Spatial regulation of microRNA gene expression in the Drosophila embryo

Proc Natl Acad Sci U S A. 2005 Nov 1;102(44):15907-11. doi: 10.1073/pnas.0507817102. Epub 2005 Oct 25.

Abstract

MicroRNAs (miRNAs) regulate posttranscriptional gene activity by binding to specific sequences in the 3' UTRs of target mRNAs. A number of metazoan miRNAs have been shown to exhibit tissue-specific patterns of expression. Here, we investigate the possibility that localized expression is mediated by tissue-specific enhancers, comparable to those seen for protein-coding genes. Two miRNA loci in Drosophila melanogaster are investigated, the mir-309-6 polycistron (8-miR) and the mir-1 gene. The 8-miR locus contains a cluster of eight distinct miRNAs that are transcribed in a common precursor RNA. The 8-miR primary transcript displays a dynamic pattern of expression in early embryos, including repression at the anterior and posterior poles. An 800-bp 5' enhancer was identified that recapitulates this complex pattern when attached to a RNA polymerase II core promoter fused to a lacZ-reporter gene. The miR-1 locus is specifically expressed in the mesoderm of gastrulating embryos. Bioinformatics methods were used to identify a mesoderm-specific enhancer located approximately 5 kb 5' of the miR-1 transcription unit. Evidence is presented that the 8-miR enhancer is regulated by the localized Huckebein repressor, whereas miR-1 is activated by Dorsal and Twist. These results provide evidence that restricted activities of the 8-miR and miR-1 miRNAs are mediated by classical tissue-specific enhancers.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • DNA-Binding Proteins / physiology
  • Drosophila Proteins / physiology
  • Drosophila melanogaster / embryology
  • Drosophila melanogaster / genetics*
  • Embryo, Nonmammalian
  • Enhancer Elements, Genetic
  • Gene Expression Regulation, Developmental / genetics*
  • Genes
  • Mesoderm / metabolism
  • MicroRNAs / genetics*
  • Nuclear Proteins / physiology
  • Phosphoproteins / physiology
  • RNA Precursors
  • Tissue Distribution
  • Transcription Factors* / physiology
  • Transcription, Genetic
  • Twist-Related Protein 1 / physiology

Substances

  • DNA-Binding Proteins
  • Drosophila Proteins
  • Hkb protein, Drosophila
  • MicroRNAs
  • Nuclear Proteins
  • Phosphoproteins
  • RNA Precursors
  • Transcription Factors
  • Twi protein, Drosophila
  • Twist-Related Protein 1
  • dl protein, Drosophila