A conserved regulatory program initiates lateral plate mesoderm emergence across chordates

Karin D. Prummel, Christopher Hess, Susan Nieuwenhuize, Hugo J. Parker, Katherine W. Rogers, Iryna Kozmikova, Claudia Racioppi, Eline C. Brombacher, Anna Czarkwiani, Dunja Knapp, Sibylle Burger, Elena Chiavacci, Gopi Shah, Alexa Burger, Jan Huisken, Maximina H. Yun, Lionel Christiaen, Zbynek Kozmik, Patrick Müller, Marianne Bronner, Robb Krumlauf and Christian Mosimann ()
Additional contact information
Karin D. Prummel: University of Zurich
Christopher Hess: University of Zurich
Susan Nieuwenhuize: University of Zurich
Hugo J. Parker: Kansas University Medical Center
Katherine W. Rogers: Friedrich Miescher Laboratory of the Max Planck Society
Iryna Kozmikova: Institute of Molecular Genetics of the ASCR
Claudia Racioppi: New York University
Eline C. Brombacher: University of Zurich
Anna Czarkwiani: TUD-CRTD Center for Regenerative Therapies Dresden
Dunja Knapp: TUD-CRTD Center for Regenerative Therapies Dresden
Sibylle Burger: University of Zurich
Elena Chiavacci: University of Zurich
Gopi Shah: Max Planck Institute of Molecular Cell Biology and Genetics
Alexa Burger: University of Zurich
Jan Huisken: Max Planck Institute of Molecular Cell Biology and Genetics
Maximina H. Yun: TUD-CRTD Center for Regenerative Therapies Dresden
Lionel Christiaen: New York University
Zbynek Kozmik: Institute of Molecular Genetics of the ASCR
Patrick Müller: Friedrich Miescher Laboratory of the Max Planck Society
Marianne Bronner: California Institute of Technology
Robb Krumlauf: Kansas University Medical Center
Christian Mosimann: University of Zurich

Nature Communications, 2019, vol. 10, issue 1, 1-15

Abstract: Abstract 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.

Date: 2019
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DOI: 10.1038/s41467-019-11561-7

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