SCAR-6 elncRNA locus epigenetically regulates PROZ and modulates coagulation and vascular function

EMBO Rep. 2024 Nov;25(11):4950-4978. doi: 10.1038/s44319-024-00272-w. Epub 2024 Oct 2.

Abstract

In this study, we characterize a novel lncRNA-producing gene locus that we name Syntenic Cardiovascular Conserved Region-Associated lncRNA-6 (scar-6) and functionally validate its role in coagulation and cardiovascular function. A 12-bp deletion of the scar-6 locus in zebrafish (scar-6gib007Δ12/Δ12) results in cranial hemorrhage and vascular permeability. Overexpression, knockdown and rescue with the scar-6 lncRNA modulates hemostasis in zebrafish. Molecular investigation reveals that the scar-6 lncRNA acts as an enhancer lncRNA (elncRNA), and controls the expression of prozb, an inhibitor of factor Xa, through an enhancer element in the scar-6 locus. The scar-6 locus suppresses loop formation between prozb and scar-6 sequences, which might be facilitated by the methylation of CpG islands via the prdm14-PRC2 complex whose binding to the locus might be stabilized by the scar-6 elncRNA transcript. Binding of prdm14 to the scar-6 locus is impaired in scar-6gib007Δ12/Δ12 zebrafish. Finally, activation of the PAR2 receptor in scar-6gib007Δ12/Δ12 zebrafish triggers NF-κB-mediated endothelial cell activation, leading to vascular dysfunction and hemorrhage. We present evidence that the scar-6 locus plays a role in regulating the expression of the coagulation cascade gene prozb and maintains vascular homeostasis.

Keywords: Cardiovascular; Endothelial Cell; Hemorrhage; Synteny lncRNA; Zebrafish.

MeSH terms

  • Animals
  • Blood Coagulation* / genetics
  • Capillary Permeability / genetics
  • Endothelial Cells / metabolism
  • Enhancer Elements, Genetic / genetics
  • Epigenesis, Genetic*
  • Gene Expression Regulation
  • Genetic Loci
  • Humans
  • NF-kappa B / metabolism
  • RNA, Long Noncoding* / genetics
  • RNA, Long Noncoding* / metabolism
  • Zebrafish Proteins* / genetics
  • Zebrafish Proteins* / metabolism
  • Zebrafish* / genetics

Substances

  • RNA, Long Noncoding
  • Zebrafish Proteins
  • NF-kappa B