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A conserved regulatory program initiates lateral plate mesoderm emergence across chordates

Prummel, Karin D. and Hess, Christopher and Nieuwenhuize, Susan and Parker, Hugo J. and Rogers, Katherine W. and Kozmikova, Iryna and Racioppi, Claudia and Brombacher, Eline C. and Czarkwiani, Anna and Knapp, Dunja and Burger, Sibylle and Chiavacci, Elena and Shah, Gopi and Burger, Alexa and Huisken, Jan and Yun, Maximina H. and Christiaen, Lionel and Kozmik, Zbynek and Müller, Patrick and Bronner, Marianne and Krumlauf, Robb and Mosimann, Christian (2019) A conserved regulatory program initiates lateral plate mesoderm emergence across chordates. Nature Communications, 10 . Art. no. 3857. ISSN 2041-1723. PMCID PMC6710290. https://resolver.caltech.edu/CaltechAUTHORS:20190903-130241403

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41467-019-11561-7DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6710290/PubMed CentralArticle
ORCID:
AuthorORCID
Parker, Hugo J.0000-0001-7646-2007
Kozmikova, Iryna0000-0002-7861-9802
Racioppi, Claudia0000-0001-8117-1124
Czarkwiani, Anna0000-0002-8845-3113
Knapp, Dunja0000-0002-7533-2208
Chiavacci, Elena0000-0003-3924-3635
Shah, Gopi0000-0002-0154-9455
Burger, Alexa0000-0001-7137-3910
Huisken, Jan0000-0001-7250-3756
Yun, Maximina H.0000-0001-9019-2453
Christiaen, Lionel0000-0001-5930-5667
Kozmik, Zbynek0000-0002-5850-2105
Müller, Patrick0000-0002-0702-6209
Bronner, Marianne0000-0003-4274-1862
Krumlauf, Robb0000-0001-9102-7927
Mosimann, Christian0000-0002-0749-2576
Additional Information:© The Author(s) 2019. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received: 8 April 2019. Accepted: 22 July 2019. Published online: 26 August 2019. 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. Data availability: The authors declare that the data supporting the findings of this study are available within the paper and its supplementary information files. Original data underlying the lamprey experiments in this manuscript are accessible from the Stowers Original Data Repository at http://odr.stowers.org/websimr/. The source data underlying Fig. 2j and Supplementary Fig. 2b and 10m are provided as a Source Data file. Reagents are available upon request. These authors contributed equally: Karin D. Prummel, Christopher Hess. Author Contributions: K.D.P., C.H., S.N., E.C.B., S.B., and C.M. designed, performed, and interpreted the zebrafish experiments; S.N., E.C., and A.B. established and performed the chicken experiments; K.D.P. performed the lightsheet imaging with technical and equipment support by G.S. and J.H.; K.W.R. and P.M. provided and generated mutants and maternal-zygotic mutant zebrafish; H.J.P., M.B., and R.K. designed, performed, and interpreted the lamprey experiments; A.C., D.K., and M.H.Y. designed, performed, and interpreted the axolotl experiments; C.R. and L.C. designed, performed, and interpreted the Ciona experiments; I.K. and Z.K. designed, performed, and interpreted the amphioxus experiments; A.C., D.K., and M.H.Y. designed and performed the axolotl experiments; K.D.P., C.H., S.N., and C.M. assembled and wrote the manuscript with contributions from all co-authors. The authors declare no competing interests. Nature Communications thanks the anonymous reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.
Funders:
Funding AgencyGrant Number
Swiss National Science Foundation (SNSF)PP00P3_139093
Swiss National Science Foundation (SNSF)150838
Marie Curie FellowshipCIG PCIG14-GA-2013-631984
Canton of ZürichUNSPECIFIED
UZH Foundation for Research in Science and the HumanitiesUNSPECIFIED
Swiss Heart FoundationUNSPECIFIED
ZUNIV FAN/UZH AlumniUNSPECIFIED
Universität ZürichUNSPECIFIED
EuFishBioMedUNSPECIFIED
Company of BiologistsUNSPECIFIED
Stowers Institute1001
NIHHL108643
Leducq Foundation15CVD01
European Molecular Biology Organization (EMBO)ALTF 1608-2014
Alexander von Humboldt FoundationUNSPECIFIED
Deutsche Forschungsgemeinschaft (DFG)DFG FZ 111
Deutsche Forschungsgemeinschaft (DFG)DFG EXC 168
Czech Science Foundation17-15374
PubMed Central ID:PMC6710290
Record Number:CaltechAUTHORS:20190903-130241403
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190903-130241403
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:98397
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:03 Sep 2019 20:40
Last Modified:03 Oct 2019 21:40

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