LETR1 is a lymphatic endothelial-specific lncRNA governing cell proliferation and migration through KLF4 and SEMA3C

Luca Ducoli, Saumya Agrawal, Eliane Sibler, Tsukasa Kouno, Carlotta Tacconi, Chung-Chao Hon, Simone D. Berger, Daniela Müllhaupt, Yuliang He, Jihye Kim, Marco D’Addio, Lothar C. Dieterich, Piero Carninci, Michiel J. L. Hoon, Jay W. Shin () and Michael Detmar ()
Additional contact information
Luca Ducoli: Swiss Federal Institute of Technology (ETH) Zurich
Saumya Agrawal: RIKEN Center for Integrative Medical Sciences
Eliane Sibler: Swiss Federal Institute of Technology (ETH) Zurich
Tsukasa Kouno: RIKEN Center for Integrative Medical Sciences
Carlotta Tacconi: Swiss Federal Institute of Technology (ETH) Zurich
Chung-Chao Hon: RIKEN Center for Integrative Medical Sciences
Simone D. Berger: Swiss Federal Institute of Technology (ETH) Zurich
Daniela Müllhaupt: Swiss Federal Institute of Technology (ETH) Zurich
Yuliang He: Swiss Federal Institute of Technology (ETH) Zurich
Jihye Kim: Swiss Federal Institute of Technology (ETH) Zurich
Marco D’Addio: Swiss Federal Institute of Technology (ETH) Zurich
Lothar C. Dieterich: Swiss Federal Institute of Technology (ETH) Zurich
Piero Carninci: RIKEN Center for Integrative Medical Sciences
Michiel J. L. Hoon: RIKEN Center for Integrative Medical Sciences
Jay W. Shin: RIKEN Center for Integrative Medical Sciences
Michael Detmar: Swiss Federal Institute of Technology (ETH) Zurich

Nature Communications, 2021, vol. 12, issue 1, 1-22

Abstract: Abstract Recent studies have revealed the importance of long noncoding RNAs (lncRNAs) as tissue-specific regulators of gene expression. There is ample evidence that distinct types of vasculature undergo tight transcriptional control to preserve their structure, identity, and functions. We determine a comprehensive map of lineage-specific lncRNAs in human dermal lymphatic and blood vascular endothelial cells (LECs and BECs), combining RNA-Seq and CAGE-Seq. Subsequent antisense oligonucleotide-knockdown transcriptomic profiling of two LEC- and two BEC-specific lncRNAs identifies LETR1 as a critical gatekeeper of the global LEC transcriptome. Deep RNA-DNA, RNA-protein interaction studies, and phenotype rescue analyses reveal that LETR1 is a nuclear trans-acting lncRNA modulating, via key epigenetic factors, the expression of essential target genes, including KLF4 and SEMA3C, governing the growth and migratory ability of LECs. Together, our study provides several lines of evidence supporting the intriguing concept that every cell type expresses precise lncRNA signatures to control lineage-specific regulatory programs.

Date: 2021
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DOI: 10.1038/s41467-021-21217-0

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