Sjogren syndrome antigen B (SSB)/La promotes global microRNA expression by binding microRNA precursors through stem-loop recognition

J Biol Chem. 2013 Jan 4;288(1):723-36. doi: 10.1074/jbc.M112.401323. Epub 2012 Nov 5.

Abstract

MicroRNAs (miRNA) control numerous physiological and pathological processes. Typically, the primary miRNA (pri-miRNA) transcripts are processed by nuclear Drosha complex into ~70-nucleotide stem-loop precursor miRNAs (pre-miRNA), which are further cleaved by cytoplasmic Dicer complex into ~21-nucleotide mature miRNAs. However, it is unclear how nascent pre-miRNAs are protected from ribonucleases, such as MCPIP1, that degrade pre-miRNAs to abort miRNA production. Here, we identify Sjögren syndrome antigen B (SSB)/La as a pre-miRNA-binding protein that regulates miRNA processing in vitro. All three RNA-binding motifs (LAM, RRM1, and RRM2) of La/SSB are required for efficient pre-miRNA binding. Intriguingly, La/SSB recognizes the characteristic stem-loop structure of pre-miRNAs, of which the majority lack a 3' UUU terminus. Moreover, La/SSB associates with endogenous pri-/pre-miRNAs and promotes miRNA biogenesis by stabilizing pre-miRNAs from nuclease (e.g. MCPIP1)-mediated decay in mammalian cells. Accordingly, we observed positive correlations between the expression status of La/SSB and Dicer in human cancer transcriptome and prognosis. These studies identify an important function of La/SSB as a global regulator of miRNA expression, and implicate stem-loop recognition as a major mechanism that mediates association between La/SSB and diverse RNA molecules.

Publication types

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

MeSH terms

  • Autoantigens / metabolism*
  • Autoimmunity
  • Cytoplasm / metabolism
  • DEAD-box RNA Helicases / metabolism
  • Gene Expression Regulation*
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Immunoprecipitation
  • MicroRNAs / metabolism*
  • Models, Biological
  • Protein Structure, Secondary
  • RNA / metabolism
  • RNA-Binding Proteins / metabolism
  • Ribonuclease III / metabolism
  • Ribonucleases / metabolism
  • Ribonucleoproteins / metabolism*
  • SS-B Antigen
  • Sjogren's Syndrome / metabolism*

Substances

  • Autoantigens
  • MicroRNAs
  • RNA-Binding Proteins
  • Ribonucleoproteins
  • RNA
  • Ribonucleases
  • DICER1 protein, human
  • Ribonuclease III
  • DEAD-box RNA Helicases