A conserved regulatory program initiates lateral plate mesoderm emergence across chordates.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
26 08 2019
Historique:
received: 08 04 2019
accepted: 22 07 2019
entrez: 28 8 2019
pubmed: 28 8 2019
medline: 18 12 2019
Statut: epublish

Résumé

Cardiovascular lineages develop together with kidney, smooth muscle, and limb connective tissue progenitors from the lateral plate mesoderm (LPM). How the LPM initially emerges and how its downstream fates are molecularly interconnected remain unknown. Here, we isolate a pan-LPM enhancer in the zebrafish-specific draculin (drl) gene that provides specific LPM reporter activity from early gastrulation. In toto live imaging and lineage tracing of drl-based reporters captures the dynamic LPM emergence as lineage-restricted mesendoderm field. The drl pan-LPM enhancer responds to the transcription factors EomesoderminA, FoxH1, and MixL1 that combined with Smad activity drive LPM emergence. We uncover specific activity of zebrafish-derived drl reporters in LPM-corresponding territories of several chordates including chicken, axolotl, lamprey, Ciona, and amphioxus, revealing a universal upstream LPM program. Altogether, our work provides a mechanistic framework for LPM emergence as defined progenitor field, possibly representing an ancient mesodermal cell state that predates the primordial vertebrate embryo.

Identifiants

pubmed: 31451684
doi: 10.1038/s41467-019-11561-7
pii: 10.1038/s41467-019-11561-7
pmc: PMC6710290
doi:

Substances chimiques

Zebrafish Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3857

Subventions

Organisme : NHLBI NIH HHS
ID : R01 HL108643
Pays : United States

Références

Science. 2016 Jan 29;351(6272):aad2197
pubmed: 26823433
Dev Biol. 1999 Nov 15;215(2):343-57
pubmed: 10545242
Nature. 2015 Apr 23;520(7548):466-73
pubmed: 25903628
Cell. 1999 Apr 2;97(1):121-32
pubmed: 10199408
Dev Biol. 2008 Jun 1;318(1):52-64
pubmed: 18436202
Genes Dev. 2000 Feb 15;14(4):435-51
pubmed: 10691736
PLoS Genet. 2009 Dec;5(12):e1000762
pubmed: 20011110
Nat Commun. 2014 Sep 05;5:4830
pubmed: 25189217
Dev Biol. 2005 Jul 1;283(1):85-96
pubmed: 15890328
Nat Commun. 2018 Jan 30;9(1):440
pubmed: 29382828
J Exp Zool B Mol Dev Evol. 2007 Jul 15;308(4):484-93
pubmed: 17520703
Development. 2017 Feb 1;144(3):464-478
pubmed: 28049660
Nat Commun. 2015 Aug 26;6:8146
pubmed: 26306682
Dev Cell. 2005 Oct;9(4):523-33
pubmed: 16198294
Dev Dyn. 2007 Sep;236(9):2410-20
pubmed: 17477393
Cell Stem Cell. 2014 Sep 4;15(3):310-325
pubmed: 25042702
Dev Dyn. 2004 Feb;229(2):328-33
pubmed: 14745957
Development. 2002 Nov;129(21):4901-14
pubmed: 12397099
Nature. 2014 Oct 23;514(7523):490-3
pubmed: 25219855
Development. 1999 Sep;126(17):3735-45
pubmed: 10433904
Development. 2015 Jun 1;142(11):1937-47
pubmed: 26015537
Development. 2005 Aug;132(15):3405-17
pubmed: 15987774
Oncogene. 2004 Sep 20;23(43):7233-46
pubmed: 15378083
Mar Genomics. 2015 Dec;24 Pt 2:159-66
pubmed: 26094865
Development. 2003 Nov;130(22):5503-17
pubmed: 14530296
Development. 2017 Jun 15;144(12):2104-2122
pubmed: 28634270
Stem Cells. 2009 Dec;27(12):2884-95
pubmed: 19711456
Nature. 1996 Oct 24;383(6602):691-6
pubmed: 8878477
Dev Biol. 2009 Mar 15;327(2):590-602
pubmed: 19159624
Evodevo. 2018 Jun 21;9:16
pubmed: 29977493
Science. 2014 Dec 12;346(6215):1311-20
pubmed: 25504712
Development. 2005 Nov;132(21):4811-8
pubmed: 16207759
Genesis. 2000 Apr;26(4):225-9
pubmed: 10748458
Nat Cell Biol. 2014 Jan;16(1):118-26
pubmed: 24335651
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
PLoS Genet. 2011 May;7(5):e1002072
pubmed: 21637786
BMC Biol. 2014 Oct 03;12:81
pubmed: 25277163
Development. 1999 May;126(10):2149-59
pubmed: 10207140
Curr Opin Genet Dev. 2015 Jun;32:119-28
pubmed: 25819888
Dev Biol. 2011 Nov 1;359(1):124-136
pubmed: 21864524
Genetics. 2012 Sep;192(1):55-66
pubmed: 22964837
Nat Commun. 2018 May 21;9(1):2001
pubmed: 29784942
Dev Biol. 2010 May 1;341(1):315-23
pubmed: 20171204
Elife. 2015 Apr 14;4:
pubmed: 25869585
Sci Rep. 2014 Jul 23;4:5791
pubmed: 25051985
Nature. 2009 Jun 4;459(7247):708-11
pubmed: 19396158
Cell Rep. 2017 Jun 27;19(13):2782-2795
pubmed: 28658625
Pharm Acta Helv. 1996 Jun;71(1):29-35
pubmed: 8786996
BMC Genomics. 2011 Dec 30;12:637
pubmed: 22208168
Genesis. 2001 Apr;29(4):172-9
pubmed: 11309850
Dev Biol. 2003 Mar 1;255(1):128-37
pubmed: 12618138
Dev Cell. 2017 Mar 27;40(6):595-607.e4
pubmed: 28325473
Nature. 2013 Oct 17;502(7471):309-10
pubmed: 24025771
Cell Stem Cell. 2017 Aug 3;21(2):179-194.e4
pubmed: 28777944
Nat Commun. 2013;4:2207
pubmed: 23884240
Dev Biol. 2013 Mar 15;375(2):182-92
pubmed: 23201012
Nature. 2012 May 13;485(7400):599-604
pubmed: 22660318
Genes Dev. 2000 May 15;14(10):1279-89
pubmed: 10817762
Annu Rev Genet. 2011;45:357-77
pubmed: 21942367
Cell. 2008 Feb 22;132(4):661-80
pubmed: 18295582
Int J Dev Biol. 2003;47(7-8):531-9
pubmed: 14756329
Development. 2008 Feb;135(3):501-11
pubmed: 18171685
Development. 2016 Aug 1;143(15):2842-52
pubmed: 27385009
Nature. 1996 Jul 25;382(6589):357-60
pubmed: 8684465
Nat Cell Biol. 2011 Aug 07;13(9):1084-91
pubmed: 21822279
Nat Protoc. 2014 Mar;9(3):529-40
pubmed: 24504478
PLoS Genet. 2009 Jan;5(1):e1000325
pubmed: 19119423
Science. 1998 Jul 3;281(5373):91-6
pubmed: 9651252
Development. 2003 Dec;130(23):5589-99
pubmed: 14522874
Development. 1999 Feb;126(3):423-34
pubmed: 9876172

Auteurs

Karin D Prummel (KD)

Institute of Molecular Life Sciences, University of Zurich, Zürich, 8057, Switzerland.

Christopher Hess (C)

Institute of Molecular Life Sciences, University of Zurich, Zürich, 8057, Switzerland.

Susan Nieuwenhuize (S)

Institute of Molecular Life Sciences, University of Zurich, Zürich, 8057, Switzerland.

Hugo J Parker (HJ)

Department of Anatomy and Cell Biology, Kansas University Medical Center, Kansas City, KS, 66160, USA.
Stowers Institute for Medical Research, Kansas City, MO, 64110, USA.

Katherine W Rogers (KW)

Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, 72076, Germany.

Iryna Kozmikova (I)

Institute of Molecular Genetics of the ASCR, Prague, 142 20, Czech Republic.

Claudia Racioppi (C)

Center for Developmental Genetics, Department of Biology, New York University, New York, NY, 10003, USA.

Eline C Brombacher (EC)

Institute of Molecular Life Sciences, University of Zurich, Zürich, 8057, Switzerland.

Anna Czarkwiani (A)

TUD-CRTD Center for Regenerative Therapies Dresden, Dresden, 01307, Germany.

Dunja Knapp (D)

TUD-CRTD Center for Regenerative Therapies Dresden, Dresden, 01307, Germany.

Sibylle Burger (S)

Institute of Molecular Life Sciences, University of Zurich, Zürich, 8057, Switzerland.

Elena Chiavacci (E)

Institute of Molecular Life Sciences, University of Zurich, Zürich, 8057, Switzerland.

Gopi Shah (G)

Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, 01307, Germany.

Alexa Burger (A)

Institute of Molecular Life Sciences, University of Zurich, Zürich, 8057, Switzerland.

Jan Huisken (J)

Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, 01307, Germany.
Morgridge Institute for Research, Madison, WI, 53715, USA.

Maximina H Yun (MH)

TUD-CRTD Center for Regenerative Therapies Dresden, Dresden, 01307, Germany.
Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, 01307, Germany.

Lionel Christiaen (L)

Center for Developmental Genetics, Department of Biology, New York University, New York, NY, 10003, USA.

Zbynek Kozmik (Z)

Institute of Molecular Genetics of the ASCR, Prague, 142 20, Czech Republic.

Patrick Müller (P)

Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, 72076, Germany.

Marianne Bronner (M)

Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, 91125, USA.

Robb Krumlauf (R)

Department of Anatomy and Cell Biology, Kansas University Medical Center, Kansas City, KS, 66160, USA.
Stowers Institute for Medical Research, Kansas City, MO, 64110, USA.

Christian Mosimann (C)

Institute of Molecular Life Sciences, University of Zurich, Zürich, 8057, Switzerland. christian.mosimann@imls.uzh.ch.

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