Chromosome 1p21.3 microdeletions comprising DPYD and MIR137 are associated with intellectual disability

J Med Genet. 2011 Dec;48(12):810-8. doi: 10.1136/jmedgenet-2011-100294. Epub 2011 Oct 15.

Abstract

Background: MicroRNAs (miRNAs) are non-coding gene transcripts involved in post-transcriptional regulation of genes. Recent studies identified miRNAs as important regulators of learning and memory in model organisms. So far, no mutations in specific miRNA genes have been associated with impaired cognitive functions.

Methods and results: In three sibs and two unrelated patients with intellectual disability (ID), overlapping 1p21.3 deletions were detected by genome-wide array analysis. The shortest region of overlap included dihydropyrimidine dehydrogenase (DPYD) and microRNA 137 (MIR137). DPYD is involved in autosomal recessive dihydropyrimidine dehydrogenase deficiency. Hemizygous DPYD deletions were previously suggested to contribute to a phenotype with autism spectrum disorder and speech delay. Interestingly, the mature microRNA transcript microRNA-137 (miR-137) was recently shown to be involved in modulating neurogenesis in adult murine neuronal stem cells. Therefore, this study investigated the possible involvement of MIR137 in the 1p21.3-deletion phenotype. The patients displayed a significantly decreased expression of both precursor and mature miR-137 levels, as well as significantly increased expression of the validated downstream targets microphthalmia-associated transcription factor (MITF) and Enhancer of Zeste, Drosophila, Homologue 2 (EZH2), and the newly identified target Kruppel-like factor 4 (KLF4). The study also demonstrated significant enrichment of miR-137 at the synapses of cortical and hippocampal neurons, suggesting a role of miR-137 in regulating local synaptic protein synthesis machinery.

Conclusions: This study showed that dosage effects of MIR137 are associated with 1p21.3 microdeletions and may therefore contribute to the ID phenotype in patients with deletions harbouring this miRNA. A local effect at the synapse might be responsible.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • Chromosome Deletion*
  • Chromosomes, Human, Pair 1 / genetics
  • Chromosomes, Human, Pair 1 / metabolism
  • DNA Copy Number Variations
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Dihydrouracil Dehydrogenase (NADP) / genetics
  • Dihydrouracil Dehydrogenase (NADP) / metabolism
  • Enhancer of Zeste Homolog 2 Protein
  • Female
  • Gene Dosage
  • Gene Expression Regulation
  • Hippocampus / cytology
  • Hippocampus / metabolism
  • Hippocampus / pathology
  • Humans
  • Intellectual Disability / genetics*
  • Intellectual Disability / metabolism
  • Intellectual Disability / pathology
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism
  • Male
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Microphthalmia-Associated Transcription Factor / genetics
  • Microphthalmia-Associated Transcription Factor / metabolism
  • Neurons / cytology
  • Neurons / metabolism
  • Neurons / pathology
  • Oligonucleotide Array Sequence Analysis
  • Phenotype
  • Polycomb Repressive Complex 2
  • Polymorphism, Single Nucleotide
  • Primary Cell Culture
  • Rats
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transfection

Substances

  • DNA-Binding Proteins
  • KLF4 protein, human
  • Klf4 protein, rat
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors
  • MIRN137 microRNA, human
  • MITF protein, human
  • MicroRNAs
  • Microphthalmia-Associated Transcription Factor
  • Transcription Factors
  • Dihydrouracil Dehydrogenase (NADP)
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • Polycomb Repressive Complex 2