Steven J Chisolm, Emily Guo, Vignesh Subramaniam, Kyle D Schulze, Thomas E Angelini
{"title":"Transitions between cooperative and crowding-dominated collective motion in non-jammed MDCK monolayers.","authors":"Steven J Chisolm, Emily Guo, Vignesh Subramaniam, Kyle D Schulze, Thomas E Angelini","doi":"10.1016/j.cdev.2024.203989","DOIUrl":"10.1016/j.cdev.2024.203989","url":null,"abstract":"<p><p>Transitions between solid-like and fluid-like states in living tissues have been found in steps of embryonic development and in stages of disease progression. Our current understanding of these transitions has been guided by experimental and theoretical investigations focused on how motion becomes arrested with increased mechanical coupling between cells, typically as a function of packing density or cell cohesiveness. However, cells actively respond to externally applied forces by contracting after a time delay, so it is possible that at some packing densities or levels of cell cohesiveness, mechanical coupling stimulates cell motion instead of suppressing it. Here we report our findings that at low densities and within multiple ranges of cell cohesiveness, cell migration speeds increase with these measures of mechanical coupling. Our observations run counter to our intuition that cell motion will be suppressed by increasingly packing or sticking cells together and may provide new insight into biological processes involving motion in dense cell populations.</p>","PeriodicalId":29860,"journal":{"name":"Cells & Development","volume":" ","pages":"203989"},"PeriodicalIF":2.1,"publicationDate":"2024-12-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142872652","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The evolutionary origin and mechanism of chordate tail regeneration. An ancient tale?","authors":"Wouter Masselink, Prayag Murawala","doi":"10.1016/j.cdev.2024.203988","DOIUrl":"https://doi.org/10.1016/j.cdev.2024.203988","url":null,"abstract":"<p><p>Chordate tail regeneration represents the remarkable ability of some chordates to partially or completely regenerate a significant portion of their primary body axis. In this review we will discuss the chordate regenerative ability, what is known about the cellular sources which contribute to the regenerating tail, how various structures such as the spinal cord and vertebral column are re-established, and how scaling of the regenerating tail is regulated. Finally, we propose that tail regeneration is evolutionarily conserved and is fundamentally different from tail development however the origin and mechanism of this process remain elusive.</p>","PeriodicalId":29860,"journal":{"name":"Cells & Development","volume":" ","pages":"203988"},"PeriodicalIF":2.1,"publicationDate":"2024-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142872630","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Homeotic transformation of tail to limbs: A novel morphogenesis in the framework of self-organization and reprogramming of cell fate during appendage regeneration.","authors":"Jutshina Hota, Swetamudra Pattnaik, Gunanidhi Sahoo, Priyambada Mohanty-Hejmadi, Pravati Kumari Mahapatra","doi":"10.1016/j.cdev.2024.203987","DOIUrl":"https://doi.org/10.1016/j.cdev.2024.203987","url":null,"abstract":"<p><p>Homeotic transformation of tail to hindlimbs in anuran tadpoles is a manifestation of the reprogramming of positional information in the event of tail regeneration. Such discovery of homeosis is of particular interest considering its occurrence in a vertebrate under the influence of a morphogen which represents a self-organizing system in the context of developmental and regenerative studies. This article reviews homeotic transformation of tail to hindlimbs including pelvic girdles induced by retinoic acid (RA) /vitamin A palmitate during tail regeneration under the scope of self-organization and the role of blastema as an organizer. Next, we present a timeline of various findings in this context.</p>","PeriodicalId":29860,"journal":{"name":"Cells & Development","volume":" ","pages":"203987"},"PeriodicalIF":2.1,"publicationDate":"2024-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142872228","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Matyas Bubna-Litic, Guillaume Charras, Roberto Mayor
{"title":"Tissue mechanics modulate morphogen signalling to induce the head organiser.","authors":"Matyas Bubna-Litic, Guillaume Charras, Roberto Mayor","doi":"10.1016/j.cdev.2024.203984","DOIUrl":"10.1016/j.cdev.2024.203984","url":null,"abstract":"<p><p>Morphogenetic movements and specification of germ layers during gastrulation are key processes that establish the vertebrate body plan. Despite substantial research into the role of tissue mechanics during gastrulation and detailed characterisation of the molecular signalling networks controlling fate determination, the interplay of mechanical cues and biochemical signals during fate specification is poorly understood. Morphogens that activate Activin/Nodal/Smad2 signalling play a key role in mesoderm induction and axial patterning. We investigate the interplay between a single molecular input and a mechanical input using the well-established ex vivo system of Activin-induced explants of the mid-blastula X. laevis animal cap ectoderm. Activin alone induces mesoderm to form a complex elongating tissue with axial patterning, making this system similar to gastruloids generated in other model organisms. We observed an increase in the expression of dorsal mesoderm markers, such as chordin and goosecoid, and loss of elongation, in Activin-induced explants that were mechanically stimulated through uniaxial compression during the induction period. In addition, head mesoderm specific markers, including cerberus 1, were also increased. We show that mechanical stimulation leads to an increase in nuclear β-catenin activity. Activation of β-catenin signalling is sufficient to induce head Organiser gene expression. Furthermore, inhibition of β-catenin is sufficient to rescue the effect of compression on an early Wnt-signalling response gene siamois. Taken together these observations support the role of mechanical stimulation in modulating Activin-dependent mesoderm induction in favour of head Organiser formation. Given the conserved role of β-catenin in the dorsal specification and the dynamic morphogenetic movements of dorsal gastrula regions, mechanics-dependent Organiser induction may be found in other vertebrate species. Finally, the finding that mechanical cues affect β-catenin-dependent axial specification can be applied in the future development of more biologically relevant and robust synthetic organoid systems.</p>","PeriodicalId":29860,"journal":{"name":"Cells & Development","volume":" ","pages":"203984"},"PeriodicalIF":2.1,"publicationDate":"2024-12-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142781203","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Cells & DevelopmentPub Date : 2024-12-01Epub Date: 2024-08-05DOI: 10.1016/j.cdev.2024.203943
Yi Ying Cheok, Grace Min Yi Tan, Yee Teng Chan, Suhailah Abdullah, Chung Yeng Looi, Won Fen Wong
{"title":"Podoplanin and its multifaceted roles in mammalian developmental program.","authors":"Yi Ying Cheok, Grace Min Yi Tan, Yee Teng Chan, Suhailah Abdullah, Chung Yeng Looi, Won Fen Wong","doi":"10.1016/j.cdev.2024.203943","DOIUrl":"10.1016/j.cdev.2024.203943","url":null,"abstract":"<p><p>Podoplanin is a vital molecule which plays an integral part in the regulation of development, immunity, and cancer. Expression of Podoplanin is detected at different early developmental stages of mammalian embryo, and it functions to modulate morphogenesis of various organ systems. In experimental animal models of different genetic backgrounds, absence of Podoplanin results in either embryonic lethality or immediate death upon birth, suggesting the importance of the gene in early developmental processes. This review discusses the gene and protein structure of Podoplanin; and elucidates various functions of Podoplanin in different systems, including central nervous system as well as respiratory, lymphatic, and cardiovascular systems.</p>","PeriodicalId":29860,"journal":{"name":"Cells & Development","volume":" ","pages":"203943"},"PeriodicalIF":2.1,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141903106","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Cells & DevelopmentPub Date : 2024-12-01Epub Date: 2024-08-14DOI: 10.1016/j.cdev.2024.203964
Anuraag Bukkuri, Frederick R Adler
{"title":"Of criminals and cancer: The importance of social bonds and innate morality on cellular societies.","authors":"Anuraag Bukkuri, Frederick R Adler","doi":"10.1016/j.cdev.2024.203964","DOIUrl":"10.1016/j.cdev.2024.203964","url":null,"abstract":"<p><p>The current dogma in cancer biology contends that cancer is an identity problem: mutations in a cell's DNA cause it to \"go rogue\" and proliferate out of control. However, this largely ignores the role of cell-cell interaction and fails to explain phenomena such as cancer reversion, the existence of cancers without mutations, and foreign-body carcinogenesis. In this proof-of-concept paper, we draw on criminology to propose that cancer may alternatively be conceptualized as a relational problem: Although a cell's genetics is essential, the influence of its interaction with other cells is equally important in determining its phenotype. We create a simple agent-based network model of interactions among normal and cancer cells to demonstrate this idea. We find that both high mutation rates and low levels of connectivity among cells can promote oncogenesis. Viewing cancer as a breakdown in communication networks among cells in a tissue complements the gene-centric paradigm nicely and provides a novel perspective for understanding and treating cancer.</p>","PeriodicalId":29860,"journal":{"name":"Cells & Development","volume":" ","pages":"203964"},"PeriodicalIF":2.1,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141996584","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Polina S Timoshina, Alexey M Nesterenko, Elena A Parshina, Eugeny E Orlov, Fedor M Eroshkin, Andrey G Zaraisky
{"title":"Dissecting the mystery of embryonic scaling: The Scalers Hypothesis and its confirmation in sea urchin embryos.","authors":"Polina S Timoshina, Alexey M Nesterenko, Elena A Parshina, Eugeny E Orlov, Fedor M Eroshkin, Andrey G Zaraisky","doi":"10.1016/j.cdev.2024.203972","DOIUrl":"https://doi.org/10.1016/j.cdev.2024.203972","url":null,"abstract":"<p><p>Embryonic scaling, the ability of embryos to regulate their spatial structure in proportion to size, remains a fascinating yet poorly studied problem in developmental biology. First described in sea urchin embryos by Hans Driesch, this phenomenon is now recognized as a striking example of how living organisms use non-equilibrium self-organization, based on reaction-diffusion (RD) systems, to generate pattern-determining morphogen concentration gradients that scale with size. Although specific molecular mechanisms for scaling such gradients have been described in some cases, a general approach for the targeted identification of such mechanisms had not been developed until recently. In search of a solution, we hypothesized the obligatory participation in scaling mechanisms of special genes, which we named \"scalers.\" We supposed that these genes share two critical features: their expression is sensitive to embryo size, and their protein products determine the scale of morphogen concentration gradients. As proof of principle, we recently identified scalers by detecting differentially expressed genes in wild-type and half-size Xenopus laevis gastrula embryos. Furthermore, we described a mechanism by which one of the identified scalers, the gene encoding Metalloproteinase 3 (Mmp3), regulates the scaling of gradients of the morphogenic protein Bmp and its antagonists, Chordin and Noggin1/2. In the present work, we have made an important theoretical generalization of the Scalers Hypothesis by proving a statement regarding the obligatory presence of scalers in closed RD systems generating morphogen concentration gradients. Furthermore, through a systematic analysis of all known types of embryonic scaling models based on RD systems, we demonstrate that scalers are present in all known types of such models, either explicitly or implicitly. Finally, to test the universality of the Scalers Hypothesis, we applied our method to identify scalers that adjust Bmp/Chordin gradients to the size of the sea urchin embryo, Strongylocentrotus droebachiensis. Our results show that at least two members of the gene cluster encoding astacin metalloproteinases of the Span family, namely bp10 and Span, exhibit properties characteristic of scalers. Namely, their expression levels increase significantly in half-size embryos, and their protein products specifically degrade Chordin. Additionally, we found that the loss of function of bp10 and span leads to a narrowing of the dorsal domain of the Bmp signaling nuclear effector, pSmad1/5. These findings not only validate the Scalers Hypothesis but also uncover a novel mechanism by which Span proteinases fine-tune Chordin and Bmp morphogen concentration gradients in sea urchins. Thus, the Scalers Hypothesis and the approach to targeted search for such genes developed on its basis open up promising avenues for future research into scaling mechanisms in various biological systems.</p>","PeriodicalId":29860,"journal":{"name":"Cells & Development","volume":" ","pages":"203972"},"PeriodicalIF":2.1,"publicationDate":"2024-10-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142509381","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"'Three signals - three body axes' as patterning principle in bilaterians.","authors":"Christof Niehrs, Ettore Zapparoli, Hyeyoon Lee","doi":"10.1016/j.cdev.2024.203944","DOIUrl":"10.1016/j.cdev.2024.203944","url":null,"abstract":"<p><p>In vertebrates, the three orthogonal body axes, anteroposterior (AP), dorsoventral (DV) and left-right (LR) are determined at gastrula and neurula stages by the Spemann-Mangold organizer and its equivalents. A common feature of AP and DV axis formation is that an evolutionary conserved interplay between growth factors (Wnt, BMP) and their extracellular antagonists (e.g. Dkk1, Chordin) creates signaling gradients for axial patterning. Recent work showed that LR patterning in Xenopus follows the same principle, with R-spondin 2 (Rspo2) as an extracellular FGF antagonist, which creates a signaling gradient that determines the LR vector. That a triad of anti-FGF, anti-BMP, and anti-Wnt governs LR, DV, and AP axis formation reveals a unifying principle in animal development. We discuss how cross-talk between these three signals confers integrated AP-DV-LR body axis patterning underlying developmental robustness, size scaling, and harmonious regulation. We propose that Urbilateria featured three orthogonal body axes that were governed by a Cartesian coordinate system of orthogonal Wnt/AP, BMP/DV, and FGF/LR signaling gradients.</p>","PeriodicalId":29860,"journal":{"name":"Cells & Development","volume":" ","pages":"203944"},"PeriodicalIF":2.1,"publicationDate":"2024-08-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141914182","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Self-organization underlies developmental robustness in plants.","authors":"Shuyao Kong, Mingyuan Zhu, Adrienne H K Roeder","doi":"10.1016/j.cdev.2024.203936","DOIUrl":"10.1016/j.cdev.2024.203936","url":null,"abstract":"<p><p>Development is a self-organized process that builds on cells and their interactions. Cells are heterogeneous in gene expression, growth, and division; yet how development is robust despite such heterogeneity is a fascinating question. Here, we review recent progress on this topic, highlighting how developmental robustness is achieved through self-organization. We will first discuss sources of heterogeneity, including stochastic gene expression, heterogeneity in growth rate and direction, and heterogeneity in division rate and precision. We then discuss cellular mechanisms that buffer against such noise, including Paf1C- and miRNA-mediated denoising, spatiotemporal growth averaging and compensation, mechanisms to improve cell division precision, and coordination of growth rate and developmental timing between different parts of an organ. We also discuss cases where such heterogeneity is not buffered but utilized for development. Finally, we highlight potential directions for future studies of noise and developmental robustness.</p>","PeriodicalId":29860,"journal":{"name":"Cells & Development","volume":" ","pages":"203936"},"PeriodicalIF":2.1,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11688513/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141499169","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Yagmur Azbazdar, Edgar M Pera, Edward M De Robertis
{"title":"Head organizer: Cerberus and IGF cooperate in brain induction in Xenopus embryos.","authors":"Yagmur Azbazdar, Edgar M Pera, Edward M De Robertis","doi":"10.1016/j.cdev.2023.203897","DOIUrl":"10.1016/j.cdev.2023.203897","url":null,"abstract":"<p><p>Neural induction by cell-cell signaling was discovered a century ago by the organizer transplantations of Spemann and Mangold in amphibians. Spemann later found that early dorsal blastopore lips induced heads and late organizers trunk-tail structures. Identifying region-specific organizer signals has been a driving force in the progress of animal biology. Head induction in the absence of trunk is designated archencephalic differentiation. Two specific head inducers, Cerberus and Insulin-like growth factors (IGFs), that induce archencephalic brain but not trunk-tail structures have been described previously. However, whether these two signals interact with each other had not been studied to date and was the purpose of the present investigation. It was found that Cerberus, a multivalent growth factor antagonist that inhibits Nodal, BMP and Wnt signals, strongly cooperated with IGF2, a growth factor that provides a positive signal through tyrosine kinase IGF receptors that activate MAPK and other pathways. The ectopic archencephalic structures induced by the combination of Cerberus and IGF2 are of higher frequency and larger than either one alone. They contain brain, a cyclopic eye and multiple olfactory placodes, without trace of trunk structures such as notochord or somites. A dominant-negative secreted IGF receptor 1 blocked Cerberus activity, indicating that endogenous IGF signals are required for ectopic brain formation. In a sensitized embryonic system, in which embryos were depleted of β-catenin, IGF2 did not by itself induce neural tissue while in combination with Cerberus it greatly enhanced formation of circular brain structures expressing the anterior markers Otx2 and Rx2a, but not spinal cord or notochord markers. The main conclusion of this work is that IGF provides a positive signal initially uniformly expressed throughout the embryo that potentiates the effect of an organizer-specific negative signal mediated by Cerberus. The results are discussed in the context of the history of neural induction.</p>","PeriodicalId":29860,"journal":{"name":"Cells & Development","volume":" ","pages":"203897"},"PeriodicalIF":3.9,"publicationDate":"2023-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138810532","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}