Natural display of nuclear-encoded RNA on the cell surface and its impact on cell interaction

Genome Biol. 2020 Sep 10;21(1):225. doi: 10.1186/s13059-020-02145-6.

Abstract

Background: Compared to proteins, glycans, and lipids, much less is known about RNAs on the cell surface. We develop a series of technologies to test for any nuclear-encoded RNAs that are stably attached to the cell surface and exposed to the extracellular space, hereafter called membrane-associated extracellular RNAs (maxRNAs).

Results: We develop a technique called Surface-seq to selectively sequence maxRNAs and validate two Surface-seq identified maxRNAs by RNA fluorescence in situ hybridization. To test for cell-type specificity of maxRNA, we use antisense oligos to hybridize to single-stranded transcripts exposed on the surface of human peripheral blood mononuclear cells (PBMCs). Combining this strategy with imaging flow cytometry, single-cell RNA sequencing, and maxRNA sequencing, we identify monocytes as the major type of maxRNA+ PBMCs and prioritize 11 candidate maxRNAs for functional tests. Extracellular application of antisense oligos of FNDC3B and CTSS transcripts inhibits monocyte adhesion to vascular endothelial cells.

Conclusions: Collectively, these data highlight maxRNAs as functional components of the cell surface, suggesting an expanded role for RNA in cell-cell and cell-environment interactions.

Keywords: Cell membrane; Cell surface; Cell-environment interaction; Endothelial cells; Extracellular RNA; Monocyte; Single cell.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Validation Study

MeSH terms

  • Animals
  • Cell Communication*
  • Cell Membrane / metabolism*
  • Humans
  • Leukocytes, Mononuclear / metabolism*
  • Mice
  • RNA / chemistry
  • RNA / isolation & purification
  • RNA / metabolism*
  • Sequence Analysis, RNA
  • Transcriptome

Substances

  • RNA