São Paulo School of Advanced Science in Stem Cell Biology Sept 16-24 Ribeirão Preto, Brazil With the FAPESP / May Rubião SPSAS on Stem Cell Biology, we intend to make a qualitative leap in bringing together national and international scientists to promote stem cell research among graduate students and young researchers. The goal of this program is to encourage more interest in and research on stem cells and closing the gap between fundamental and applied research focused on stem cell therapy and tissue bioengineering.
The partnership that we established with the International Society for Stem Cell Research (ISSCR) to carry out the SPSAS on Stem Cell Biology and the course-ending international symposium will encourage more interest in and research on stem cells so that the participants can continue to play a significant global role in advancing this field.
Undergraduate, graduate students, and post-doctoral fellows from all countries are encouraged to apply.
The Selection Committee will select 100 participants (50 from all states of Brazil and 50 international) to be fully funded by the FAPESP SPSAS Program. Funding includes travel, travel insurance (for international participants only), accommodation, and meals throughout the event. Application deadlines and selection criteria: https://www.sbbc.org.br/spsas-stemcellbiology/application/
Doing great science depends on teamwork, whether this is within the lab or in collaboration with other labs. However, sometimes the resources that support our work can be overlooked. Our ‘Featured resource’ series aims to shine a light on these unsung heroes of the science world. In our latest article, we hear from Cheryl Telmer, who describes the work of Echinobase.
Overview
Echinobase (www.echinobase.org) is a model organism knowledgebase for the echinoderm research community (Arshinoff et al. 2022). The Phylum Echinodermata has 5 Classes: the basal branching Crinoidea (crinoids), and the 4 motile Eleutherozoa Classes including Asterozoa, composed of the Ophiuroidea (brittle stars) and Asteroidea (starfish) and the Echinozoa, composed of the Echinoidea (sea urchins and sand dollars) and Holothuroidea (sea cucumbers). Echinoderms, along with the phyla Chordata and Hemichordata are Deuterostomes. The species used in research labs have many advantages for studying embryo development and regeneration including an abundance of gametes, synchronized fertilization, transparent embryos and larvae, ease of microinjection and micromanipulation, and variation in development within and between a species. This has made echinoderms a premier model system to study gene regulation, genomic control of cell specification and gene regulatory networks in development and evolution.
Echinobase is the third generation computational resource for the support of all genomic data and research using echinoderm model organisms.
The Echinobase Teams
Echinobase has been developed from previous databases including SpBase (previously funded by NIH R01 to PI Andy Cameron, 2007-2012) and EchinoBase (NIH P41 to PI Cameron, 2012-2018). Echinobase development is now funded through a collaborative NIH P41 between Carnegie Mellon University (PIs Hinman/Ettensohn) and the University of Calgary (PI Vize). The database and software development team are in Calgary and also run the Xenopus knowledgebase, Xenbase. The data curation and bioinformatics team are at Carnegie Mellon University, where the PIs are leading researchers in the echinoderm research community. The current Echinobase is a clone of Xenbase which has adapted multiple new features and content in support of the echinoderm community, and broader needs of the developmental biology communities.
Support for Genomics Research
The most current genome assemblies are hosted on Echinobase. Currently four species are fully supported, Strongylocentrotus purpuratus (purple sea urchin), Lytechinus variegatus (variegated sea urchin), Patiria miniata (bat star) and Acanthaster planci (Crown of Thorns sea star). Partial support (BLAST and JBrowse) is provided for Asterias rubens (sugar star) and Anneissia japonica (feather star, a crinoid). Search and BLAST tools are available on the landing page or through the over 38,000 gene pages. Gene pages also display gene model HGNC compliant names, multispecies orthology, GO terms, a link to the JBrowse genome browser, and a gene expression plotting tool. Tabs beyond the summary on the gene page provide gene specific literature, transcripts, expression data, protein sequences, interactants and more.
The Echinoderm Anatomical Ontology
The Echinoderm Anatomical Ontology (ECAO) describes echinoderm anatomy and embryological development using a controlled vocabulary of anatomy terms and developmental stages that are organized in a hierarchy with a graphical structure. Echinobase curators use ECAO terms to describe the spatiotemporal expression patterns of endogenous gene products, the transcriptional activity of cis-regulatory modules, the effects of morpholinos, and other types of biological information. The ECAO is constantly being updated in response to the latest published echinoderm research.
The ECAO contains 1000’s of terms and relationships. Each anatomical system (e.g. nervous system, skeletal system), tissue and structure (e.g. ciliary band, mesoderm, blastopore) and many cell types (e.g. pigment cell, serotonergic neuron, skeletogenic mesenchyme cell) are separate terms; each term is fully defined and related to other terms by is_a, part_of, develops_from and develops_into relationships. The ontology makes text and data computer readable and allows our code to link and infer relationships between many different types of content.
Manual and Automated Curation
Automated literature collection has retrieved over 18,000 publications for automated and manual curation. Text matching automatically links gene symbols or names appearing in manuscript text to gene pages. Manual curation extracts sequence information for morpholinos, gRNAs, and cis-regulatory elements and itemizes antibodies used in experiments.
Sharing on EchinoWiki and FTP
To support the community, collections of data, protocols and other resources are shared using EchinoWiki and an FTP site. To enable interdisciplinary and collaborative studies, contact information for community members and groups and information about their research are available and searchable.
Help from users
The echinoderm research community has always been extremely supportive and can continue to do so at many levels. It is highly important and appreciated if users cite Echinobase whenever possible in articles, presentations and funding applications (citation link in the top right corner of the webpage “Citing Echinobase”). These acknowledgements make Echinobase’s impact on research more tangible and specifically the article citations provide metrics that can be used for funding applications.
Help from authors
Authors can also contribute in several ways to simplify the curation of their articles, ultimately allowing their data to be more quickly available on the website.
When you write your paper…
In addition to “Citing Echinobase”, clear, detailed and accurate descriptions of the experiments and resources minimizes the curation effort and reduces the need to contact the authors. Articles should mention official Echinobase identifiers and nomenclature for entities such as genes, alleles, and anatomical structures.
Bibliography
Arshinoff BI, Cary GA, Karimi K, Foley S, Agalakov S, Delgado F, Lotay VS, Ku CJ, Pells TJ, Beatman TR, Kim E, Cameron RA, Vize PD, Telmer CA, Croce J, Ettensohn CA, Hinman VF, Echinobase: leveraging an extant model organism database to build a knowledgebase supporting research on the genomics and biology of echinoderms, Nucleic Acids Research, Volume 50, Issue D1, 10.1093/nar/gkab1005
We loved Ewan St. John Smith’s tweet about the Chronophage clock that can be found in our home city, Cambridge. With Ewan’s permission, we have reproduced most of the thread celebrating the birthday of the clock’s inventor, Dr John C Taylor OBE, but you can also find the tweetorial on Twitter.
Today (25 November) marks a special day in the annual rhythm of the Corpus Chronophage Clock.
I (Ewan St. John Smith) am a Fellow in Pharmacology at Corpus Christi College, Cambridge, teaching medicine & biology, but I am also the Custodian of the Corpus Chronophage Clock. One of my jobs is to give tours of the Clock on College feast day but, today there is a need for a virtual tour.
A tour of the clock. Image credit: Fiona Gilsenan
The Clock sits on what used to be the entrance to a Natwest Bank, a building built in 1866 (architect Horace Francis) that originally housed the London County Bank. Natwest’s lease ended in 2005. The College needed better library provision for students. The then library was situated under the Parker Library and moving students out meant better facilities for students/researchers to access the Parker. However, the old entrance to Natwest couldn’t just be bricked up due to planning restrictions. What to do? That’s where inventor & alumnus Dr John C Taylor OBE comes in. Inventor of the bimetallic thermostat control present in electric kettles (http://johnctaylor.com), John is also an horologist & designed the Corpus Chronophage Clock that was built by Huxley Bertram.
But this is no ordinary clock. The escapement wheel is made from a single sheet of steel, plated in gold, created by a series of explosions in a vacuum, the radiating ripples that this has created allude to the Big Bang & the clock was inaugurated in 2008 by Stephen Hawking. Atop the wheel sits the Chronophage (time eater). It is an example of the grasshopper escapement mechanism invented by John Harrison in the 1700s. The Chronophage’s mouth opens at 30 sec past each minute, snapping shut when the minute is over: time passes & we all die.
Video credit: Ewan St. John Smith
When the hour is struck, there is no chiming of bells, but rather the rustling of chains & a hammer strikes a wooden coffin to sound out the passing of another hour – perhaps a little off putting for those studying in the library behind the clock! To tell the time, there are 3 LED wheels (2736 LEDs) to show seconds, minutes & hours, but this clock can play tricks…
Behind the clock face. Image courtesy of Corpus Christi College and Ewan S.t John Smith
Because our perception of time is always altered by what is going on & the clock’s trickery adds to that. In this video the clock is behaving…
Video credit: Ewan St. John Smith
But here the clock is playing tricks, watch the pendulum in this video! The clock has 50 tricks, a special set is reserved for 4 special days: John Harrison’s birthday (March 24th), John Taylor’s birthday (Nov. 25th – today 🥳), New Year’s Day & Corpus Christi Day.
Video credit: Ewan St. John Smith
When playing these tricks, the clock gets a little out of time, but have no fear, it can run 10% fast & 90% slow, thus enabling a rapid realignment. This ability also enables the clock to cope with the clocks going forwards/backwards. (For fun, here are more tricks!)
Video credit: Ewan St. John Smith
The pendulum has an inscription. Joh = Johannes = John; Sarto = Taylor, Monan = Monanensis = Isle of Man, Inv. = Invenit = to create, MMVIII = 2008: John Taylor from the Isle of Man made this in 2008. There are 10 peaks on the rhodium dish at the bottom that can be pointed at by the pendulum when playing certain tricks, a further homage to John Harrison and the accuracy achieved with his clocks centuries ago!
And of course, like all good clocks, there is a key, but this one is purely ceremonial. When spun, the key tells you to which clock it belongs & top left is the image of the bimetallic thermostat for the kettle!
The Chronophage has proved inspirational, perhaps most recently in research from Andrea Brand’s lab where they identified a temporal transcription factor in Drosophila that they named Chronophage in view of its role in regulating neurogenesis
Model of Chronophage (Cph) function in the NB7-1 lineage from Fox, et al.
So, that’s a little overview of what is truly an incredible thing, slap bang in the middle of Cambridge for everyone to see with plenty more secrets to share, all of which are courtesy of the man whose birthday it is today, Dr John C Taylor OBE.
We developed a Shiny App to explore our latest scRNAseq dataset of the E12.5 mouse hem and choroid plexus. You can access it here. It comes as a complement to our previous App focusing on the ventral, lateral and dorsal pallium.
Two complementary Shiny Apps to explore cell diversity in the developing mouse telencephalon
Image provided by the MRC National Mouse Genetics Network. For permission to reproduce, contact the MRC National Mouse Genetics Network.
The September issue of our journal Disease Models & Mechanisms (DMM) has a focus on how researchers can best leverage model organisms to improve our understanding of human health and disease. Here, we highlight some of the articles and encourage you to visit the journal website, where all the articles are available to read Open Access.
The issue includes a Special Article by Keith Cheng, Hugo Bellen and colleagues on the importance of promoting validation and cross-phylogenetic integration in model organism research. The article draws on a discussion series organised by the National Institutes of Health (NIH) to gather opinions on how researchers can further extend the utility of model organisms in the future. The authors discuss some of the key ideas identified by the NIH discussions, including:
Developing new tools and technologies. Ideas include humanising model organisms to better model human diseases, generating reference atlases to allow comparison between model organism and human data, and developing new reagents such as species-specific antibodies.
Broadening the range of model organism species used in research. Different species offer specific advantages for modelling human disease. For example, hamsters share similar lung physiology to humans so have proved useful in COVID-19 studies. Expanding the range of species used in disease research could therefore offer researchers greater access to useful models that have been previously overlooked or underused.
Increasing genetic variation. Laboratory animal strains are often inbred to reduce variation. However, humans have a great deal of genetic diversity, so it will be important to use a suite of diverse models to better reflect the variation in human disease.
Integration between different disciplines and organisms. It will be important to integrate phenotypic data from different disciplines (such as biochemistry, cell biology, genomics and behavioural studies) as well as data from studies in different model organism species. This will help to form a more complete picture of the disease phenotype.
Owen Sansom, Director of the Cancer Research UK Beatson Institute and the MRC National Mouse Genetics Network.
An example of a new initiative that aims to improve integration across disciplines is the UK Medical Research Council (MRC) National Mouse Genetics Network. You can read more about this in Owen Sansom’s Editorial. Owen explains that the Network will comprise seven research clusters, each focusing on different yet complementary research areas. The aim is to share data, techniques and resources, and to encourage collaboration within the mouse model community.
A figure from the JAX group’s paper showing tumour growth in a human leukaemia xenograft over time in three different host mouse strains (blue, green, black). Tumour size (measured using bioluminescence) is shown on the y-axis, with time in days marked on the x-axis. The results show that the NR strain (blue) supports the most extensive tumour growth.
The September issue of DMM also contains a study from Muneer Hasham and colleagues at the Jackson Laboratory (JAX), USA, which expands the genetic diversity of mouse models available for xenografting experiments. Xenografting human cancer cells in mice is a well-established method for studying tumour development and testing potential therapeutic drugs. These mice must lack B- and T-lymphocytes for xenografting to be successful, and researchers can achieve this by generating mouse strains that are Rag1 deficient. However, the genetic diversity of available Rag1-/- mouse strains is limited.
In their paper, the JAX group generate five genetically diverse Rag1-/- mouse strains. Together, these strains cover 90% of the known allelic diversity in the mouse genome. They show that the genetic background of the host strain plays an important role in the outcome of the xenograft; for example, they find that tumour size varies between the five different host strains. This article was also highlighted as the DMM Editor’s Choice.
You can read a response to the work by Dr Hasham and colleagues in the same issue of DMM, where Ryan Devlin and Ed Roberts tackle the question of how researchers can build a healthy mouse model system to better interrogate cancer biology. Taking the JAX lab paper as a case study, they suggest implementing a ‘Swiss cheese model’ to design better experiments. This model is already used in accident prevention strategies, where the concept of layering multiple strategies (each with their own weaknesses, as represented by holes in the slice of cheese) is employed to reduce the chance of an accident.
An individual model can be represented as a slice of Swiss cheese (A), where the holes represent limitations that might cause failure of a potential treatment in a clinical trial. As models are refined, these holes become smaller (B), and increasing the genetic diversity of the model increases the size of the slice (C). Layering multiple models (D) can allow researchers to prevent misleading results that may be influenced by a limitation in one model.
This figure from the JAX Perspective illustrates key strategies for improving translation of animal models. These include establishment of common research standards, use of diverse genetic backgrounds within a species, requiring adequate statistical power and better access to public databases to facilitate meta-analyses of multi-omics data.
In a similar vein, Ryan and Ed suggest that researchers can layer a suite of different mouse models, rather than trying to identify the ‘best’ model. This is because each model has its own weaknesses so, by combining models that complement one another, scientists can reduce the chances of a harmful or ineffective chemotherapeutic drug reaching the clinical trial stage.
Finally, researchers from JAX have also provided a Perspective for the October issue of DMM. In the article, Karen Svenson and colleagues respond to the NIH’s 2021 recommendations to improve the reproducibility of animal studies. They share their own experiences of addressing this issue, with a specific focus on mouse models.
Want to keep up with the latest news from DMM? Visit the DMM website and follow the journal on Twitter and/or Mastodon to find out more.
“We’re testing the air for tigers and digging up dead bodies as we explore the exciting new field of environmental DNA”
Dr Sally Le Page
In the latest episode of the Genetics Unzipped podcast, we’re testing the air for tigers and digging up dead bodies as we explore the exciting new field of environmental DNA. Dr Sally Le Page chats with Prof. Elizabeth Clare about sampling the DNA of rare species from the air, and Dr Kirstin Meyer-Kaiser and Charles Konsitzke tells us about their project using eDNA to recover the missing bodies of fallen service personnel.
By Zoe Mann, Ahmed Mahmoud, Ana Rita Diogo Robelo and Neha Agrawal
Hidden away in the beautiful countryside, a group of scientists gathered at Buxted Park to brainstorm the roles of metabolism in the developmental origins of health and disease (DOHaD). In this peaceful setting, early career researchers (ECRs) had the opportunity to network and exchange ideas with leaders in their respective fields. Being one of the first in-person workshops since the pandemic, energy levels and excitement were high.
The program, which was well organized by Alex Gould and Sally Dunwoodie, was filled with interdisciplinary presentations and stimulating, fruitful discussions between scientists, which continued throughout the day over lunch, coffee breaks, long leisurely walks and well into the evening over dinner and drinks. The venue and small size of the Workshop promoted engagement between participants in a way that is not possible at larger scientific meetings. Also, attendees were encouraged to present unpublished data, which prompted useful and interesting discussions about the most recent advances in DOHaD. For the majority, this workshop bore new collaborations, ideas and friendships.
Throughout the week, we listened to outstanding talks exploring the role of developmental metabolism in worms, flies, xenopus, birds, mice and humans. The interdisciplinary nature of this Workshop revealed that regardless of the model system and field of study pursued by the participating scientists, a common theme remained consistent, which is the importance of the DOHaD in their respective fields. Furthermore, it was fascinating and refreshing to hear many works that bridge together transcriptomics, proteomics and metabolomics for a comprehensive understanding of how genetics, nutrition and environment can modulate metabolism and, consequently, development. For example, metabolic disruptions in the placenta can have a defining role in disease manifestation in multiple organs later in life. Similarly, early exposure to hypoxia during development can have lasting detrimental metabolic effects on offspring. Understanding these processes is therefore informative not only for developmental biology, but also for informing clinical research and public health policy.
A ‘hot topics’ discussion on the penultimate day was helpful in identifying important ideas and focus areas for further development in this field. The role of cutting-edge technologies, such as spatial metabolomics and assessing metabolomes at single cell resolution, was highlighted. In particular, the need to communicate the importance of DOHaD in both research and clinical settings was strongly emphasized throughout the meeting. Indeed, broadening our view will allow the scientific community to acknowledge that, not only the genetic background, but also the metabolic state of an organism, can be associated with and even drive developmental defects or tumorigenesis. Additionally, a major conclusion from the Workshop was the need to advocate for increased awareness of DOHaD, even amongst developmental biologists.
In this focused setting, the friendly environment and small community inspired new interdisciplinary research aimed at uncovering the mechanistic links between early-life metabolism and adult health and disease. Should the chance to take part in one of these Company of Biologists Workshops arise, do not hesitate to apply. You will hear about cutting-edge research, build new and inspiring collaborations, network with leaders in the field and, above all, have fun.
Developmental metabolism and the origins of health and disease Workshop (2 votes) Loading...
In the past couple of weeks, #ScienceTwitter was full of tweets starting with ‘If Twitter ends today, can we all agree that…’, professing their love for a particular model organism, and whether qPCR is essential for validation! Of course, Twitter hasn’t collapsed but the #devbio community, including ourselves, have been trying Mastodon as an alternative. Read on to find out some of the talking points that caught our attention.
To move or not to move?
Question: what is the trigger point at which we should all leave Twitter? Maybe when it functions as a platform upon which the amount of disinformation amplified exceeds the amount of information? Has that just happened?
We’re at @the_node@mstdn.science, and we’re still building our community on Mastodon, but below are some of our favourites so far. Let us know who we should be adding to our list!
We have just released Mastodon beta-26. This release sums the work of the past 2 years and results in major changes in feature for the users. I describe some of the new features below, but for more info, check https://t.co/6etC6mVmBcpic.twitter.com/NfNv1152se
Investigating the rules of cell-to-cell interaction during pre-somitic mesoderm elongation
I discovered the field of developmental biology through independent reading during the first year of my undergraduate biomedical sciences program. I was fascinated by the process through which embryos develop, and the more I learned, the more questions I had. As Lewis Wolpert said, “Understanding the process of development in no way removes that sense of wonder”. I knew I wanted to gain some experience in working with embryos and I had the amazing opportunity to work in Ben Steventon’s lab at the Department of Genetics, University of Cambridge.
During development, cells interact with one another to generate collective migration. For example, cranial neural crest cells counterbalance contact inhibition of locomotion and coattraction to migrate through the embryo (Carmona-Fontaine et al., 2009; Carmona-Fontaine et al., 2011). The interactions between the cells of the pre-somitic mesoderm during vertebrate elongation are not understood as well. I focused on investigating the behaviour of the medial somite progenitor (MSP) population, using chick embryos as a model system.
I started by taking stage HH4 chick embryos out of eggs and placing them in PBS. Using a small syringe needle I then explanted the MSP region, which is located in the anterior primitive streak just below Hensen’s node. I transferred each explant on a dish coated with fibronectin and I imaged them every 10 minutes for 20 hours. After watching how the cells migrate in the dish (figure 1, movie 1), I wanted to find out how different explants would interact. I decided to culture two explants from the same region (anterior streak) next to each other, as well as an explant from the anterior region and an explant from the posterior region.
Figure 1 – Migration of cells from the MSP region, imaged at 10x for 20 hours.
Movie 1 – Migration of cells from the MSP region, imaged at 10x for 20 hours
Surprisingly, in both situations, the cells did not mix. The anterior streak explants attracted each other in some cases (figure 2, movie 2), while the posterior streak explant seemed to be attracted by the anterior streak explant (figure 3, movie 3). There is no significant difference between the average timing of migration onset in anterior and posterior explants (figure 4A). To measure the rate of migration, I calculated the rate of change of diameter, and again there was no significant difference between the two populations (figure 4B). The attraction is not likely to be influenced by the distance, as there is no significant difference between the mean initial distance separating the explants in the cases where attraction occurs or does not. However, there seems to be a weak positive correlation between the initial size of the explant with the rate of migration. Explants with a larger initial diameter generally have a greater rate of change of diameter. This is true for both anterior explants (figure 4C) and posterior explants (figure 4D).
Figure 2 – Two anterior streak explants from different embryos cultured together, imaged at 10x for 20 hours. The explants attract each other; however, the cells do not mix.
Movie 2 – Two anterior streak explants from different embryos cultured together, imaged at 10x for 20 hours.
Figure 3 – Anterior streak explant (unlabelled) and posterior streak explant (GFP) from different embryos cultured together, imaged at 10x for 20 hours. The posterior explant is attracted by the anterior explant; however, the cells do not mix.
Movie 3 – Anterior streak explant (unlabelled) and posterior streak explant (GFP) from different embryos cultured together, imaged at 10x for 20 hours.
Figure 4 – Features of migration
A – Mean timing of migration onset in anterior and posterior streak explants. A T test was performed, and there is no significant difference between the onset of migration (p = 0.529).
B – Mean rate of change of diameter of posterior and anterior explants. A T test was performed, and there is no significant difference between the rate of change of diameter (p = 0.819).
C – Variation of the rate of change of diameter against initial diameter in anterior streak explants. There is a positive correlation between the initial diameter and the rate of change of diameter.
D – Variation of the rate of change of diameter against initial diameter in posterior streak explants. There is a positive correlation between the initial diameter and the rate of change of diameter.
I had an amazing experience working in the lab. Initially, I found it tricky to remove the embryos out of the egg and explant the region. I ended up breaking a few embryos and losing some explants. However, practicing the techniques every day helped me improve quickly. Each week I got more and more comfortable doing my experiments and my movies have significantly improved. The people in the lab were very friendly and always happy to help, so I had great support throughout my placement. I enjoyed the lab environment and the weeks passed by incredibly quickly. If I had more time, I would have liked to investigate the role of FGF signalling in the migration of these cells. I would have liked to inhibit FGF receptors to find whether the explants still attract or not, since streak cells are attracted by FGF4 and repelled by FGF8 (Yang et al., 2002). However, there seems to be more FGF8 and less FGF4 in the MSP region (Lawson et al., 2001; Shamim and Mason, 1999), so the fact that the explants attract seems to oppose this evidence.
I am interested in pursuing a PhD and my experience from this summer has only made me more determined. I gained valuable insights into the reality of working in research. I had encountered some difficulties with my experiments and spent some time troubleshooting, however that did not put me off. Moreover, it made the results so much more rewarding, giving me a realistic view of what it is like to start a new project and how long experiments take. I appreciate the freedom I had in deciding which experiments to perform, how I would analyse the data, and the general structure of my day.
I think everybody who is curious about research should apply for a BSDB summer studentship. There is nothing like experiencing research first-hand. I would like to thank Ben for hosting me in his lab, Tim for encouraging me to apply for this scheme in the first place, and everybody in the lab for teaching me various skills and being patient with me.
References
Carmona-Fontaine, C., Matthews, H., Kuriyama, S., Moreno, M., Dunn, G., Parsons, M., Stern, C. and Mayor, R., 2008. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature, 456(7224), pp.957-961.
Carmona-Fontaine, C., Theveneau, E., Tzekou, A., Tada, M., Woods, M., Page, K., Parsons, M., Lambris, J. and Mayor, R., 2011. Complement Fragment C3a Controls Mutual Cell Attraction during Collective Cell Migration. Developmental Cell, 21(6), pp.1026- 1037.
Lawson, A., Colas, J. and Schoenwolf, G., 2001. Classification scheme for genes expressed during formation and progression of the avian primitive streak. The Anatomical Record, 262(2), pp.221-226.
Shamim, H. and Mason, I., 1999. Expression of Fgf4 during early development of the chick embryo. Mechanisms of Development, 85(1-2), pp.189-192.
Wolpert, L., 2008. The triumph of the embryo. Mineola, N.Y.: Dover Publications, p.199.
Yang, X., Dormann, D., Münsterberg, A. and Weijer, C., 2002. Cell Movement Patterns during Gastrulation in the Chick Are Controlled by Positive and Negative Chemotaxis Mediated by FGF4 and FGF8. Developmental Cell, 3(3), pp.425-437.
Epithelial Outgrowth Through Mesenchymal Rings Drives Alveologenesis Nicholas M. Negretti, Yeongseo Son, Philip Crooke, Erin J. Plosa, John T. Benjamin, Christopher S. Jetter, Claire Bunn, Nicholas Mignemi, John Marini, Alice N. Hackett, Meaghan Ransom, David Nichols, Susan H. Guttentag, Heather H. Pua, Timothy S. Blackwell, William Zacharias, David B. Frank, John A. Kozub, Anita Mahadevan-Jansen, Jonathan A. Kropski, Christopher V.E. Wright, Bryan Millis, Jennifer M. S. Sucre
Sequencing and chromosome-scale assembly of the giant Pleurodeles waltl genome Thomas Brown, Ahmed Elewa, Svetlana Iarovenko, Elaiyaraja Subramanian, Alberto Joven Araus, Andreas Petzold, Miyuki Susuki, Ken-ichi T. Suzuki, Toshinori Hayashi, Atsushi Toyoda, Catarina Oliveira, Ekaterina Osipova, Nicholas D. Leigh, Andras Simon, Maximina H. Yun
PCLAF-DREAM Drives Alveolar Cell Plasticity for Lung Regeneration Bongjun Kim, Yuanjian Huang, Kyung-Pil Ko, Shengzhe Zhang, Gengyi Zou, Jie Zhang, Moon Jong Kim, Danielle Little, Lisandra Vila Ellis, Margherita Paschini, Sohee Jun, Kwon-Sik Park, Jichao Chen, Carla Kim, Jae-Il Park
A stem cell zoo uncovers intracellular scaling of developmental tempo across mammals Jorge Lázaro, Maria Costanzo, Marina Sanaki-Matsumiya, Charles Girardot, Masafumi Hayashi, Katsuhiko Hayashi, Sebastian Diecke, Thomas B. Hildebrandt, Giovanna Lazzari, Jun Wu, Stoyan Petkov, Rüdiger Behr, Vikas Trivedi, Mitsuhiro Matsuda, Miki Ebisuya
A Canine Model of Chronic Ischemic Heart Failure Muhammad S. Khan, Douglas Smego, Yuki Ishidoya, Annie M. Hirahara, Emmanuel Offei, Sofia R. Castillo, Omar Gharbia, Joseph A. Palatinus, Lauren Krueger, TingTing Hong, Guillaume L. Hoareau, Ravi Ranjan, Craig Selzman, Robin Shaw, Derek J. Dosdall
In vivo generation of heart and vascular system by blastocyst complementation Giulia Coppiello, Paula Barlabé, Marta Moya-Jódar, Gloria Abizanda, Carolina Barreda, Elena Iglesias, Javier Linares, Estibaliz Arellano-Viera, Adrian Ruiz-Villalba, Eduardo Larequi, Xonia Carvajal-Vergara, Beatriz Pelacho, Felipe Prósper, Xabier L. Aranguren
Single-cell transcriptomic atlas reveals increased regeneration in diseased human inner ears Tian Wang, Angela H. Ling, Sara E. Billings, Davood K. Hosseini, Yona Vaisbuch, Grace S. Kim, Patrick J. Atkinson, Zahra N. Sayyid, Ksenia A. Aaron, Dhananjay Wagh, Nicole Pham, Mirko Scheibinger, Akira Ishiyama, Peter Santa Maria, Nikolas H. Blevins, Robert K. Jackler, Stefan Heller, Ivan A. Lopez, Nicolas Grillet, Taha A. Jan, Alan G. Cheng
RAPTOR: A Five-Safes approach to a secure, cloud native and serverless genomics data repository Chih Chuan Shih, Jieqi Chen, Ai Shan Lee, Nicolas Bertin, Maxime Hebrard, Chiea Chuen Khor, Zheng Li, Joanna Hui Juan Tan, Wee Yang Meah, Su Qin Peh, Shi Qi Mok, Kar Seng Sim, Jianjun Liu, Ling Wang, Eleanor Wong, Jingmei Li, Aung Tin, Ching-Yu Chen, Chew-Kiat Heng, Jian-Min Yuan, Woon-Puay Koh, Seang Mei Saw, Yechiel Friedlander, Xueling Sim, Jin Fang Chai, Yap Seng Chong, Sonia Davila, Liuh Ling Goh, Eng Sing Lee, Tien Yin Wong, Neerja Karnani, Khai Pang Leong, Khung Keong Yeo, John C Chambers, Su Chi Lim, Rick Siow Mong Goh, Patrick Tan, Rajkumar Dorajoo
Rabbit Development as a Model for Single Cell Comparative Genomics Mai-Linh N. Ton, Daniel Keitley, Bart Theeuwes, Carolina Guibentif, Jonas Ahnfelt-Rønne, Thomas Kjærgaard Andreassen, Fernando J. Calero-Nieto, Ivan Imaz-Rosshandler, Blanca Pijuan-Sala, Jennifer Nichols, Èlia Benito-Gutiérrez, John C. Marioni, Berthold Göttgens
Comprehensive cell atlas of the first-trimester developing human brain Emelie Braun, Miri Danan-Gotthold, Lars E. Borm, Elin Vinsland, Ka Wai Lee, Peter Lönnerberg, Lijuan Hu, Xiaofei Li, Xiaoling He, Žaneta Andrusivová, Joakim Lundeberg, Ernest Arenas, Roger A. Barker, Erik Sundström, Sten Linnarsson