Oncogenic All1 fusion proteins target Drosha-mediated microRNA processing

Proc Natl Acad Sci U S A. 2007 Jun 26;104(26):10980-5. doi: 10.1073/pnas.0704559104. Epub 2007 Jun 20.

Abstract

MicroRNAs (miRNAs) are noncoding small RNA of approximately 22 bases, which suppress expression of target genes through translational block or degradation of a target's transcript. Recent studies uncovered specific miRNA expression profiles in human malignancies. Nevertheless, the mechanisms underlying cancer-specific miRNA expression are largely unknown. miRNA biogenesis consists of a series of steps beginning with generation of a primary transcript, termed pri-miRNA, and continuing into excision of a stem-loop hairpin structure within pri-miRNA by the nuclear RNaseIII enzyme Drosha, transportation to the cytoplasm, and further processing by a second RNaseIII enzyme Dicer, into a 22-base mature duplex RNA. In principle, alteration in any step during this maturation process could affect miRNA production. The ALL-1 (also termed MLL) gene was originally isolated by virtue of its involvement in recurrent chromosome translocations associated with acute leukemias, particularly in infant and therapy-related leukemias. These translocations result in the fusion of ALL-1 with partner genes and the consequent production of chimeric leukemogenic proteins. Here, we identify specific miRNAs up-regulated in leukemias triggered by All1 fusions. Further, we demonstrate coimmunoprecipitation of the All1/Af4 and All1/Af9 fusions with Drosha, disrupted by treatment with DNase I. Finally, we present evidence from ChIP experiments for All1 fusion protein-mediated recruitment of Drosha to target genes encoding miRNAs. Such recruitment may underlie the enhanced expression of the relevant miRNAs.

Publication types

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

MeSH terms

  • Gene Expression Regulation, Neoplastic
  • Histone-Lysine N-Methyltransferase
  • Humans
  • Leukemia / etiology
  • Leukemia / genetics*
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Myeloid-Lymphoid Leukemia Protein / genetics*
  • Oncogene Proteins, Fusion / physiology*
  • RNA Processing, Post-Transcriptional*
  • Ribonuclease III / metabolism
  • Ribonuclease III / physiology*
  • Up-Regulation

Substances

  • ALL1-AF4 fusion protein, human
  • KMT2A protein, human
  • MLL-AF9 fusion protein, human
  • MicroRNAs
  • Oncogene Proteins, Fusion
  • Myeloid-Lymphoid Leukemia Protein
  • Histone-Lysine N-Methyltransferase
  • DROSHA protein, human
  • Ribonuclease III