Hand2 delineates mesothelium progenitors and is reactivated in mesothelioma

Karin D. Prummel, Helena L. Crowell, Susan Nieuwenhuize, Eline C. Brombacher, Stephan Daetwyler, Charlotte Soneson, Jelena Kresoja-Rakic, Agnese Kocere, Manuel Ronner, Alexander Ernst, Zahra Labbaf, David E. Clouthier, Anthony B. Firulli, Héctor Sánchez-Iranzo, Sundar R. Naganathan, Rebecca O’Rourke, Erez Raz, Nadia Mercader, Alexa Burger, Emanuela Felley-Bosco, Jan Huisken, Mark D. Robinson and Christian Mosimann ()
Additional contact information
Karin D. Prummel: University of Colorado School of Medicine, Anschutz Medical Campus
Helena L. Crowell: University of Zurich
Susan Nieuwenhuize: University of Colorado School of Medicine, Anschutz Medical Campus
Eline C. Brombacher: University of Zurich
Stephan Daetwyler: Max Planck Institute of Molecular Cell Biology and Genetics
Charlotte Soneson: University of Zurich
Jelena Kresoja-Rakic: University of Colorado School of Medicine, Anschutz Medical Campus
Agnese Kocere: University of Colorado School of Medicine, Anschutz Medical Campus
Manuel Ronner: University Hospital Zurich
Alexander Ernst: University of Bern
Zahra Labbaf: Institute for Cell Biology, ZMBE
David E. Clouthier: University of Colorado Anschutz Medical Campus
Anthony B. Firulli: Indiana Medical School
Héctor Sánchez-Iranzo: Centro Nacional de Investigaciones Cardiovasculares (CNIC-ISCIII)
Sundar R. Naganathan: Ecole Polytechnique Federale de Lausanne
Rebecca O’Rourke: University of Colorado School of Medicine, Anschutz Medical Campus
Erez Raz: Institute for Cell Biology, ZMBE
Nadia Mercader: University of Bern
Alexa Burger: University of Colorado School of Medicine, Anschutz Medical Campus
Emanuela Felley-Bosco: University Hospital Zurich
Jan Huisken: Max Planck Institute of Molecular Cell Biology and Genetics
Mark D. Robinson: University of Zurich
Christian Mosimann: University of Colorado School of Medicine, Anschutz Medical Campus

Nature Communications, 2022, vol. 13, issue 1, 1-21

Abstract: Abstract The mesothelium lines body cavities and surrounds internal organs, widely contributing to homeostasis and regeneration. Mesothelium disruptions cause visceral anomalies and mesothelioma tumors. Nonetheless, the embryonic emergence of mesothelia remains incompletely understood. Here, we track mesothelial origins in the lateral plate mesoderm (LPM) using zebrafish. Single-cell transcriptomics uncovers a post-gastrulation gene expression signature centered on hand2 in distinct LPM progenitor cells. We map mesothelial progenitors to lateral-most, hand2-expressing LPM and confirm conservation in mouse. Time-lapse imaging of zebrafish hand2 reporter embryos captures mesothelium formation including pericardium, visceral, and parietal peritoneum. We find primordial germ cells migrate with the forming mesothelium as ventral migration boundary. Functionally, hand2 loss disrupts mesothelium formation with reduced progenitor cells and perturbed migration. In mouse and human mesothelioma, we document expression of LPM-associated transcription factors including Hand2, suggesting re-initiation of a developmental program. Our data connects mesothelium development to Hand2, expanding our understanding of mesothelial pathologies.

Date: 2022
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Persistent link: https://EconPapers.repec.org/RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29311-7

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DOI: 10.1038/s41467-022-29311-7

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