Building Pluripotency Identity in the Early Embryo and Derived Stem Cells

Overview

Journal Cells

Publisher MDPI

Specialties Biochemistry
Biophysics
Cell Biology
Molecular Biology

Date 2021 Aug 27

PMID 34440818

Citations 6

Authors

Paola Rebuzzini

Maurizio Zuccotti

Silvia Garagna

Affiliations

Soon will be listed here.

Abstract

The fusion of two highly differentiated cells, an oocyte with a spermatozoon, gives rise to the zygote, a single totipotent cell, which has the capability to develop into a complete, fully functional organism. Then, as development proceeds, a series of programmed cell divisions occur whereby the arising cells progressively acquire their own cellular and molecular identity, and totipotency narrows until when pluripotency is achieved. The path towards pluripotency involves transcriptome modulation, remodeling of the chromatin epigenetic landscape to which external modulators contribute. Both human and mouse embryos are a source of different types of pluripotent stem cells whose characteristics can be captured and maintained in vitro. The main aim of this review is to address the cellular properties and the molecular signature of the emerging cells during mouse and human early development, highlighting similarities and differences between the two species and between the embryos and their cognate stem cells.

Citing Articles

Interplay of chromatin remodeling BAF complexes in mouse embryonic and epiblast stem cell conversion and maintenance.

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Longitudinal profiling of human androgenotes through single-cell analysis unveils paternal gene expression dynamics in early embryo development.

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The Dynamics of Histone Modifications during Mammalian Zygotic Genome Activation.

Sotomayor-Lugo F, Iglesias-Barrameda N, Castillo-Aleman Y, Casado-Hernandez I, Villegas-Valverde C, Bencomo-Hernandez A Int J Mol Sci. 2024; 25(3).

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References

Xu R, Li C, Liu X, Gao S . Insights into epigenetic patterns in mammalian early embryos. Protein Cell. 2020; 12(1):7-28. PMC: 7815849. DOI: 10.1007/s13238-020-00757-z. View

Johnson M, McConnell J . Lineage allocation and cell polarity during mouse embryogenesis. Semin Cell Dev Biol. 2004; 15(5):583-97. DOI: 10.1016/j.semcdb.2004.04.002. View

Gafni O, Weinberger L, AlFatah Mansour A, Manor Y, Chomsky E, Ben-Yosef D . Derivation of novel human ground state naive pluripotent stem cells. Nature. 2013; 504(7479):282-6. DOI: 10.1038/nature12745. View

Geng T, Zhang D, Jiang W . Epigenetic Regulation of Transition Among Different Pluripotent States: Concise Review. Stem Cells. 2019; 37(11):1372-1380. DOI: 10.1002/stem.3064. View

Yan L, Yang M, Guo H, Yang L, Wu J, Li R . Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol. 2013; 20(9):1131-9. DOI: 10.1038/nsmb.2660. View

Dinger M, Amaral P, Mercer T, Pang K, Bruce S, Gardiner B . Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 2008; 18(9):1433-45. PMC: 2527704. DOI: 10.1101/gr.078378.108. View

Kojima Y, Tam O, Tam P . Timing of developmental events in the early mouse embryo. Semin Cell Dev Biol. 2014; 34:65-75. DOI: 10.1016/j.semcdb.2014.06.010. View

Brons I, Smithers L, Trotter M, Rugg-Gunn P, Sun B, Chuva de Sousa Lopes S . Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature. 2007; 448(7150):191-5. DOI: 10.1038/nature05950. View

Gerri C, Menchero S, Mahadevaiah S, Turner J, Niakan K . Human Embryogenesis: A Comparative Perspective. Annu Rev Cell Dev Biol. 2020; 36:411-440. DOI: 10.1146/annurev-cellbio-022020-024900. View

10.

Li M, Izpisua Belmonte J . Deconstructing the pluripotency gene regulatory network. Nat Cell Biol. 2018; 20(4):382-392. PMC: 6620196. DOI: 10.1038/s41556-018-0067-6. View

11.

Schulz K, Harrison M . Mechanisms regulating zygotic genome activation. Nat Rev Genet. 2018; 20(4):221-234. PMC: 6558659. DOI: 10.1038/s41576-018-0087-x. View

12.

Stein P, Worrad D, Belyaev N, Turner B, Schultz R . Stage-dependent redistributions of acetylated histones in nuclei of the early preimplantation mouse embryo. Mol Reprod Dev. 1997; 47(4):421-9. DOI: 10.1002/(SICI)1098-2795(199708)47:4<421::AID-MRD8>3.0.CO;2-M. View

13.

Illingworth R, Holzenspies J, Roske F, Bickmore W, Brickman J . Polycomb enables primitive endoderm lineage priming in embryonic stem cells. Elife. 2016; 5. PMC: 5056788. DOI: 10.7554/eLife.14926. View

14.

Smith Z, Chan M, Mikkelsen T, Gu H, Gnirke A, Regev A . A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature. 2012; 484(7394):339-44. PMC: 3331945. DOI: 10.1038/nature10960. View

15.

Bao M, Li J, Zhou Q, Li G, Zeng J, Zhao J . Effects of miR‑590 on oxLDL‑induced endothelial cell apoptosis: Roles of p53 and NF‑κB. Mol Med Rep. 2015; 13(1):867-73. DOI: 10.3892/mmr.2015.4606. View

16.

Wicklow E, Blij S, Frum T, Hirate Y, Lang R, Sasaki H . HIPPO pathway members restrict SOX2 to the inner cell mass where it promotes ICM fates in the mouse blastocyst. PLoS Genet. 2014; 10(10):e1004618. PMC: 4207610. DOI: 10.1371/journal.pgen.1004618. View

17.

Abu-Halima M, Khaizaran Z, Ayesh B, Fischer U, Khaizaran S, Al-Battah F . MicroRNAs in combined spent culture media and sperm are associated with embryo quality and pregnancy outcome. Fertil Steril. 2020; 113(5):970-980.e2. DOI: 10.1016/j.fertnstert.2019.12.028. View

18.

Czechanski A, Byers C, Greenstein I, Schrode N, Donahue L, Hadjantonakis A . Derivation and characterization of mouse embryonic stem cells from permissive and nonpermissive strains. Nat Protoc. 2014; 9(3):559-74. PMC: 4112089. DOI: 10.1038/nprot.2014.030. View

19.

OLeary T, Heindryckx B, Lierman S, van der Jeught M, Duggal G, De Sutter P . Derivation of human embryonic stem cells using a post-inner cell mass intermediate. Nat Protoc. 2013; 8(2):254-64. DOI: 10.1038/nprot.2012.157. View

20.

Tang F, Barbacioru C, Bao S, Lee C, Nordman E, Wang X . Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell. 2010; 6(5):468-78. PMC: 2954317. DOI: 10.1016/j.stem.2010.03.015. View