Synthesis and delivery of short, noncoding RNA by B lymphocytes

Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):20182-7. doi: 10.1073/pnas.1311145110. Epub 2013 Nov 25.

Abstract

Evolutionarily conserved short (20-30 nucleotides) noncoding RNAs (microRNAs) are powerful regulators of gene expression in a variety of physiological and pathological processes. As such, means to efficiently modulate microRNA function constitute an important therapeutic opportunity. Here we demonstrate that primary B lymphocytes can be genetically programmed with nonviral plasmid DNA for the biogenesis and delivery of antisense sequences (anti-microRNA) against microRNA-150 (miR-150). Within 18 h of transfection with an anti-miR-150 construct, primary B lymphocytes secrete ∼3,000 copies of anti-miR-150 molecules per cell. Anti-miR-150 molecules released by B lymphocytes were internalized by CD8 T lymphocytes during cross-priming in vitro and in vivo, resulting in marked down-regulation of endogenous miR-150. However, such internalization was not observed in the absence of cross-priming. These results suggest that shuttling anti-miR-150 molecules from B lymphocytes to T cells requires the activation of receiver T cells via the antigen receptor. Finally, anti-miR-150 synthesized in B cells were secreted both as free and extracellular vesicle-associated fractions, but only extracellular vesicle-associated anti-miR-150 were apparently taken up by CD8 T cells. Collectively, these data indicate that primary B lymphocytes represent an efficient platform for the synthesis and delivery of short, noncoding RNA, paving the way for an approach to immunogenomic therapies.

Keywords: immunotherapy; microvesicles.

Publication types

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

MeSH terms

  • Animals
  • Antibodies / immunology
  • B-Lymphocytes / metabolism*
  • Cross-Priming
  • Flow Cytometry
  • Gene Expression Regulation / genetics*
  • Gene Targeting / methods*
  • Humans
  • Immunotherapy / methods*
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Microscopy, Fluorescence
  • Oligonucleotides / genetics
  • Plasmids / genetics
  • RNA, Small Untranslated / biosynthesis*
  • RNA, Small Untranslated / metabolism*
  • Real-Time Polymerase Chain Reaction
  • Transfection

Substances

  • Antibodies
  • MIRN150 microRNA, human
  • MicroRNAs
  • Oligonucleotides
  • RNA, Small Untranslated