DevelopmentPub Date : 2025-03-15Epub Date: 2025-03-26DOI: 10.1242/dev.204398
Anne Bourdais, Patricia Viard, Jenny Bormann, Côme Sesboüé, Daniel Guerrier, Nicole Therville, Julie Guillermet-Guibert, John Carroll, Guillaume Halet
{"title":"Distinct requirements for PI3K isoforms p110α and p110δ for PIP3 synthesis in mouse oocytes and early embryos.","authors":"Anne Bourdais, Patricia Viard, Jenny Bormann, Côme Sesboüé, Daniel Guerrier, Nicole Therville, Julie Guillermet-Guibert, John Carroll, Guillaume Halet","doi":"10.1242/dev.204398","DOIUrl":"10.1242/dev.204398","url":null,"abstract":"<p><p>The phosphoinositide 3-kinase (PI3K)/Akt pathway is thought to regulate key steps of mammalian oogenesis, such as dormant oocyte awakening during follicular activation, meiotic resumption and oocyte maturation. Supporting evidence is, however, indirect, as oocyte PI3K activation has never been formally demonstrated, and the PI3K isoforms involved have not been revealed. Here, we employed fluorescent PIP3 biosensors to characterize PI3K dynamics in mouse oocytes and we investigated the contribution of the PI3K isoform p110α by conditional genetic ablation. Prophase oocytes showed baseline PI3K/Akt activation that could be further stimulated by adding Kit ligand. Contrary to previous reports, maternal PI3K proved dispensable for oocyte maturation in vitro, yet it was required for PIP3 synthesis in early embryos. We further show that oocyte p110α is not essential for oogenesis and female fertility. Accordingly, our data suggest that Kit ligand activates isoform p110δ for PIP3 synthesis in oocytes. In contrast, constitutive PIP3 synthesis in early embryos is achieved by maternal p110α acting redundantly with p110δ. This study highlights the relevance of PIP3 biosensors in establishing the dynamics, mechanisms and roles of maternal PI3K signaling during mammalian oogenesis.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":" ","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-03-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143467310","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2025-03-15Epub Date: 2025-03-31DOI: 10.1242/dev.204592
Dagmar Wilhelm, Aitana Perea-Gomez, Axel Newton, Marie-Christine Chaboissier
{"title":"Gonadal sex determination in vertebrates: rethinking established mechanisms.","authors":"Dagmar Wilhelm, Aitana Perea-Gomez, Axel Newton, Marie-Christine Chaboissier","doi":"10.1242/dev.204592","DOIUrl":"10.1242/dev.204592","url":null,"abstract":"<p><p>Sex determination and differentiation are fundamental processes that are not only essential for fertility but also influence the development of many other organs, and hence, are important for species diversity and survival. In mammals, sex is determined by the inheritance of an X or a Y chromosome from the father. The Y chromosome harbours the testis-determining gene SRY, and it has long been thought that its absence is sufficient for ovarian development. Consequently, the ovarian pathway has been treated as a default pathway, in the sense that ovaries do not have or need a female-determining factor. Recently, a female-determining factor has been identified in mouse as the master regulator of ovarian development. Interestingly, this scenario was predicted as early as 1983. In this Review, we discuss the model predicted in 1983, how the mechanisms and genes currently known to be important for sex determination and differentiation in mammals have changed or supported this model, and finally, reflect on what these findings might mean for sex determination in other vertebrates.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":"152 6","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-03-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143751156","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2025-03-01Epub Date: 2025-03-12DOI: 10.1242/dev.204555
Christopher De Bono, Yichi Xu, Samina Kausar, Marine Herbane, Camille Humbert, Sevda Rafatov, Chantal Missirian, Mathias Moreno, Weiyang Shi, Yorick Gitton, Alberto Lombardini, Ivo Vanzetta, Séverine Mazaud-Guittot, Alain Chédotal, Anaïs Baudot, Stéphane Zaffran, Heather C Etchevers
{"title":"Multi-modal refinement of the human heart atlas during the first gestational trimester.","authors":"Christopher De Bono, Yichi Xu, Samina Kausar, Marine Herbane, Camille Humbert, Sevda Rafatov, Chantal Missirian, Mathias Moreno, Weiyang Shi, Yorick Gitton, Alberto Lombardini, Ivo Vanzetta, Séverine Mazaud-Guittot, Alain Chédotal, Anaïs Baudot, Stéphane Zaffran, Heather C Etchevers","doi":"10.1242/dev.204555","DOIUrl":"10.1242/dev.204555","url":null,"abstract":"<p><p>Forty first-trimester human hearts were studied to lay groundwork for further studies of the mechanisms underlying congenital heart defects. We first sampled 49,227 cardiac nuclei from three fetuses at 8.6, 9.0, and 10.7 post-conceptional weeks (pcw) for single-nucleus RNA sequencing, enabling the distinction of six classes comprising 21 cell types. Improved resolution led to the identification of previously unappreciated cardiomyocyte populations and minority autonomic and lymphatic endothelial transcriptomes, among others. After integration with 5-7 pcw heart single-cell RNA-sequencing data, we identified a human cardiomyofibroblast progenitor preceding the diversification of cardiomyocyte and stromal lineages. Spatial transcriptomic analysis (six Visium sections from two additional hearts) was aided by deconvolution, and key spatial markers validated on sectioned and whole hearts in two- and three-dimensional space and over time. Altogether, anatomical-positional features, including innervation, conduction and subdomains of the atrioventricular septum, translate latent molecular identity into specialized cardiac functions. This atlas adds unprecedented spatial and temporal resolution to the characterization of human-specific aspects of early heart formation.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":" ","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143381787","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2025-03-01Epub Date: 2025-03-14DOI: 10.1242/dev.204624
Eliana Nehme, Amitesh Panda, Isabelle Migeotte, Vincent Pasque
{"title":"Extra-embryonic mesoderm during development and in in vitro models.","authors":"Eliana Nehme, Amitesh Panda, Isabelle Migeotte, Vincent Pasque","doi":"10.1242/dev.204624","DOIUrl":"10.1242/dev.204624","url":null,"abstract":"<p><p>Extra-embryonic tissues provide protection and nutrition in vertebrates, as well as a connection to the maternal tissues in mammals. The extra-embryonic mesoderm is an essential and understudied germ layer present in amniotes. It is involved in hematopoiesis, as well as in the formation of extra-embryonic structures such as the amnion, umbilical cord and placenta. The origin and specification of extra-embryonic mesoderm are not entirely conserved across species, and the molecular mechanisms governing its formation and function are not fully understood. This Review begins with an overview of the embryonic origin and function of extra-embryonic mesoderm in vertebrates from in vivo studies. We then compare in vitro models that generate extra-embryonic mesoderm-like cells. Finally, we discuss how insights from studying both embryos and in vitro systems can aid in designing even more advanced stem cell-based embryo models.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":"152 5","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143623932","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2025-03-01Epub Date: 2025-03-11DOI: 10.1242/dev.204728
{"title":"The people behind the papers - Juan Yang and Xuanmao Chen.","authors":"","doi":"10.1242/dev.204728","DOIUrl":"10.1242/dev.204728","url":null,"abstract":"<p><p>In mammalian embryos, brains develop from the inside out, with younger neurons moving to the outer layers in a process called radial migration. A new paper in Development finds that, during postnatal development, some of the neurons in the outer layers of the brain undergo a 'reverse movement', repositioning themselves by moving in the opposite direction to the initial radial migration. To learn more about the story behind the paper, we caught up with first author Juan Yang and corresponding author Xuanmao Chen, Associate Professor of Neurobiology at the University of New Hampshire (UNH), USA.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":"152 5","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143604186","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2025-03-01Epub Date: 2025-03-07DOI: 10.1242/dev.204501
Ling S Loh, Kyle A DeMarr, Martina Tsimba, Christa Heryanto, Alejandro Berrio, Nipam H Patel, Arnaud Martin, W Owen McMillan, Gregory A Wray, Joseph J Hanly
{"title":"Lepidopteran scale cells derive from sensory organ precursors through a canonical lineage.","authors":"Ling S Loh, Kyle A DeMarr, Martina Tsimba, Christa Heryanto, Alejandro Berrio, Nipam H Patel, Arnaud Martin, W Owen McMillan, Gregory A Wray, Joseph J Hanly","doi":"10.1242/dev.204501","DOIUrl":"10.1242/dev.204501","url":null,"abstract":"<p><p>The success of butterflies and moths is tightly linked to the origin of scales within the group. A long-standing hypothesis postulates that scales are homologous to the well-described mechanosensory bristles found in the fruit fly Drosophila melanogaster, as both derive from an epithelial precursor. Previous histological and candidate gene approaches identified parallels in genes involved in scale and bristle development. Here, we provide developmental and transcriptomic evidence that the differentiation of lepidopteran scales derives from the sensory organ precursor (SOP). Live imaging in lepidopteran pupae shows that SOP cells undergo two asymmetric divisions that first abrogate the neurogenic lineage, and then lead to a differentiated scale precursor and its associated socket cell. Single-nucleus RNA sequencing using early pupal wings revealed differential gene expression patterns that mirror SOP development, suggesting a shared developmental program. Additionally, we recovered a newly associated gene, the transcription factor pdm3, involved in the proper differentiation of butterfly wing scales. Altogether, these data open up avenues for understanding scale type specification and development, and illustrate how single-cell transcriptomics provide a powerful platform for understanding evolution of cell types.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":"152 5","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11925400/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143572540","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2025-03-01Epub Date: 2025-03-11DOI: 10.1242/dev.204405
Tamsin J Samuels, Elizabeth J Torley, Valeriia Nadmitova, Emily L Naden, Phoebe E Blair, Frankjel A Hernandez Frometa, Felipe Karam Teixeira
{"title":"Destabilisation of bam transcripts terminates the mitotic phase of Drosophila female germline differentiation.","authors":"Tamsin J Samuels, Elizabeth J Torley, Valeriia Nadmitova, Emily L Naden, Phoebe E Blair, Frankjel A Hernandez Frometa, Felipe Karam Teixeira","doi":"10.1242/dev.204405","DOIUrl":"10.1242/dev.204405","url":null,"abstract":"<p><p>The tight control of the mitotic phase of differentiation is crucial to prevent tumourigenesis while securing tissue homeostasis. In the Drosophila female germline, differentiation involves precisely four mitotic divisions, and accumulating evidence suggests that bag of marbles (bam), the initiator of differentiation, is also involved in controlling the number of divisions. To test this hypothesis, we depleted Bam from differentiating cells and found a reduced number of mitotic divisions. We examined the regulation of Bam using RNA imaging methods and found that the bam 3' UTR conveys instability to the transcript in the eight-cell cyst and early 16-cell cyst. We show that the RNA-binding protein Rbp9 is responsible for timing bam mRNA decay. Rbp9 itself is part of a sequential cascade of RNA-binding proteins activated downstream of Bam, and we show that it is regulated through a change in transcription start site, driven by Rbfox1. Altogether, we propose a model in which Bam expression at the beginning of differentiation initiates a series of events that eventually terminates the Bam expression domain.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":" ","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143440303","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2025-03-01Epub Date: 2025-03-11DOI: 10.1242/dev.204300
Juan Yang, Soheila Mirhosseiniardakani, Liyan Qiu, Kostandina Bicja, Abigail Del Greco, Kevin JungKai Lin, Mark Lyon, Xuanmao Chen
{"title":"Cilia directionality reveals a slow reverse movement of principal neurons for positioning and lamina refinement in the cerebral cortex.","authors":"Juan Yang, Soheila Mirhosseiniardakani, Liyan Qiu, Kostandina Bicja, Abigail Del Greco, Kevin JungKai Lin, Mark Lyon, Xuanmao Chen","doi":"10.1242/dev.204300","DOIUrl":"10.1242/dev.204300","url":null,"abstract":"<p><p>Currently, not much is known about neuronal positioning and the roles of primary cilia in postnatal neurodevelopment. We show that primary cilia of principal neurons undergo marked changes in positioning and orientation, concurrent with postnatal neuron positioning in the mouse cerebral cortex. Primary cilia of early- and late-born principal neurons in compact layers display opposite orientations, while neuronal primary cilia in loose laminae are predominantly oriented toward the pia. In contrast, astrocytes and interneurons, and neurons in nucleated brain regions do not display specific cilia directionality. We further discovered that the cell bodies of principal neurons in inside-out laminated regions spanning from the hippocampal CA1 region to neocortex undergo a slow 'reverse movement' for postnatal positioning and lamina refinement. Furthermore, selective disruption of cilia function in the forebrain leads to altered lamination and gyrification in the retrosplenial cortex that is formed by reverse movement. Collectively, this study identifies reverse movement as a fundamental process for principal cell positioning that refines lamination in the cerebral cortex and casts light on the evolutionary transition from three-layered allocortices to six-layered neocortices.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":"152 5","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12050088/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143604180","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2025-03-01Epub Date: 2025-03-03DOI: 10.1242/dev.204297
Viviane Medeiros Oliveira-Valença, Jacqueline Marie Roberts, Vitória Melo Fernandes-Cerqueira, Carolina Herkenhoff Colmerauer, Beatriz Cardoso de Toledo, Pedro Lucas Santos-França, Rafael Linden, Rodrigo Alves Portela Martins, Maurício Rocha-Martins, Alejandra Bosco, Monica Lynn Vetter, Mariana Souza da Silveira
{"title":"POU4F2 overexpression promotes the genesis of retinal ganglion cell-like projection neurons from late progenitors.","authors":"Viviane Medeiros Oliveira-Valença, Jacqueline Marie Roberts, Vitória Melo Fernandes-Cerqueira, Carolina Herkenhoff Colmerauer, Beatriz Cardoso de Toledo, Pedro Lucas Santos-França, Rafael Linden, Rodrigo Alves Portela Martins, Maurício Rocha-Martins, Alejandra Bosco, Monica Lynn Vetter, Mariana Souza da Silveira","doi":"10.1242/dev.204297","DOIUrl":"10.1242/dev.204297","url":null,"abstract":"<p><p>Retinal ganglion cells (RGCs) are the projection neurons of the retina, and their death promotes an irreversible blindness. Several factors were described to control their genesis during retinal development. These include Atoh7, a major orchestrator of the RGC program, and downstream targets of this transcription factor, including Pou4f factors, that in turn regulate key aspects of terminal differentiation. The absence of POU4F family genes results in defects in RGC differentiation, aberrant axonal elaboration and, ultimately, RGC death. This confirms the requirement of POU4F factors for RGC development and survival, with a crucial role in regulating RGC axon outgrowth and pathfinding. Here, we have investigated in vivo whether ectopic Pou4f2 expression in late retinal progenitor cells (late RPCs) is sufficient to induce the generation of cells with RGC properties, including long-range axon projections. We show that Pou4f2 overexpression generates RGC-like cells that share morphological and transcriptional features with RGCs that are normally generated during early development and extend axonal projections up to the brain. In conclusion, these results show that POU4F2 alone is sufficient to promote the crucial properties of projection neurons that arise from retinal progenitors outside their developmental window.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":" ","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143413505","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2025-03-01Epub Date: 2025-03-13DOI: 10.1242/dev.204736
{"title":"The people behind the papers - Matthew Kourakis and William Smith.","authors":"","doi":"10.1242/dev.204736","DOIUrl":"10.1242/dev.204736","url":null,"abstract":"<p><p>The caudal nerve cord of the tunicate Ciona has similar anatomical features to the vertebrate spinal cord, but it is reported to lack motor neurons or to contain ill-defined neurons. In a new study, William Smith and colleagues looked at a later developmental stage than previous studies and identified functional motor neurons in the Ciona larval tail, suggesting homology between the Ciona caudal nerve cord and the vertebrate spinal cord. To find out more about the work, we caught up with first author Matthew Kourakis and corresponding author William Smith, Professor at the University of California, Santa Barbara, USA.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":"152 5","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143623936","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}