Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom DOI Creative Commons
Guojun Sheng, Thorsten Boroviak, Urs Schmidt‐Ott

и другие.

Philosophical Transactions of the Royal Society B Biological Sciences, Год журнала: 2022, Номер 377(1865)

Опубликована: Окт. 17, 2022

Open AccessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Sheng Guojun, Boroviak Thorsten E., Schmidt-Ott Urs and Srinivas Shankar 2022Extraembryonic tissues: exploring concepts, definitions functions across the animal kingdomPhil. Trans. R. Soc. B3772021025020210250http://doi.org/10.1098/rstb.2021.0250SectionOpen AccessIntroductionExtraembryonic kingdom Guojun http://orcid.org/0000-0001-6759-3785 International Research Center for Medical Sciences, Kumamoto University, 860-0811, Japan [email protected] Contribution: Writing – original draft, review & editing Google Scholar Find author on PubMed Search more papers by , E. http://orcid.org/0000-0001-8703-8949 Department of Physiology, Development Neuroscience, University Cambridge, Cambridge CB2 3EG, UK http://orcid.org/0000-0002-1351-9472 Organismal Biology Anatomy, Chicago, IL 60637, USA http://orcid.org/0000-0001-5726-7791 Anatomy Genetics, Oxford, Oxford OX3 7TY, Published:17 October 2022https://doi.org/10.1098/rstb.2021.02501. IntroductionAll emerging life must function while being built. The developing embryo requires an aqueous environment, a supply nutrients, gas exchange waste management. Extraembryonic membranes accomplish these challenges providing multifunctional organs interfaces between outside world.The importance extraembryonic tissues is particularly evident in animals that have adapted terrestrial life. For instance, amniotic vertebrates four amnion, chorion, allantois yolk sac, with each performing specialized, essential physiological functions. Terrestrial arthropods evolved other tissues, such as serosa amnion insects, which perform similar their vertebrate counterparts (e.g. drought resistance, embryonic tissue morphogenesis possibly management) innate immunity). Traditionally, were perceived only during embryogenesis, subsequently shed at birth or hatching.Under close scrutiny, however, embryonic–extraembryonic dichotomy far from straight-forward. boundaries are often ill-defined; fates so-called may not be entirely extraembryonic; physiological, biomechanical, morphogenetic signalling roles, regard development under-appreciated; evolutionary constraints conservation diversification poorly understood. Increasingly, molecular cellular evidence points toward certain arbitrariness making distinction tissues. Therefore, we feel it timely dedicate theme issue current understanding entities traditionally viewed extraembryonic.Our goal present raise awareness both interconnection well further studies ‘holistic' development.This features research articles complements panarthropods. Among them, eight focus mammalian Matsuo et al. [1] discuss developmental mechanical roles Reichert's membrane mice, non-cellular basal lamina separating trophectoderm parietal sac endoderm. Thowfeequ [2] idea shifting time space early mouse development. Pfeffer [3] hypothesizes connection cavitation epiblast loss Rauber's layer (polar trophoblast covering inner cell mass) mammals. Chowdhary Hadjantonakis [4] describe ontogeny specification primitive endoderm mice. Downs [5] examines embryogenesis Siriwardena [6] compare implantation different primate species suggest mechanisms controlling invasion depth provide new insights into human placental disorders. Chuva de Sousa Lopes [7] modes amniogenesis amniotes signatures ectoderm mesoderm Roelen [8] primordial germ boundary territories subsequent gonadal colonization.Extraembryonic non-mammalian additional papers. Concha Reig [9] give comprehensive overview origin, form, teleost structures, is, syncytial enveloping layer. Wen [10] investigate differences chorioallantoic live-bearing egg-laying lizards. Nagai [11] chick hypothesize evolutionarily conserved process underlying mesothelial fusion formation placenta eutherian Wittington [12] placentation vertebrates, reminding readers deep roots diverse strategies adopted groups fulfill needs.Extraembryonic Panarthropoda discussed five articles. Panfilio [13] anatomy, ontogeny, function, genetic regulation insects. Treffkorn [14] assess potential occurrence onychophorans (velvet worms) tardigrades (water bears), two invertebrate clades closely related arthropods. Prpic Pechmann [15] candidate spiders chelicerates. Jacob [16] immune hemimetabolous previously was known holometabolous Some flies, including fruit fly Drosophila melanogaster lack differentiated along its instead develop unique tissue, dubbed amnioserosa. Kwan [17] trace heritage examine how serosa-specific amnio-specific trajectories merged one D. melanogaster.These offer snapshot views intricacy complexity embryonic-extraembryonic crosstalk However, contrast development, concepts gastrulation, formation, dorsal-ventral anterior–posterior axis can broadly applied all metazoans, no unifying themes emerged We hope will encourage biologists work investigating questions regarding phylogeny application regenerative medicine. example, there common defining invertebrates? Do follow largely decoupled meet specific needs organisms development? Which panarthropods contribute cells fetus what cells? How involved patterning? chelicerates lasting tissue? What insect ventral (and cavity)? drove cyclorrhaphan flies? Does residual (dorsal) lower Cyclorrhapha drive same movements than amnioserosa? If so, does dorsal power processes?Finally, practical use knowledge model vitro reconstituting environment fetal–maternal interface, role usually fulfilled Currently, know relatively little about principles guide differentiation stem towards proper organization any tissue. spark discussions, debate collaborations within field, ultimately moving but still somewhat mysterious level.Data accessibilityThis has data.Authors' contributionsG.S.: writing—original writing—review editing; T.E.B.: U.S.-O.: S.S.: editing.All authors gave final approval publication agreed held accountable performed therein.Conflict interest declarationThis put together Guest Editor team under supervision journal's Editorial staff, following Royal Society's ethical codes best-practice guidelines. invited contributions handled process. Individual Editors assessing where they had personal, professional financial conflict described. Independent reviewers assessed Invitation did guarantee inclusion.FundingWe received funding study.FootnotesOne contribution 18 ‘Extraembryonic kingdom’.© 2022 Authors.Published Society terms Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, permits unrestricted use, provided source credited.References1. I, Kimura-Yoshida C, Ueda Y. 2022Developmental embryos. Phil. B 377, 20210257. (doi:10.1098/rstb.2021.0257) Link, Scholar2. S, S. 2022Embryonic development: space. 20210255. (doi:10.1098/rstb.2021.0255) Scholar3. PL. 2022Alternative leading gastrulation: losing polar (Rauber's layer) gaining cavity. 20210254. (doi:10.1098/rstb.2021.0254) Scholar4. A-K. 2022Journey endoderm: maturation. 20210252. (doi:10.1098/rstb.2021.0252) Scholar5. KM. 2022The allantois: interface. 20210251. (doi:10.1098/rstb.2021.0251) Scholar6. D, TE. 2022Evolutionary divergence primates. 20210256. (doi:10.1098/rstb.2021.0256) Scholar7. SM, BAJ, Lawson KA, Zwijsen A. mice amniotes. 20210258. (doi:10.1098/rstb.2021.0258) Scholar8. SM. 2022Stay road: colonization 20210259. (doi:10.1098/rstb.2021.0259) Scholar9. ML, G. 2022Origin, form structures fishes. 20210264. (doi:10.1098/rstb.2021.0264) Scholar10. J, Ishihara T, Renfree MB, Griffith OW. 2022Comparing maternal–fetal oviparous viviparous 20210262. (doi:10.1098/rstb.2021.0262) Scholar11. H, Tanoue Y, Nakamura Chan CJJ, Yamada Saitou M, Fukuda 2022Mesothelial mediates formation. 20210263. (doi:10.1098/rstb.2021.0263) Scholar12. Whittington CM, Buddle AL, OW, Carter AM. specializations placentation. 20210261. (doi:10.1098/rstb.2021.0261) Scholar13. extended analogy insects 20210268. (doi:10.1098/rstb.2021.0268) Scholar14. Mayer G, Janssen 2022Review extra-embryonic closest arthropod relatives, tardigrades. 20210270. (doi:10.1098/rstb.2021.0270) Scholar15. N-M, M. chelicerates: outlook. 20210269. (doi:10.1098/rstb.2021.0269) Scholar16. Jacobs CGC, van der Hulst R, Chen Y-T, Williamson RP, Roth Zee M.2022Immune eggs. 20210266. (doi:10.1098/rstb.2021.0266) Scholar17. U, CW. 2022How epithelia became one: Drosophila's 20210265. (doi:10.1098/rstb.2021.0265) Next Article VIEW FULL TEXT DOWNLOAD FiguresRelatedReferencesDetails This Issue05 December 2022Volume 377Issue 1865Theme kingdom’ compiled edited Sheng, Boroviak, InformationDOI:https://doi.org/10.1098/rstb.2021.0250PubMed:36252213Published by:Royal SocietyPrint ISSN:0962-8436Online ISSN:1471-2970History: Manuscript received11/08/2022Manuscript accepted11/08/2022Published online17/10/2022Published print05/12/2022 License:© credited. impact Subjectsdevelopmental biologyevolutiongenetics

Язык: Английский

Lumen expansion is initially driven by apical actin polymerization followed by osmotic pressure in a human epiblast model DOI Creative Commons
Dhiraj Indana, A. P. Zakharov, Youngbin Lim

и другие.

Cell stem cell, Год журнала: 2024, Номер 31(5), С. 640 - 656.e8

Опубликована: Май 1, 2024

Язык: Английский

Процитировано

11
Transgene-Free Ex Utero Derivation of A Human Post-Implantation Embryo Model Solely from Genetically Unmodified Naïve PSCs DOI Open Access
Bernardo Oldak,

Emilie Wildschutz,

Vladyslav Bondarenko

и другие.

bioRxiv (Cold Spring Harbor Laboratory), Год журнала: 2023, Номер unknown

Опубликована: Июнь 15, 2023

Abstract Our ability to study early human post-implantation development remains highly limited due the ethical and technical challenges associated with intrauterine of embryo after implantation. Despite great progress made on gastruloids, axioloids in vitro cultured blastoids, such elegant models do not constitute an integrated Stem cell-derived Embryo Models (SEMs) that includes all key extra-embryonic tissues conceptus (e.g., hypoblast, yolk-sac, trophoblasts, amnion, extraembryonic mesoderm), thus, recapitulate epiblast within context these compartments. Mouse naïve pluripotent stem cells (PSCs) have recently been shown give rise embryonic capable self-assembling into post-gastrulation mouse SEMs, while bypassing blastocyst-like stage, eventually initiating organogenesis ex utero . Here, we implement critical adaptations extend finding humans, using only genetically unmodified PSCs, thus circumventing need for ectopic expression lineage promoting transgenes. Such SEMs organization known compartments stage embryos, including epiblast, mesoderm, trophoblast surrounding latter layers. The organized hallmarks embryogenesis up 13-14 days post-fertilization (dpf, Carnegie 6a), as bilaminar disk formation, lumenogenesis, amniogenesis, anterior-posterior symmetry breaking, PGC specification, primary secondary yolk sac mesoderm expansion defines a chorionic cavity connective stalk. This new platform constitutes tractable cell-based model experimentally interrogating previously inaccessible windows peri- development.

Язык: Английский

Процитировано

21
Efficient derivation of embryonic stem cells and primordial germ cell-like cells in cattle DOI Creative Commons

A. Shirasawa,

Masafumi Hayashi,

Mayumi Shono

и другие.

Journal of Reproduction and Development, Год журнала: 2024, Номер 70(2), С. 82 - 95

Опубликована: Янв. 1, 2024

The induction of the germ cell lineage from pluripotent stem cells (in vitro gametogenesis) will help understand mechanisms underlying differentiation and provide an alternative source gametes for reproduction. This technology is especially important cattle, which are among most livestock species milk meat production. Here, we developed a new method robust primordial cell-like (PGCLCs) newly established bovine embryonic (bES) cells. First, refined culture conditions pre-implantation embryos ES Inhibition RHO increased number epiblast in dramatically improved efficiency establishment. We then determined suitable PGCLC using bES harboring BLIMP1-tdTomato TFAP2C-mNeonGreen (BTTN) reporter constructs. After 24-h with bone morphogenetic protein 4 (BMP4), followed by three-dimensional BMP4 chemical agonist WNT signaling antagonist, became positive reporters. A set (PGC) marker genes, including PRDM1/BLIMP1, TFAP2C, SOX17, NANOS3, were expressed BTTN-positive These PGCLCs (bPGCLCs) isolated as KIT/CD117-positive CD44-negative populations. anticipate that this efficient establishment be useful cell-based reproductive technologies cattle.

Язык: Английский

Процитировано

9
The guinea pig serves as an alternative model to study human preimplantation development DOI Creative Commons
Jésica Canizo, Cheng Zhao, Sophie Petropoulos

и другие.

Nature Cell Biology, Год журнала: 2025, Номер unknown

Опубликована: Апрель 4, 2025

Abstract Preimplantation development is an important window of human embryogenesis. However, ethical constraints and the limitations involved in studying embryos often necessitate use alternative model systems. Here we identify guinea pig as a promising small animal to study preimplantation development. Using single-cell RNA-sequencing, generated atlas development, revealing its close resemblance early embryogenesis terms timing compaction, early-, mid- late-blastocyst formation, implantation, spatio-temporal expression key lineage markers. We also show conserved roles Hippo, MEK-ERK JAK-STAT signalling. Furthermore, multi-species analysis highlights divergent genes during pluripotency. The serves valuable for advancing stem cell research, can be leveraged better understand longer-term impact exposures on offspring outcomes.

Язык: Английский

Процитировано

1
A single-cell atlas of pig gastrulation as a resource for comparative embryology DOI Creative Commons
Luke Simpson, A. Strange, Doris Klisch

и другие.

Nature Communications, Год журнала: 2024, Номер 15(1)

Опубликована: Июнь 18, 2024

Abstract Cell-fate decisions during mammalian gastrulation are poorly understood outside of rodent embryos. The embryonic disc pig embryos mirrors humans, making them a useful proxy for studying gastrulation. Here we present single-cell transcriptomic atlas gastrulation, revealing cell-fate emergence dynamics, as well conserved and divergent gene programs governing early porcine, primate, murine development. We highlight heterochronicity in extraembryonic cell-types, despite the broad conservation cell-type-specific transcriptional programs. apply these findings combination with functional investigations, to outline spatial, molecular, temporal events definitive endoderm specification. find FOXA2 + /TBXT- cells directly form endoderm, contrasting later-emerging FOXA2/TBXT+ node/notochord progenitors. Unlike mesoderm, none progenitors undergo epithelial-to-mesenchymal transition. Endoderm/Node fate hinges on balanced WNT hypoblast-derived NODAL, which is extinguished upon endodermal differentiation. These emphasise interplay between topological signalling determination

Язык: Английский

Процитировано

5
Using extended growth of cattle embryos in culture to gain insights into bovine developmental events on embryonic days 8 to 10 DOI Creative Commons
Ekaterina Isaac, D.K. Berg, Peter Pfeffer

и другие.

Theriogenology, Год журнала: 2023, Номер 214, С. 10 - 20

Опубликована: Окт. 6, 2023

We have previously described an extended embryo culture system, based on uterine composition, growth factors and the cell additive B27, for growing cattle embryos in vitro beyond embryonic day 7. Here, are compared to developed uterus used establish a developmental staging framework useful understanding events occurring until Day 10. Immunofluorescence or mRNA expression of ICM/epiblast markers OCT4, SOX2 NANOG, hypoblast GATA6, SOX17 GATA4 trophoblast genes CDX2, GATA3, ASCL2 IFNT revealed presence four stages during this period that can be molecularly distinguished. These expanded blastocyst, hatched layering early migration. Interestingly NANOG show reciprocal at blastocyst stage, well before GATA6 refines similar so-called "salt pepper" mutually exclusive ICM stage. is only seen from when starts migrating around cavity. Intriguingly, still expresses OCT4 all cells phase, while some cells. By hypoblast-epiblast stage no remains except protein, which waning once begins migrating. Lastly, it shown cultured exhibit increased stress marker TP53 epiblast late comparison produced environment.

Язык: Английский

Процитировано

7
Interspecies control of development during mammalian gastrulation DOI Creative Commons
Luke Simpson, Ramiro Alberio

Emerging Topics in Life Sciences, Год журнала: 2023, Номер 7(4), С. 397 - 408

Опубликована: Ноя. 7, 2023

Gastrulation represents a pivotal phase of development and aberrations during this period can have major consequences, from minor anatomical deviations to severe congenital defects. Animal models are used study gastrulation, however, there is considerable morphological molecular diversity gastrula across mammalian species. Here, we provide an overview the latest research on interspecies developmental control mammals. This includes single-cell atlases several which enabled comparisons temporal dynamics differentiation. These studies highlight conserved cell differentiation regulators both absolute relative differences in between Recent advances vitro culture techniques facilitated derivation, maintenance lines range species creation multi-species gastrulation. Gastruloids three-dimensional aggregates capable self-organising recapitulating aspects Such enable outside confines embryo. We recent evidence that processes such as somitogenesis neuronal maturation scale with known vivo tempo scaling likely due intrinsic biochemistry. also examples being influenced by extrinsic factors, including conditions, chimeric co-culture, xenotransplantation. collective underscore complexity gastrulation species, highlighting necessity additional datasets decipher intricate balance cellular programs signals shaping embryogenesis.

Язык: Английский

Процитировано

5
Actin polymerization drives lumen formation in a human epiblast model DOI Open Access
Dhiraj Indana, A. P. Zakharov, Youngbin Lim

и другие.

bioRxiv (Cold Spring Harbor Laboratory), Год журнала: 2023, Номер unknown

Опубликована: Апрель 20, 2023

Summary Lumens or fluid-filled cavities are a ubiquitous feature of mammals and often evolutionarily linked to the origin body-plan complexity. Post-implantation, pluripotent epiblast in human embryo forms central lumen, paving way for gastrulation. While osmotic pressure gradients drive lumen formation many developmental contexts, mechanisms lumenogenesis unknown. Here, we study pluripotent-stem-cell-based model using engineered hydrogels that confinement faced by blastocyst. Actin polymerization into dense mesh-like network at apical surface generates forces early expansion, as leaky junctions prevent gradients. Theoretical modeling reveals actin stiff drives opening, but predicts switch driven growth larger sizes is required avoid buckling cell layer. Consistent with this prediction, once reaches radius around 12 μm, tight mature, develop further growth. Human epiblasts show transcriptional signature during lumenogenesis. Thus, opening epiblast, may serve general mechanism

Язык: Английский

Процитировано

4
The Guinea Pig: A New Model for Human Preimplantation Development DOI Creative Commons
Jésica Canizo, Cheng Zhao, Sophie Petropoulos

и другие.

bioRxiv (Cold Spring Harbor Laboratory), Год журнала: 2024, Номер unknown

Опубликована: Фев. 6, 2024

ABSTRACT Preimplantation development is an important window of human embryogenesis. During this time, the initial lineages are formed which largely govern embryo competence, implantation, and ultimately developmental potential fetus. Ethical constraints limitations surrounding embryos research often necessitates use a model system. We now identify guinea pig as promising small animal model, closely recapitulates early embryogenesis in terms timing compaction, early-, mid-, late-blastocyst formation implantation. also observe conserved spatio-temporal expression key lineage markers, roles both Hippo MEK-ERK signaling incomplete X-Chromosome inactivation. Further, our multi-species analysis highlights divergent genes during preimplantation development. The serves exciting new will enhance pluripotency can be leveraged to better understand longer term impact exposures on offspring outcomes.

Язык: Английский

Процитировано

1
Single-cell analysis of preimplantation embryonic development in guinea pigs DOI Creative Commons

Tongxing Guan,

Jing Guo,

Runxia Lin

и другие.

BMC Genomics, Год журнала: 2024, Номер 25(1)

Опубликована: Сен. 30, 2024

Guinea pigs exhibit numerous physiological similarities to humans, yet the details of their preimplantation embryonic development remain largely unexplored.

Язык: Английский

Процитировано

1