A new era of stem cell and developmental biology: from blastoids to synthetic embryos and beyond
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Recent discoveries in stem cell and developmental biology have introduced a new era marked by the generation of in vitro models that recapitulate early mammalian development, providing unprecedented opportunities for extensive research in embryogenesis. Here, we present an overview of current techniques that model early mammalian embryogenesis, specifically noting models created from stem cells derived from two significant species: Homo sapiens, for its high relevance, and Mus musculus, a historically common and technically advanced model organism. We aim to provide a holistic understanding of these in vitro models by tracing the historical background of the progress made in stem cell biology and discussing the fundamental underlying principles. At each developmental stage, we present corresponding in vitro models that recapitulate the in vivo embryo and further discuss how these models may be used to model diseases. Through a discussion of these models as well as their potential applications and future challenges, we hope to demonstrate how these innovative advances in stem cell research may be further developed to actualize a model to be used in clinical practice.
Abstract
Recent discoveries in stem cell and developmental biology have introduced a new era marked by the generation of in vitro models that recapitulate early mammalian development, providing unprecedented opportunities for extensive research in embryogenesis. Here, we present an overview of current techniques that model early mammalian embryogenesis, specifically noting models created from stem cells derived from two significant species: Homo sapiens, for its high relevance, and Mus musculus, a historically common and technically advanced model organism. We aim to provide a holistic understanding of these in vitro models by tracing the historical background of the progress made in stem cell biology and discussing the fundamental underlying principles. At each developmental stage, we present corresponding in vitro models that recapitulate the in vivo embryo and further discuss how these models may be used to model diseases. Through a discussion of these models as well as their potential applications and future challenges, we hope to demonstrate how these innovative advances in stem cell research may be further developed to actualize a model to be used in clinical practice.
참고문헌 (115)
- Lewis, E. B., "A gene complex controlling segmentation in Drosophila", Nature, 276, pp.565~570 (1978)
- Nusslein-Volhard, C., "Mutations affecting segment number and polarity in Drosophila", Nature, 287, pp.795~801 (1980)
- Perlman, R. L., "Mouse models of human disease: an evolutionary perspective", Evol. Med. Public Health, 2016, pp.170~176 (2016)
- Steinbock, B., "Life Before Birth: The Moral and Legal Status of Embryos and Fetuses" (2011), Oxford University Press
- Clevers, H., "Modeling development and disease with organoids", Cell, 165, pp.1586~1597 (2016)
- Kim, J., "Human organoids : model systems for human biology and medicine", Nat. Rev. Mol. Cell Biol, 21, pp.571~584 (2020)
- van den Brink, S. C., "3D gastruloids : a novel frontier in stem cell-based in vitro modeling of mammalian gastrulation", Trends Cell Biol, 31, pp.747~759 (2021)
- Shahbazi, M. N., "Self-organization of stem cells into embryos : a window on early mammalian development", Science, 364, pp.948~951 (2019)
- Terhune, A. H., "Stem cell-based models of early mammalian development", Development, 149, pp.dev201015~ (2022)
- Bredenoord, A. L., "Human tissues in a dish: the research and ethical implications of organoid technology", Science, 355, pp.eaaf9414~ (2017)
- Wobus, A. M., "Embryonic stem cells : prospects for developmental biology and cell therapy", Physiol. Rev, 85, pp.635~678 (2005)
- Weinberger, L., "Dynamic stem cell states : naive to primed pluripotency in rodents and humans", Nat. Rev. Mol. Cell Biol, 17, pp.155~169 (2016)
- Fuchs, E., "Stem cells: a new lease on life", Cell, 100, pp.143~155 (2000)
- Thomson, J. A., "Embryonic stem cell lines derived from human blastocysts", Science, 282, pp.1145~1147 (1998)
- Weissman, I. L., "Stem cells: units of development, units of regeneration, and units in evolution", Cell, 100, pp.157~168 (2000)
- Okita, K., "Generation of germline-competent induced pluripotent stem cells", Nature, 448, pp.313~317 (2007)
- Stevens, L. C., "Spontaneous testicular teratomas in an inbred strain of mice", Proc. Natl Acad. Sci. USA, 40, pp.1080~1087 (1954)
- Kleinsmith, L. J., "Jr Multipotentiality of single embryonal carcinoma cells", Cancer Res, 24, pp.1544~1551 (1964)
- Evans, M. J, "The isolation and properties of a clonal tissue culture strain of pluripotent mouse teratoma cells", J. Embryol. Exp. Morphol, 28, pp.163~176 (1972)
- Evans, M. J., "Establishment in culture of pluripotential cells from mouse embryos", Nature, 292, pp.154~156 (1981)
- Martin, G. R., "Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells", Proc. Natl Acad. Sci. USA, 78, pp.7634~7638 (1981)
- Ginis, I., "Differences between human and mouse embryonic stem cells", Dev. Biol, 269, pp.360~380 (2004)
- Hanna, J., "Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs", Proc. Natl Acad. Sci. USA, 107, pp.9222~9227 (2010)
- Loh, Y. H., "The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells", Nat. Genet, 38, pp.431~440 (2006)
- Brons, I. G., "Derivation of pluripotent epiblast stem cells from mammalian embryos", Nature, 448, pp.191~195 (2007)
- Tesar, P. J., "New cell lines from mouse epiblast share defining features with human embryonic stem cells", Nature, 448, pp.196~199 (2007)
- Nichols, J., "Naive and primed pluripotent states", Cell Stem Cell, 4, pp.487~492 (2009)
- Theunissen, T. W., "Mechanisms of gene regulation in human embryos and pluripotent stem cells", Development, 144, pp.4496~4509 (2017)
- Marks, H., "The transcriptional and epigenomic foundations of ground state pluripotency", Cell, 149, pp.590~604 (2012)
- Smith, A. G., "Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides", Nature, 336, pp.688~690 (1988)
- Niwa, H., "Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3", Genes Dev, 12, pp.2048~2060 (1998)
- Lanner, F., "The role of FGF", Erk signaling in pluripotent cells, 2010, pp.137, 3351~3360
- James, D., "TGFbeta", activin, Development, pp.2005, 132[DOI]
- Ware, C. B., "Derivation of naive human embryonic stem cells", Proc. Natl Acad. Sci. USA, 111, pp.4484~4489 (2014)
- Gafni, O., "Derivation of novel human ground state naive pluripotent stem cells", Nature, 504, pp.282~286 (2013)
- Bayerl, J., "Principles of signaling pathway modulation for enhancing human naive pluripotency induction", Cell Stem Cell, 28, pp.1549~1565 (2021)
- Braude, P., "Human gene expression first occurs between the four-and eight-cell stages of preimplantation development", Nature, 332, pp.459~461 (1988)
- Schulz, K. N., "Mechanisms regulating zygotic genome activation", Nat. Rev. Genet, 20, pp.221~234 (2019)
- Mole, M. A., "Comparative analysis of human and mouse development : from zygote to pre-gastrulation", Curr. Top. Dev. Biol, 136, pp.113~138 (2020)
- Schultz, R. M., "Regulation of zygotic gene activation in the mouse", Bioessays, 15, pp.531~538 (1993)
- Mazid, M. A., "Rolling back human pluripotent stem cells to an eight-cell embryo-like stage", Nature, 605, pp.315~324 (2022)
- Fleming, T. P., "Cell adhesion in the preimplantation mammalian embryo and its role in trophectoderm differentiation and blastocyst morphogenesis", Front. Biosci, 6, pp.D1000~D1007 (2001)
- Zhu, M., "Principles of self-organization of the mammalian embryo", Cell, 183, pp.1467~1478 (2020)
- Tanaka, S., "Promotion of trophoblast stem cell proliferation by FGF4", Science, 282, pp.2072~2075 (1998)
- Kunath, T., "Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts", Development, 132, pp.1649~1661 (2005)
- Rivron, N. C., "Blastocyst-like structures generated solely from stem cells", Nature, 557, pp.106~111 (2018)
- Li, R., "Generation of blastocyst-like structures from mouse embryonic and adult cell cultures", Cell, 179, pp.687~702 (2019)
- Sozen, B., "Self-organization of mouse stem cells into an extended potential blastoid", Dev. Cell, 51, pp.698~712 (2019)
- Ying, Q. L., "The ground state of embryonic stem cell self-renewal", Nature, 453, pp.519~523 (2008)
- Arnold, S. J, "Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo", Nat. Rev. Mol. Cell Biol, 10, pp.91~103 (2009)
- Yamanaka, Y., "FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst", Development, 137, pp.715~724 (2010)
- Guo, G., "Human naive epiblast cells possess unrestricted lineage potential", Cell Stem Cell, 28, pp.1040~1056 (2021)
- Yang, Y., "Derivation of pluripotent stem cells with in vivo embryonic and extraembryonic potency", Cell, 169, pp.243~257 (2017)
- Io, S., "Capturing human trophoblast development with naive pluripotent stem cells in vitro", Cell Stem Cell, 28, pp.1023~1039 (2021)
- Kagawa, H., "Human blastoids model blastocyst development and implantation", Nature, 601, pp.600~605 (2022)
- Yu, L., "Blastocyst-like structures generated from human pluripotent stem cells", Nature, 591, pp.620~626 (2021)
- Yanagida, A., "Naive stem cell blastocyst model captures human embryo lineage segregation", Cell Stem Cell, 28, pp.1016~1022 (2021)
- Yang, J., "Establishment of mouse expanded potential stem cells", Nature, 550, pp.393~397 (2017)
- Gao, X., "Establishment of porcine and human expanded potential stem cells", Nat. Cell Biol, 21, pp.687~699 (2019)
- Sozen, B., "Reconstructing aspects of human embryogenesis with pluripotent stem cells", Nat. Commun, 12, pp.5550~ (2021)
- Fan, Y., "Generation of human blastocyst-like structures from pluripotent stem cells", Cell Discov, 7, pp.81~ (2021)
- Liu, X., "Modelling human blastocysts by reprogramming fibroblasts into iBlastoids", Nature, 591, pp.627~632 (2021)
- Lovell-Badge, R., "ISSCR Guidelines for Stem Cell Research and Clinical Translation : the 2021 update", Stem Cell Rep, 16, pp.1398~1408 (2021)
- Zhao, C., "Reprogrammed blastoids contain amnion-like cells but not trophectoderm", bioRxiv, ~ (2021)
- Martin, G. R, "Differentiation of clonal lines of teratocarcinoma cells:formation of embryoid bodies in vitro", Proc. Natl Acad. Sci. USA, 72, pp.1441~1445 (1975)
- Ying, Q. L., "Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture", Nat. Biotechnol, 21, pp.183~186 (2003)
- D'Amour, K. A., "Efficient differentiation of human embryonic stem cells to definitive endoderm", Nat. Biotechnol, 23, pp.1534~1541 (2005)
- ten Berge, D., "Wnt signaling mediates self-organization and axis formation in embryoid bodies", Cell Stem Cell, 3, pp.508~518 (2008)
- van den Brink, S. C., "Symmetry breaking, germ layer specification and axial organisation in aggregates of mouse embryonic stem cells", Development, 141, pp.4231~4242 (2014)
- Turner, D. A., "Anteroposterior polarity and elongation in the absence of extra-embryonic tissues and of spatially localised signalling in gastruloids : mammalian embryonic organoids", Development, 144, pp.3894~3906 (2017)
- van den Brink, S. C., "Single-cell and spatial transcriptomics reveal somitogenesis in gastruloids", Nature, 582, pp.405~409 (2020)
- Warmflash, A., "A method to recapitulate early embryonic spatial patterning in human embryonic stem cells", Nat. Methods, 11, pp.847~854 (2014)
- Etoc, F., "A balance between secreted inhibitors and edge sensing controls gastruloid self-organization", Dev. Cell, 39, pp.302~315 (2016)
- Martyn, I., "Mapping cell migrations and fates in a gastruloid model to the human primitive streak", Development, 146, pp.dev179564~ (2019)
- Blin, G., "Geometrical confinement controls the asymmetric patterning of brachyury in cultures of pluripotent cells", Development, 145, pp.dev166025~ (2018)
- Muncie, J. M., "Mechanical tension promotes formation of gastrulation-like nodes and patterns mesoderm specification in human embryonic stem cells", Dev. Cell, 55, pp.679~694 (2020)
- Beccari, L., "Multi-axial self-organization properties of mouse embryonic stem cells into gastruloids", Nature, 562, pp.272~276 (2018)
- Girgin, M. U., "Gastruloids generated without exogenous Wnt activation develop anterior neural tissues", Stem Cell Rep, 16, pp.1143~1155 (2021)
- Minn, K. T., "High-resolution transcriptional and morphogenetic profiling of cells from micropatterned human ESC gastruloid cultures", Elife, 9, pp.e59445~ (2020)
- Simunovic, M., "A 3D model of a human epiblast reveals BMP4-driven symmetry breaking", Nat. Cell Biol, 21, pp.900~910 (2019)
- Libby, A. R. G., "Axial elongation of caudalized human organoids mimics aspects of neural tube development", Development, 148, pp.dev198275~ (2021)
- Simunovic, M., "In vitro attachment and symmetry breaking of a human embryo model assembled from primed embryonic stem cells", Cell Stem Cell, 29, pp.962~972 (2022)
- Moris, N., "An in vitro model of early anteroposterior organization during human development", Nature, 582, pp.410~415 (2020)
- Olmsted, Z. T., "Co-development of central and peripheral neurons with trunk mesendoderm in human elongating multi-lineage organized gastruloids", Nat. Commun, 12, pp.3020~ (2021)
- Karzbrun, E., "Human neural tube morphogenesis in vitro by geometric constraints", Nature, 599, pp.268~272 (2021)
- Whye, D., "Dynamic 3D combinatorial generation of hPSC-derived neuromesodermal organoids with diverse regional and cellular identities", Curr. Protoc, 2, pp.e568~ (2022)
- Yaman, Y. I., "Controlling human organoid symmetry breaking reveals signaling gradients drive segmentation clock waves", Cell, 186, pp.513~527 (2023)
- Yamanaka, Y., "Reconstituting human somitogenesis in vitro", Nature, 614, pp.509~520 (2023)
- Diaz-Cuadros, M., "In vitro characterization of the human segmentation clock", Nature, 580, pp.113~118 (2020)
- Xu, P. F., "Construction of a mammalian embryo model from stem cells organized by a morphogen signalling centre", Nat. Commun, 12, pp.3277~ (2021)
- Vianello, S., "In vitro endoderm emergence and self-organisation in the absence of extraembryonic tissues and embryonic architecture", PhD, pp.2021
- Veenvliet, J. V., "Mouse embryonic stem cells self-organize into trunk-like structures with neural tube and somites", Science, 370, pp.eaba4937~ (2020)
- Harrison, S. E., "Assembly of embryonic and extraembryonic stem cells to mimic embryogenesis in vitro", Science, 356, pp.eaal1810~ (2017)
- Sozen, B., "Self-assembly of embryonic and two extra-embryonic stem cell types into gastrulating embryo-like structures", Nat. Cell Biol, 20, pp.979~989 (2018)
- Zhang, S., "Implantation initiation of self-assembled embryo-like structures generated using three types of mouse blastocyst-derived stem cells", Nat. Commun, 10, pp.496~ (2019)
- Amadei, G., "Embryo model completes gastrulation to neurulation and organogenesis", Nature, 610, pp.143~153 (2022)
- New, D. A, "Development of explanted rat embryos in circulating medium", J. Embryol. Exp. Morphol, 17, pp.513~525 (1967)
- New, D. A., "Culture of explanted rat embryos in rotating tubes", J. Reprod. Fertil, 35, pp.135~138 (1973)
- Aguilera-Castrejon, A., "Ex utero mouse embryogenesis from pregastrulation to late organogenesis", Nature, 593, pp.119~124 (2021)
- Tarazi, S., "Post-gastrulation synthetic embryos generated ex utero from mouse naive ESCs", Cell, 185, pp.3290~3306 (2022)
- Weatherbee, B. A. T., "Pluripotent stem cell-derived model of the postimplantation human embryo", Nature (2023)[DOI]
- Oldak B., "Complete human day 14 post-implantation embryo models from naïve ES cells", Nature (2023)[DOI]
- Williams, J. L., "Causes of death in infants and children with congenital heart disease", Pediatr. Cardiol, 42, pp.1308~1315 (2021)
- Nguyen, D. C., "Microscale generation of cardiospheres promotes robust enrichment of cardiomyocytes derived from human pluripotent stem cells", Stem Cell Rep, 3, pp.260~268 (2014)
- Giacomelli, E., "Three-dimensional cardiac microtissues composed of cardiomyocytes and endothelial cells co-differentiated from human pluripotent stem cells", Development, 144, pp.1008~1017 (2017)
- Polonchuk, L., "Cardiac spheroids as promising in vitro models to study the human heart microenvironment", Sci. Rep, 7, pp.7005~ (2017)
- Andersen, P., "Precardiac organoids form two heart fields via Bmp", Wnt signaling, 2018, pp.9, 3140~
- Hofbauer, P., "Cardioids reveal self-organizing principles of human cardiogenesis", Cell, 184, pp.3299~3317 (2021)
- Rossi, G., "Capturing cardiogenesis in gastruloids", Cell Stem Cell, 28, pp.230~240 (2021)
- Olmsted, Z. T., "A combined human gastruloid model of cardiogenesis and neurogenesis", iScience, 25, pp.104486~ (2022)
- Olmsted, Z. T., "Generation of human elongating multi-lineage organized(EMLO)gastruloids", Res. Square (2021)[DOI]
- Rivron, N., "Debate ethics of embryo models from stem cells", Nature, 564, pp.183~185 (2018)
- Yuan, C. J., "Developmental toxicity assessment of common excipients using a stem cell-based in vitro morphogenesis model", Food Chem. Toxicol, 109, pp.376~385 (2017)
- Li, A. S. W., "Methoxyacetic acid inhibits histone deacetylase and impairs axial elongation morphogenesis of mouse gastruloids in a retinoic acid signaling-dependent manner", Birth Defects Res, 112, pp.1043~1056 (2020)
- Mantziou, V., "In vitro teratogenicity testing using a 3D, embryo-like gastruloid system", Reprod. Toxicol, 105, pp.72~90 (2021)
