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 BronnerRobb Krumlauf, Christian Mosimann

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Article number3857
JournalNature Communications
Volume10
Issue number1
DOIs
StatePublished - Dec 1 2019

Fingerprint

Chordata
Mesoderm
Prednisolone
Muscle
Zebrafish
Transcription Factors
Genes
Tissue
Imaging techniques
Lancelets
draculin
Ambystoma mexicanum
Lampreys
connective tissue
smooth muscle
Gastrulation
vertebrates
chickens
embryos
kidneys

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

Cite this

Prummel, K. D., Hess, C., Nieuwenhuize, S., Parker, H. J., Rogers, K. W., Kozmikova, I., ... Mosimann, C. (2019). A conserved regulatory program initiates lateral plate mesoderm emergence across chordates. Nature Communications, 10(1), [3857]. https://doi.org/10.1038/s41467-019-11561-7

A conserved regulatory program initiates lateral plate mesoderm emergence across chordates. / Prummel, Karin D.; Hess, Christopher; Nieuwenhuize, Susan; Parker, Hugo J.; Rogers, Katherine W.; Kozmikova, Iryna; Racioppi, Claudia; Brombacher, Eline C.; Czarkwiani, Anna; Knapp, Dunja; Burger, Sibylle; Chiavacci, Elena; Shah, Gopi; Burger, Alexa; Huisken, Jan; Yun, Maximina H.; Christiaen, Lionel; Kozmik, Zbynek; Müller, Patrick; Bronner, Marianne; Krumlauf, Robb; Mosimann, Christian.

In: Nature Communications, Vol. 10, No. 1, 3857, 01.12.2019.

Research output: Contribution to journalArticle

Prummel, KD, Hess, C, Nieuwenhuize, S, Parker, HJ, Rogers, KW, Kozmikova, I, Racioppi, C, Brombacher, EC, Czarkwiani, A, Knapp, D, Burger, S, Chiavacci, E, Shah, G, Burger, A, Huisken, J, Yun, MH, Christiaen, L, Kozmik, Z, Müller, P, Bronner, M, Krumlauf, R & Mosimann, C 2019, 'A conserved regulatory program initiates lateral plate mesoderm emergence across chordates', Nature Communications, vol. 10, no. 1, 3857. https://doi.org/10.1038/s41467-019-11561-7
Prummel KD, Hess C, Nieuwenhuize S, Parker HJ, Rogers KW, Kozmikova I et al. A conserved regulatory program initiates lateral plate mesoderm emergence across chordates. Nature Communications. 2019 Dec 1;10(1). 3857. https://doi.org/10.1038/s41467-019-11561-7
Prummel, Karin D. ; Hess, Christopher ; Nieuwenhuize, Susan ; Parker, Hugo J. ; Rogers, Katherine W. ; Kozmikova, Iryna ; Racioppi, Claudia ; Brombacher, Eline C. ; Czarkwiani, Anna ; Knapp, Dunja ; Burger, Sibylle ; Chiavacci, Elena ; Shah, Gopi ; Burger, Alexa ; Huisken, Jan ; Yun, Maximina H. ; Christiaen, Lionel ; Kozmik, Zbynek ; Müller, Patrick ; Bronner, Marianne ; Krumlauf, Robb ; Mosimann, Christian. / A conserved regulatory program initiates lateral plate mesoderm emergence across chordates. In: Nature Communications. 2019 ; Vol. 10, No. 1.
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