DevelopmentPub Date : 2025-01-15Epub Date: 2025-01-20DOI: 10.1242/dev.204264
Lauren Bobzin, Audrey Nickle, Sebastian Ko, Michaela Ince, Aaron Huang, Arshia Bhojwani, Ryan Roberts, Amy E Merrill
{"title":"FGFR2 directs inhibition of WNT signaling to regulate anterior fontanelle closure during skull development.","authors":"Lauren Bobzin, Audrey Nickle, Sebastian Ko, Michaela Ince, Aaron Huang, Arshia Bhojwani, Ryan Roberts, Amy E Merrill","doi":"10.1242/dev.204264","DOIUrl":"10.1242/dev.204264","url":null,"abstract":"<p><p>The calvarial bones of the infant skull are linked by transient fibrous joints known as sutures and fontanelles, which are essential for skull compression during birth and expansion during postnatal brain growth. Genetic conditions caused by pathogenic variants in FGFR2, such as Apert, Pfeiffer, and Crouzon syndromes, result in calvarial deformities due to premature suture fusion and a persistently open anterior fontanelle (AF). In this study, we investigated how Fgfr2 regulates AF closure by leveraging mouse genetics and single-cell transcriptomics. We find that AF cells, marked by the tendon/ligament factor SCX, are spatially organized into ecto- and endocranial domains that selectively differentiate into ligament, bone, and cartilage to form the posterior frontal suture. We show that AF cell differentiation is non-autonomously regulated by FGFR2 signaling in osteogenic front cells of the frontal bones, which regulate WNT signaling in neighboring AF cells by expressing the secreted WNT inhibitor Wif1. Upon loss of Fgfr2, Wif1 expression is downregulated, and AF cells fail to form the posterior frontal suture. This study identifies an FGF-WNT signaling circuit that that directs suture formation within the AF during postnatal development.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":" ","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-01-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11829768/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142946426","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 : 2025-01-01Epub Date: 2025-01-02DOI: 10.1242/dev.203164
Carolyn Engel-Pizcueta, Covadonga F Hevia, Adrià Voltes, Jean Livet, Cristina Pujades
{"title":"Her9 controls the stemness properties of hindbrain boundary cells.","authors":"Carolyn Engel-Pizcueta, Covadonga F Hevia, Adrià Voltes, Jean Livet, Cristina Pujades","doi":"10.1242/dev.203164","DOIUrl":"10.1242/dev.203164","url":null,"abstract":"<p><p>The different spatiotemporal distribution of progenitor and neurogenic capacities permits that brain regions engage asynchronously in neurogenesis. In the hindbrain, rhombomere progenitor cells contribute to neurons during the first neurogenic phase, whereas boundary cells participate later. To analyze what maintains boundary cells as non-neurogenic progenitors, we addressed the role of Her9, a zebrafish Hes1-related protein. her9 expression is temporarily sustained in boundary cells independently of Notch at early embryonic stages, while they are non-neurogenic progenitors. Complementary functional approaches show that Her9 inhibits the onset of Notch signaling and the neurogenic program, keeping boundary cells as progenitors. Multicolor clonal analysis combined with genetic perturbations reveal that Her9 expands boundary progenitors by promoting symmetric proliferative and preventing neurogenic cell divisions. Her9 also regulates the proliferation of boundary cells by inhibiting the cell cycle arrest gene cdkn1ca and interplaying with Cyclin D1. Moreover, her9 is enriched in hindbrain radial glial cells at late embryonic stages independently of Notch. Together these data demonstrate that Her9 maintains the stemness properties of hindbrain boundary progenitors and late radial glial cells, ensuring the different temporal distribution of neurogenic capacities within the hindbrain.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":" ","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11829766/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142766998","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 : 2025-01-01Epub Date: 2025-01-02DOI: 10.1242/dev.202796
Rodrigo García-Tejera, Jing-Yi Tian, Marc Amoyel, Ramon Grima, Linus J Schumacher
{"title":"Licensing and niche competition in spermatogenesis: mathematical models suggest complementary regulation of tissue maintenance.","authors":"Rodrigo García-Tejera, Jing-Yi Tian, Marc Amoyel, Ramon Grima, Linus J Schumacher","doi":"10.1242/dev.202796","DOIUrl":"10.1242/dev.202796","url":null,"abstract":"<p><p>To maintain and regenerate adult tissues after injury, division and differentiation of tissue-resident stem cells must be precisely regulated. It remains elusive which regulatory strategies prevent exhaustion or overgrowth of the stem cell pool, whether there is coordination between multiple mechanisms, and how to detect them from snapshots. In Drosophila testes, somatic stem cells transition to a state that licenses them to differentiate, but remain capable of returning to the niche and resuming cell division. Here, we build stochastic mathematical models for the somatic stem cell population to investigate how licensing contributes to homeostasis. We find that licensing, in combination with differentiation occurring in pairs, is sufficient to maintain homeostasis and prevent stem cell extinction from stochastic fluctuations. Experimental data have shown that stem cells are competing for niche access, and our mathematical models demonstrate that this contributes to the reduction in the variability of stem cell numbers but does not prevent extinction. Hence, a combination of both regulation strategies, licensing with pairwise differentiation and competition for niche access, may be needed to reduce variability and prevent extinction simultaneously.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":"152 1","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11829763/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142914014","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 : 2025-01-01Epub Date: 2025-01-06DOI: 10.1242/dev.204567
Sarah J Bray, Stephen J Royle, Holly A Shiels, Daniel St Johnston
{"title":"The Company of Biologists: celebrating 100 years.","authors":"Sarah J Bray, Stephen J Royle, Holly A Shiels, Daniel St Johnston","doi":"10.1242/dev.204567","DOIUrl":"10.1242/dev.204567","url":null,"abstract":"","PeriodicalId":11375,"journal":{"name":"Development","volume":"152 1","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142930976","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 : 2025-01-01Epub Date: 2025-01-09DOI: 10.1242/dev.204438
Dillan Saunders, Carlos Camacho-Macorra, Benjamin Steventon
{"title":"Spinal cord elongation enables proportional regulation of the zebrafish posterior body.","authors":"Dillan Saunders, Carlos Camacho-Macorra, Benjamin Steventon","doi":"10.1242/dev.204438","DOIUrl":"10.1242/dev.204438","url":null,"abstract":"<p><p>Early embryos display a remarkable ability to regulate tissue patterning in response to changes in tissue size. However, it is not clear whether this ability continues into post-gastrulation stages. Here, we performed targeted removal of dorsal progenitors in the zebrafish tailbud using multiphoton ablation. This led to a proportional reduction in the length of the spinal cord and paraxial mesoderm in the tail, revealing a capacity for the regulation of tissue morphogenesis during tail formation. Following analysis of cell proliferation, gene expression, signalling and cell movements, we found no evidence of cell fate switching from mesoderm to neural fate to compensate for neural progenitor loss. Furthermore, tail paraxial mesoderm length is not reduced upon direct removal of an equivalent number of mesoderm progenitors, ruling out the hypothesis that neuromesodermal competent cells enable proportional regulation. Instead, reduction in cell number across the spinal cord reduces both spinal cord and paraxial mesoderm length. We conclude that spinal cord elongation is a driver of paraxial mesoderm elongation in the zebrafish tail and that this can explain proportional regulation upon neural progenitor reduction.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":" ","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11829759/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142913973","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 : 2025-01-01Epub Date: 2025-01-02DOI: 10.1242/dev.204551
{"title":"Transitions in development - an interview with Maria Almuedo-Castillo.","authors":"","doi":"10.1242/dev.204551","DOIUrl":"https://doi.org/10.1242/dev.204551","url":null,"abstract":"<p><p>Maria Almuedo-Castillo is a Junior Group Leader at the Andalusian Center for Development Biology (CABD). Maria's group studies how mechanical forces are translated into the gene regulatory signals that impact a cell. We spoke to Maria over Teams to learn more about her early-career research, her transition into being a group leader, and her insights into navigating the academic profession.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":"152 1","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142920993","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 : 2025-01-01Epub Date: 2025-01-07DOI: 10.1242/dev.199746
Yuji Matsuoka, Taro Nakamura, Takahito Watanabe, Austen A Barnett, Sayuri Tomonari, Guillem Ylla, Carrie A Whittle, Sumihare Noji, Taro Mito, Cassandra G Extavour
{"title":"Establishment of CRISPR/Cas9-based knock-in in a hemimetabolous insect: targeted gene tagging in the cricket Gryllus bimaculatus.","authors":"Yuji Matsuoka, Taro Nakamura, Takahito Watanabe, Austen A Barnett, Sayuri Tomonari, Guillem Ylla, Carrie A Whittle, Sumihare Noji, Taro Mito, Cassandra G Extavour","doi":"10.1242/dev.199746","DOIUrl":"10.1242/dev.199746","url":null,"abstract":"<p><p>Studies of traditional model organisms such as the fruit fly Drosophila melanogaster have contributed immensely to our understanding of the genetic basis of developmental processes. However, the generalizability of these findings cannot be confirmed without functional genetic analyses in additional organisms. Direct genome editing using targeted nucleases has the potential to transform hitherto poorly understood organisms into viable laboratory organisms for functional genetic study. To this end, we present a method to induce targeted genome knockout and knock-in of desired sequences in an insect that serves as an informative contrast to Drosophila, the cricket Gryllus bimaculatus. The efficiency of germline transmission of induced mutations is comparable with that reported for other well-studied laboratory organisms, and knock-ins targeting introns yield viable, fertile animals in which knock-in events are directly detectable by visualization of a fluorescent marker in the expression pattern of the targeted gene. Combined with the recently assembled and annotated genome of this cricket, this knock-in/knockout method increases the viability of G. bimaculatus as a tractable system for functional genetics in a basally branching insect.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":" ","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11829760/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142603764","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 : 2025-01-01Epub Date: 2025-01-07DOI: 10.1242/dev.203003
Yusuke Mori, Sierra Smith, Jiacheng Wang, Nadia Eliora, Kira L Heikes, Akankshi Munjal
{"title":"Versican controlled by Lmx1b regulates hyaluronate density and hydration for semicircular canal morphogenesis.","authors":"Yusuke Mori, Sierra Smith, Jiacheng Wang, Nadia Eliora, Kira L Heikes, Akankshi Munjal","doi":"10.1242/dev.203003","DOIUrl":"10.1242/dev.203003","url":null,"abstract":"<p><p>During inner ear semicircular canal morphogenesis in zebrafish, patterned canal-genesis zones express genes for extracellular matrix component synthesis. These include hyaluronan and the hyaluronan-binding chondroitin sulfate proteoglycan Versican, which are abundant in the matrices of many developing organs. Charged hyaluronate polymers play a key role in canal morphogenesis through osmotic swelling. However, the developmental factor(s) that pattern the synthesis of the matrix components and regulation of hyaluronate density and swelling are unknown. Here, we identify the transcription factor Lmx1b as a positive transcriptional regulator of hyaluronan, Versican, and chondroitin synthesis genes crucial for canal morphogenesis. We show that Versican regulates hyaluronan density through its protein core, whereas the charged chondroitin side chains contribute to the hydration of hyaluronate-containing extracellular matrices. Versican-tuned properties of hyaluronate matrices may be a broadly used mechanism in morphogenesis with important implications for understanding diseases in which these matrices are impaired, and for hydrogel engineering for tissue regeneration.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":" ","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11829767/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142799756","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}
{"title":"Fate specification triggers a positive feedback loop of TEAD-YAP and NANOG to promote epiblast formation in preimplantation embryos.","authors":"Naoki Hirono, Masakazu Hashimoto, Hiromi Shimojo, Hiroshi Sasaki","doi":"10.1242/dev.203091","DOIUrl":"10.1242/dev.203091","url":null,"abstract":"<p><p>In preimplantation embryos, epiblast (EPI) fate specification from the inner cell mass is controlled by the segregation of NANOG and GATA6 expression. TEAD-YAP interaction is activated during EPI formation and is required for pluripotency factor expression. These events occur asynchronously with similar timing during EPI formation, and their relationship remains elusive. Here, we examined the relationship between NANOG-GATA6 and TEAD-YAP. The nuclear accumulation of YAP takes place only in EPI-specified cells, and a positive feedback loop operates between NANOG and TEAD-YAP. The effects of TEAD-YAP on SOX2 upregulation in EPI-specified cells are likely indirect. EPI fate specification also alters the response of Nanog, Sox2 and Cdx2 to TEAD-YAP. These results suggest that EPI-fate specification alters the transcriptional network from the morula-like to the EPI-specified state and activates TEAD-YAP to trigger a positive feedback loop with NANOG, which stabilizes the EPI fate. The coordinated occurrence of these processes in individual cells likely supports proper EPI formation under the condition of asynchronous EPI-fate specification.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":" ","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142766599","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}
{"title":"Optogenetic control of cAMP oscillations reveals frequency-selective transcription factor dynamics in Dictyostelium.","authors":"Kensuke Yamashita, Kazuya Shimane, Tetsuya Muramoto","doi":"10.1242/dev.204403","DOIUrl":"10.1242/dev.204403","url":null,"abstract":"<p><p>Oscillatory dynamics and their modulation are crucial for cellular decision-making; however, analysing these dynamics remains challenging. Here, we present a tool that combines the light-activated adenylate cyclase mPAC with the cAMP biosensor Pink Flamindo, enabling precise manipulation and real-time monitoring of cAMP oscillation frequencies in Dictyostelium. High-frequency modulation of cAMP oscillations induced cell aggregation and multicellular formation, even at low cell densities, such as a few dozen cells. At the population level, chemotactic aggregation is driven by modulated frequency signals. Additionally, modulation of cAMP frequency significantly reduced the amplitude of the shuttling behaviour of the transcription factor GtaC, demonstrating low-pass filter characteristics capable of converting subtle oscillation changes, such as from 6 min to 4 min, into gene expression. These findings enhance our understanding of frequency-selective cellular decoding and its role in cellular signalling and development.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":" ","pages":""},"PeriodicalIF":3.7,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11829771/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142946434","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}