Human embryonic genome activation initiates at the one-cell stage.

embryonic genome activation (EGA) fertilization human one-cell embryo single-cell RNA-seq totipotency transcriptome zygote

Journal

Cell stem cell
ISSN: 1875-9777
Titre abrégé: Cell Stem Cell
Pays: United States
ID NLM: 101311472

Informations de publication

Date de publication:
03 02 2022
Historique:
received: 08 04 2021
revised: 24 08 2021
accepted: 29 11 2021
pubmed: 23 12 2021
medline: 19 4 2022
entrez: 22 12 2021
Statut: ppublish

Résumé

In human embryos, the initiation of transcription (embryonic genome activation [EGA]) occurs by the eight-cell stage, but its exact timing and profile are unclear. To address this, we profiled gene expression at depth in human metaphase II oocytes and bipronuclear (2PN) one-cell embryos. High-resolution single-cell RNA sequencing revealed previously inaccessible oocyte-to-embryo gene expression changes. This confirmed transcript depletion following fertilization (maternal RNA degradation) but also uncovered low-magnitude upregulation of hundreds of spliced transcripts. Gene expression analysis predicted embryonic processes including cell-cycle progression and chromosome maintenance as well as transcriptional activators that included cancer-associated gene regulators. Transcription was disrupted in abnormal monopronuclear (1PN) and tripronuclear (3PN) one-cell embryos. These findings indicate that human embryonic transcription initiates at the one-cell stage, sooner than previously thought. The pattern of gene upregulation promises to illuminate processes involved at the onset of human development, with implications for epigenetic inheritance, stem-cell-derived embryos, and cancer.

Identifiants

pubmed: 34936886
pii: S1934-5909(21)00484-7
doi: 10.1016/j.stem.2021.11.012
pmc: PMC8826644
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

209-216.e4

Subventions

Organisme : Medical Research Council
ID : MR/N000080/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S026193/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00014/5
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00014/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_12012/5
Pays : United Kingdom
Organisme : Medical Research Council
ID : G1000839
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N020294/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 208363/Z/17/Z
Pays : United Kingdom
Organisme : Cancer Research UK
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/S017593/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/P009506/1
Pays : United Kingdom

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

Mol Reprod Dev. 2005 Nov;72(3):281-90
pubmed: 16094646
PLoS One. 2013 Sep 10;8(9):e73987
pubmed: 24040138
Protein Cell. 2017 Oct;8(10):776-779
pubmed: 28825190
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Cell. 2017 Jan 26;168(3):442-459.e20
pubmed: 28111071
Dev Biol. 1988 Jul;128(1):15-20
pubmed: 2454852
Dev Cell. 2019 Jul 1;50(1):5-6
pubmed: 31265812
Brief Bioinform. 2018 Sep 28;19(5):776-792
pubmed: 28334202
Nat Commun. 2020 Oct 1;11(1):4917
pubmed: 33004802
Bioinformatics. 2015 Jan 15;31(2):166-9
pubmed: 25260700
J Reprod Infertil. 2019 Jul-Sep;20(3):127-131
pubmed: 31423415
Nat Rev Mol Cell Biol. 2020 May;21(5):255-267
pubmed: 32071436
Cell. 2018 Jul 12;174(2):391-405.e19
pubmed: 29937225
Nat Commun. 2021 Jun 21;12(1):3804
pubmed: 34155196
J Reprod Fertil. 1997 Mar;109(2):223-8
pubmed: 9155731
Nat Struct Mol Biol. 2013 Sep;20(9):1131-9
pubmed: 23934149
Sci Rep. 2018 Dec 17;8(1):17890
pubmed: 30559372
Biol Reprod. 2006 Dec;75(6):877-84
pubmed: 16943360
Mol Hum Reprod. 2010 Dec;16(12):938-43
pubmed: 20837506
Development. 2016 Oct 1;143(19):3459-3469
pubmed: 27578796
Hum Reprod. 1993 Jul;8(7):1101-9
pubmed: 8408494
Mol Hum Reprod. 1996 May;2(5):299-306
pubmed: 9238696
Dev Cell. 2017 Aug 21;42(4):316-332
pubmed: 28829942
J Biol Chem. 2011 Nov 25;286(47):40743-9
pubmed: 21953461
Reproduction. 2020 Nov;160(5):773-782
pubmed: 33065541
Am J Hum Genet. 2020 Jul 2;107(1):24-33
pubmed: 32502391
Nature. 2013 Aug 29;500(7464):593-7
pubmed: 23892778
Nat Genet. 2016 May;48(5):497-9
pubmed: 26974008
Cell. 2018 Mar 22;173(1):248-259.e15
pubmed: 29526463
Chromosoma. 1988;96(5):341-52
pubmed: 3409776
Biol Reprod. 1987 Sep;37(2):395-401
pubmed: 3676394
Cell. 2020 Jul 9;182(1):127-144.e23
pubmed: 32502394
Nat Methods. 2010 Dec;7(12):1009-15
pubmed: 21057496
Cell. 2016 May 5;165(4):1012-26
pubmed: 27062923
Dev Biol. 1988 Jan;125(1):181-6
pubmed: 3334716
Nat Cell Biol. 2019 Dec;21(12):1468-1478
pubmed: 31792376
Dev Cell. 2005 Sep;9(3):327-38
pubmed: 16139224
EMBO Rep. 2008 Mar;9(3):246-51
pubmed: 18311174
Cell Stem Cell. 2021 Jun 3;28(6):1016-1022.e4
pubmed: 33957081
Bioinformatics. 2014 Feb 15;30(4):523-30
pubmed: 24336805
Nat Genet. 2017 Jun;49(6):941-945
pubmed: 28459456
Cell. 2006 Apr 21;125(2):315-26
pubmed: 16630819
Development. 2000 Sep;127(17):3795-803
pubmed: 10934024
PLoS One. 2013 Oct 15;8(10):e77700
pubmed: 24143257
Nature. 2008 Nov 27;456(7221):470-6
pubmed: 18978772
Trends Genet. 2013 Oct;29(10):569-74
pubmed: 23810203
Dev Biol. 1988 Oct;129(2):304-14
pubmed: 2458285
Gigascience. 2019 Sep 1;8(9):
pubmed: 31531674
Stem Cell Rev Rep. 2009 Jun;5(2):140-58
pubmed: 19521804
Cancer Cell. 2005 May;7(5):433-44
pubmed: 15894264
J Appl Genet. 2018 Feb;59(1):43-57
pubmed: 29344903
J Biol Chem. 2006 Nov 17;281(46):34725-9
pubmed: 16987807
Fertil Steril. 1989 Mar;51(3):460-5
pubmed: 2920845
Nat Biotechnol. 2015 Mar;33(3):290-5
pubmed: 25690850
Nature. 2021 Mar;591(7851):620-626
pubmed: 33731924
Nat Methods. 2018 Apr;15(4):255-261
pubmed: 29481549
Genome Biol. 2010;11(3):R25
pubmed: 20196867
Trends Cell Biol. 2015 Feb;25(2):82-91
pubmed: 25448353
Hum Reprod Update. 2008 Sep-Oct;14(5):431-46
pubmed: 18603645
EMBO J. 2011 May 4;30(9):1841-51
pubmed: 21468028
Cell Rep. 2017 Jul 25;20(4):785-793
pubmed: 28746865
Nat Commun. 2021 Mar 1;12(1):1361
pubmed: 33649327
Nature. 1988 Mar 31;332(6163):459-61
pubmed: 3352746
Science. 2018 Oct 19;362(6412):356-360
pubmed: 30237246
Hum Reprod. 2011 Jun;26(6):1270-83
pubmed: 21502182
Nature. 2021 Mar;591(7851):627-632
pubmed: 33731926
Genome Biol. 2014 Feb 03;15(2):R29
pubmed: 24485249
Reprod Biomed Online. 2004 Oct;9(4):418-24
pubmed: 15511342
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
Mol Reprod Dev. 2000 Jun;56(2 Suppl):319-24
pubmed: 10824994
Development. 2011 Sep;138(17):3699-709
pubmed: 21775417
Nat Genet. 2017 Jun;49(6):925-934
pubmed: 28459457
Nature. 2018 May;557(7704):256-260
pubmed: 29720659
Mol Cell Biol. 2012 Jul;32(14):2722-37
pubmed: 22586272
Nat Biotechnol. 2011 Jan;29(1):24-6
pubmed: 21221095
Stem Cells. 2013 Jun;31(6):1051-63
pubmed: 23404835
Protein Cell. 2015 May;6(5):363-372
pubmed: 25894090
J Assist Reprod Genet. 2016 May;33(5):581-588
pubmed: 27052831
Hum Reprod. 2019 May 1;34(5):894-902
pubmed: 30863841
Am J Hum Genet. 2018 Apr 5;102(4):649-657
pubmed: 29606300
Cell Stem Cell. 2019 Nov 7;25(5):697-712.e6
pubmed: 31588047

Auteurs

Maki Asami (M)

Laboratory of Mammalian Molecular Embryology, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, England.

Brian Y H Lam (BYH)

MRC Metabolic Diseases Unit, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, University of Cambridge, Cambridge CB2 0QQ, England.

Marcella K Ma (MK)

MRC Metabolic Diseases Unit, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, University of Cambridge, Cambridge CB2 0QQ, England.

Kara Rainbow (K)

MRC Metabolic Diseases Unit, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, University of Cambridge, Cambridge CB2 0QQ, England.

Stefanie Braun (S)

Ovation Fertility Austin, Embryology and Andrology Laboratories, Austin, TX 78731, USA.

Matthew D VerMilyea (MD)

Ovation Fertility Austin, Embryology and Andrology Laboratories, Austin, TX 78731, USA. Electronic address: mvermilyea@ovationfertility.com.

Giles S H Yeo (GSH)

MRC Metabolic Diseases Unit, Wellcome-MRC Institute of Metabolic Science, Addenbrooke's Hospital, University of Cambridge, Cambridge CB2 0QQ, England. Electronic address: gshy2@cam.ac.uk.

Anthony C F Perry (ACF)

Laboratory of Mammalian Molecular Embryology, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, England. Electronic address: perry135@aol.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH