Dynamics of primitive streak regression controls the fate of neuromesodermal progenitors in the chicken embryo.

bipotency body axis formation cell biology cell dynamics chicken developmental biology direct lineage tracing neuromesodermal progenitor single cell analysis

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
06 07 2021
Historique:
received: 12 11 2020
accepted: 23 06 2021
entrez: 6 7 2021
pubmed: 7 7 2021
medline: 23 9 2021
Statut: epublish

Résumé

In classical descriptions of vertebrate development, the segregation of the three embryonic germ layers completes by the end of gastrulation. Body formation then proceeds in a head to tail fashion by progressive deposition of lineage-committed progenitors during regression of the primitive streak (PS) and tail bud (TB). The identification by retrospective clonal analysis of a population of neuromesodermal progenitors (NMPs) contributing to both musculoskeletal precursors (paraxial mesoderm) and spinal cord during axis formation challenged these notions. However, classical fate mapping studies of the PS region in amniotes have so far failed to provide direct evidence for such bipotential cells at the single-cell level. Here, using lineage tracing and single-cell RNA sequencing in the chicken embryo, we identify a resident cell population of the anterior PS epiblast, which contributes to neural and mesodermal lineages in trunk and tail. These cells initially behave as monopotent progenitors as classically described and only acquire a bipotential fate later, in more posterior regions. We show that NMPs exhibit a conserved transcriptomic signature during axis elongation but lose their epithelial characteristicsin the TB. Posterior to anterior gradients of convergence speed and ingression along the PS lead to asymmetric exhaustion of PS mesodermal precursor territories. Through limited ingression and increased proliferation, NMPs are maintained and amplified as a cell population which constitute the main progenitors in the TB. Together, our studies provide a novel understanding of the PS and TB contribution through the NMPs to the formation of the body of amniote embryos.

Identifiants

pubmed: 34227938
doi: 10.7554/eLife.64819
pii: 64819
pmc: PMC8260230
doi:
pii:

Banques de données

GEO
['GSE161905', 'GSE114186']

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NICHD NIH HHS
ID : R01 HD097068
Pays : United States
Organisme : EMBO
ID : ALTF 406-2015

Informations de copyright

© 2021, Guillot et al.

Déclaration de conflit d'intérêts

CG, YD, AM, BR, OP No competing interests declared

Références

Nature. 2019 Feb;566(7745):490-495
pubmed: 30787436
Dev Cell. 2017 Feb 27;40(4):331-341.e4
pubmed: 28245920
Dev Cell. 2002 Sep;3(3):425-37
pubmed: 12361604
Development. 2008 Jul;135(13):2289-99
pubmed: 18508860
Development. 2002 Oct;129(20):4855-66
pubmed: 12361976
Neuron. 2014 Feb 5;81(3):505-20
pubmed: 24507188
Development. 2014 Nov;141(22):4243-53
pubmed: 25371361
Development. 1996 Sep;122(9):2933-46
pubmed: 8787766
J Exp Zool. 1947 Feb;104(1):69-100
pubmed: 20285008
Int J Dev Biol. 1998;42(7):909-16
pubmed: 9853821
Dev Dyn. 2001 Mar;220(3):284-9
pubmed: 11241836
Nature. 2020 Jun;582(7812):405-409
pubmed: 32076263
Development. 2017 Dec 01;144(23):4462-4472
pubmed: 28835474
Proc Natl Acad Sci U S A. 2006 Dec 26;103(52):19806-11
pubmed: 17179040
Development. 2019 Jun 24;146(12):
pubmed: 31152001
Development. 1991 Jun;112(2):615-26
pubmed: 1794328
PLoS Biol. 2012;10(10):e1001415
pubmed: 23118616
Nature. 2018 Oct;562(7726):272-276
pubmed: 30283134
Nat Neurosci. 2011 Aug 30;14(11):1481-8
pubmed: 21878933
Dev Biol. 1997 Jan 1;181(1):102-15
pubmed: 9015268
Development. 2018 Nov 9;145(21):
pubmed: 30333213
Dev Biol. 2011 May 15;353(2):309-20
pubmed: 21397594
Development. 2007 Aug;134(15):2829-40
pubmed: 17611225
Development. 1997 Feb;124(4):881-93
pubmed: 9043069
PLoS Biol. 2014 Aug 26;12(8):e1001937
pubmed: 25157815
Mech Dev. 1995 May;51(1):51-65
pubmed: 7669693
J Exp Zool. 1993 Nov 15;267(4):431-46
pubmed: 8270895
Bioinformatics. 2011 Jun 15;27(12):1739-40
pubmed: 21546393
EMBO Rep. 2004 Jul;5(7):728-33
pubmed: 15192698
Dev Biol. 2020 May 15;461(2):160-171
pubmed: 32059837
Dev Cell. 2017 May 8;41(3):243-261.e7
pubmed: 28457792
PeerJ. 2014 Jun 19;2:e453
pubmed: 25024921
Development. 2003 Aug;130(16):3807-19
pubmed: 12835396
Nature. 2010 Jul 8;466(7303):248-52
pubmed: 20613841
Elife. 2015 Feb 26;4:
pubmed: 25719209
Methods Cell Biol. 2008;87:257-70
pubmed: 18485301
Mech Dev. 1996 Mar;55(1):79-89
pubmed: 8734501
Development. 1999 Nov;126(21):4691-701
pubmed: 10518487
Dev Cell. 2017 Feb 27;40(4):342-353.e10
pubmed: 28245921
Cell. 2019 Feb 7;176(4):928-943.e22
pubmed: 30712874
Wilhelm Roux Arch Entwickl Mech Org. 1929 Jun;119(1):188-321
pubmed: 28353845
Anat Rec. 1947 Dec;99(4):653
pubmed: 18935458
Development. 1987 Jan;99(1):109-26
pubmed: 3652985
Elife. 2020 Jun 29;9:
pubmed: 32597756
Development. 1993 Dec;119(4):991-1004
pubmed: 7916680
Curr Biol. 2019 Jan 7;29(1):35-50.e4
pubmed: 30554902
Anat Embryol (Berl). 1979 Jul 26;156(3):319-29
pubmed: 475001
Development. 2019 May 20;146(10):
pubmed: 31023877
Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50
pubmed: 16199517
Curr Protoc Mol Biol. 2001 May;Chapter 9:Unit9.14
pubmed: 18265282
Curr Biol. 2000 Jul 13;10(14):869-72
pubmed: 10899008
Dev Dyn. 1992 Mar;193(3):235-48
pubmed: 1600242
Neuron. 2015 Sep 2;87(5):999-1007
pubmed: 26299474
Elife. 2016 Jan 18;5:e10042
pubmed: 26780186
Dev Dyn. 1992 Dec;195(4):231-72
pubmed: 1304821
Development. 2015 Sep 1;142(17):2864-75
pubmed: 26329597
J Struct Biol. 2005 Aug;151(2):182-95
pubmed: 16043363
Genes Dev. 1997 Mar 1;11(5):603-15
pubmed: 9119225
Dev Cell. 2021 Jan 11;56(1):141-153.e6
pubmed: 33308481
Dev Cell. 2009 Sep;17(3):365-76
pubmed: 19758561
Development. 2000 Jan;127(2):255-67
pubmed: 10603344
Development. 1996 May;122(5):1523-34
pubmed: 8625839
Development. 2009 May;136(10):1591-604
pubmed: 19395637
Nature. 2020 Apr;580(7801):113-118
pubmed: 31915384
J Virol. 1992 Aug;66(8):5110-3
pubmed: 1321291
Cell. 2018 Oct 18;175(3):859-876.e33
pubmed: 30318151
Dev Dyn. 1994 Nov;201(3):279-89
pubmed: 7881130
Cell. 1995 Nov 17;83(4):641-53
pubmed: 7585967
Cell Stem Cell. 2020 Feb 6;26(2):172-186.e6
pubmed: 31956040
Nat Methods. 2009 May;6(5):343-5
pubmed: 19363495
Proc Natl Acad Sci U S A. 2007 Feb 20;104(8):2744-9
pubmed: 17299044
Cell. 2015 May 21;161(5):1187-1201
pubmed: 26000487
Development. 2019 Jan 2;146(1):
pubmed: 30559277
Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11400-6
pubmed: 8876147
Development. 2002 Jun;129(12):2807-22
pubmed: 12050131

Auteurs

Charlene Guillot (C)

Department of Pathology, Brigham and Women's Hospital, Boston, United States.
Department of Genetics, Harvard Medical School, Boston, United States.
Harvard Stem Cell Institute, Boston, United States.

Yannis Djeffal (Y)

Department of Pathology, Brigham and Women's Hospital, Boston, United States.
Department of Genetics, Harvard Medical School, Boston, United States.
Harvard Stem Cell Institute, Boston, United States.

Arthur Michaut (A)

Department of Pathology, Brigham and Women's Hospital, Boston, United States.
Department of Genetics, Harvard Medical School, Boston, United States.
Harvard Stem Cell Institute, Boston, United States.

Brian Rabe (B)

Department of Genetics, Harvard Medical School, Boston, United States.
Howard Hughes Medical Institute, Boston, United States.

Olivier Pourquié (O)

Department of Pathology, Brigham and Women's Hospital, Boston, United States.
Department of Genetics, Harvard Medical School, Boston, United States.
Harvard Stem Cell Institute, Boston, United States.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH