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; Christian Mosimann

doi:10.1038/s41467-019-11561-7

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

Biology and Genomics

Research output: Contribution to journal › Article › peer-review

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 language	English (US)
Article number	3857
Journal	Nature communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-11561-7
State	Published - Dec 1 2019

ASJC Scopus subject areas

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

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10.1038/s41467-019-11561-7

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Prummel, K. D., Hess, C., Nieuwenhuize, S., Parker, H. J., Rogers, K. W., Kozmikova, I., Racioppi, C., Brombacher, E. C., Czarkwiani, A., Knapp, D., Burger, S., Chiavacci, E., Shah, G., Burger, A., Huisken, J., Yun, M. H., Christiaen, L., Kozmik, Z., Müller, P., ... 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

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

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title = "A conserved regulatory program initiates lateral plate mesoderm emergence across chordates",

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.",

author = "Prummel, {Karin D.} and Christopher Hess and Susan Nieuwenhuize and Parker, {Hugo J.} and Rogers, {Katherine W.} and Iryna Kozmikova and Claudia Racioppi and Brombacher, {Eline C.} and Anna Czarkwiani and Dunja Knapp and Sibylle Burger and Elena Chiavacci and Gopi Shah and Alexa Burger and Jan Huisken and Yun, {Maximina H.} and Lionel Christiaen and Zbynek Kozmik and Patrick M{\"u}ller and Marianne Bronner and Robb Krumlauf and Christian Mosimann",

note = "Funding Information: We thank Seraina B{\"o}tschi, Lukas Obernosterer, and Vesna Barros for technical and husbandry support; the lab of Stephan Neuhauss for zebrafish husbandry support; the labs of Esther St{\"o}ckli and Jerome Gros for chicken experimentation support; the ZMB at UZH for imaging support; Fiona Wardle for input and support on the ChIP-seq panel in Fig. 5a; the lab of Magdalini Polymenidou for vibratome access; Karol{\'i}na Ditrychov{\'a} for cloning the pKD001 construct; Rebecca Burdine for sharing transcription factor constructs; Mark Miller for animal illustrations in Fig. 7a; the Stowers Institute histology facility for assistance with lamprey embryo sectioning; Hans-Henning Epperlein for discussions on salamander embryology; Diego Safian for suggesting Genomicus for synteny analysis; and all members of the Mosimann lab for constructive input. This work has been supported by a Swiss National Science Foundation (SNSF) professorship [PP00P3_139093] and SNSF R{\textquoteright}Equip grant 150838 (Lightsheet Fluorescence Microscopy), a Marie Curie Career Integration Grant from the European Commission [CIG PCIG14-GA-2013-631984], the Canton of Z{\"u}rich, the UZH Foundation for Research in Science and the Humanities, the Swiss Heart Foundation, and the ZUNIV FAN/UZH Alumni to C.M.; a UZH CanDoc to C.H.; EuFishBioMed and Company of Biologists travel fellowships to K.D.P.; the Stowers Institute (grant #1001) to H.J.P. and R.K.; NIH/NHLBI R01 award HL108643, trans-Atlantic network of excellence award 15CVD01 from the Leducq Foundation to L.C.; a long-term fellowship ALTF 1608-2014 from EMBO to C.R.; Alexander von Humboldt fellowship to A.C. and DFG Research Center (DFG FZ 111) and Cluster of Excellence (DFG EXC 168) funds to M.H.Y.; Czech Science Foundation 17-15374 S to Z.K. Publisher Copyright: {\textcopyright} 2019, The Author(s).",

year = "2019",

month = dec,

day = "1",

doi = "10.1038/s41467-019-11561-7",

language = "English (US)",

volume = "10",

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T1 - A conserved regulatory program initiates lateral plate mesoderm emergence across chordates

AU - Prummel, Karin D.

AU - Hess, Christopher

AU - Nieuwenhuize, Susan

AU - Parker, Hugo J.

AU - Rogers, Katherine W.

AU - Kozmikova, Iryna

AU - Racioppi, Claudia

AU - Brombacher, Eline C.

AU - Czarkwiani, Anna

AU - Knapp, Dunja

AU - Burger, Sibylle

AU - Chiavacci, Elena

AU - Shah, Gopi

AU - Burger, Alexa

AU - Huisken, Jan

AU - Yun, Maximina H.

AU - Christiaen, Lionel

AU - Kozmik, Zbynek

AU - Müller, Patrick

AU - Bronner, Marianne

AU - Krumlauf, Robb

AU - Mosimann, Christian

N1 - Funding Information: We thank Seraina Bötschi, Lukas Obernosterer, and Vesna Barros for technical and husbandry support; the lab of Stephan Neuhauss for zebrafish husbandry support; the labs of Esther Stöckli and Jerome Gros for chicken experimentation support; the ZMB at UZH for imaging support; Fiona Wardle for input and support on the ChIP-seq panel in Fig. 5a; the lab of Magdalini Polymenidou for vibratome access; Karolína Ditrychová for cloning the pKD001 construct; Rebecca Burdine for sharing transcription factor constructs; Mark Miller for animal illustrations in Fig. 7a; the Stowers Institute histology facility for assistance with lamprey embryo sectioning; Hans-Henning Epperlein for discussions on salamander embryology; Diego Safian for suggesting Genomicus for synteny analysis; and all members of the Mosimann lab for constructive input. This work has been supported by a Swiss National Science Foundation (SNSF) professorship [PP00P3_139093] and SNSF R’Equip grant 150838 (Lightsheet Fluorescence Microscopy), a Marie Curie Career Integration Grant from the European Commission [CIG PCIG14-GA-2013-631984], the Canton of Zürich, the UZH Foundation for Research in Science and the Humanities, the Swiss Heart Foundation, and the ZUNIV FAN/UZH Alumni to C.M.; a UZH CanDoc to C.H.; EuFishBioMed and Company of Biologists travel fellowships to K.D.P.; the Stowers Institute (grant #1001) to H.J.P. and R.K.; NIH/NHLBI R01 award HL108643, trans-Atlantic network of excellence award 15CVD01 from the Leducq Foundation to L.C.; a long-term fellowship ALTF 1608-2014 from EMBO to C.R.; Alexander von Humboldt fellowship to A.C. and DFG Research Center (DFG FZ 111) and Cluster of Excellence (DFG EXC 168) funds to M.H.Y.; Czech Science Foundation 17-15374 S to Z.K. Publisher Copyright: © 2019, The Author(s).

PY - 2019/12/1

Y1 - 2019/12/1

N2 - 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.

AB - 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.

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A conserved regulatory program initiates lateral plate mesoderm emergence across chordates

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