge cells, and active, instructive signaling that plays a role in the establishment of embryonic polarity and orchestrates the formation of another extraembryonic tissue, the marginal zone, essential for positioning the first midline structure, the primitive streak, at the beginning of gastrulation.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"519 ","pages":"Pages 13-20"},"PeriodicalIF":2.5,"publicationDate":"2024-12-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11785533/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142812672","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Decoding a Cell's Fate: How Notch and receptor tyrosine kinase signals specify the Drosophila R7 photoreceptor","authors":"Ronald A. Arias, Andrew Tomlinson","doi":"10.1016/j.ydbio.2024.12.001","DOIUrl":"10.1016/j.ydbio.2024.12.001","url":null,"abstract":"<div><div>The process by which the <em>Drosophila</em> R7 photoreceptor is specified has become a classic model for understanding how cell-cell signals direct cell fates. In the R7 precursor cell, both the Notch and receptor tyrosine kinase (RTK) signaling pathways are active, and the information they encode directs the specification of the R7 photoreceptor identity. In this process, Notch performs three distinct functions: it both opposes and promotes the actions of the RTK pathway to specify the photoreceptor fate, and it determines the type of photoreceptor that is specified. The RTK pathway drives transcription of <em>phyl</em> - a gene expression necessary for photoreceptor specification. We show that Notch activity induces transcription of the <em>yan</em> gene which encodes a transcriptional repressor of <em>phyl</em>. This defines an antagonism between the two pathways, with RTK promoting and Notch opposing <em>phyl</em> transcription. We previously showed that Notch activity supplies Sevenless to the R7 precursor to allow the RTK pathway hyperactivation required to overcome the Notch repression, and we now identify the regulation of Yan activity as a site of integration of RTK and Notch signaling pathways. Once the cell is specified as a photoreceptor, the third Notch function then prevents <em>seven-up</em> (<em>svp</em>) transcription. The Svp transcription factor directs the R1/6 photoreceptor fate, and the prevention of its expression ensures the default R7 specification.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"519 ","pages":"Pages 21-29"},"PeriodicalIF":2.5,"publicationDate":"2024-12-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142799657","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"CRISPR-Cas13d as a molecular tool to achieve targeted gene expression knockdown in chick embryos","authors":"Minyoung Kim , Erica J. Hutchins","doi":"10.1016/j.ydbio.2024.11.013","DOIUrl":"10.1016/j.ydbio.2024.11.013","url":null,"abstract":"<div><div>The chick embryo is a classical model system commonly used in developmental biology due to its amenability to gene perturbation experiments. Pairing this powerful model organism with cutting-edge technology can significantly expand the range of experiments that can be performed. Recently, the CRISPR-Cas13d system has been successfully adapted for use in zebrafish, medaka, killifish, and mouse embryos to achieve targeted gene expression knockdown. Despite its success in other animal models, no prior study has explored the potential of CRISPR-Cas13d in the chick. Here, we present an adaptation of the CRISPR-Cas13d system to achieve targeted gene expression knockdown in the chick embryo. As proof-of-principle, we demonstrate the knockdown of PAX7, an early neural crest marker. Application of this adapted CRISPR-Cas13d technique resulted in effective knockdown of PAX7 expression and function, comparable to knockdown achieved by translation-blocking morpholino. CRISPR-Cas13d complements preexisting knockdown tools such as CRISPR-Cas9 and morpholinos, thereby expanding the experimental potential and versatility of the chick model system.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"519 ","pages":"Pages 5-12"},"PeriodicalIF":2.5,"publicationDate":"2024-11-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142767407","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}