A point mutation in the pre-ZRS disrupts sonic hedgehog expression in the limb bud and results in triphalangeal thumb-polysyndactyly syndrome

Genet Med. 2018 Nov;20(11):1405-1413. doi: 10.1038/gim.2018.18. Epub 2018 Mar 15.

Abstract

Purpose: The zone of polarizing activity regulatory sequence (ZRS) is an enhancer that regulates sonic hedgehog during embryonic limb development. Recently, mutations in a noncoding evolutionary conserved sequence 500 bp upstream of the ZRS, termed the pre-ZRS (pZRS), have been associated with polydactyly in dogs and humans. Here, we report the first case of triphalangeal thumb-polysyndactyly syndrome (TPT-PS) to be associated with mutations in this region and show via mouse enhancer assays how this mutation leads to ectopic expression throughout the developing limb bud.

Methods: We used linkage analysis, whole-exome sequencing, Sanger sequencing, fluorescence in situ hybridization, multiplex ligation-dependent probe amplification, single-nucleotide polymorphism array, and a mouse transgenic enhancer assay.

Results: Ten members of a TPT-PS family were included in this study. The mutation was linked to chromosome 7q36 (LOD score 3.0). No aberrations in the ZRS could be identified. A point mutation in the pZRS (chr7:156585476G>C; GRCh37/hg19) was detected in all affected family members. Functional characterization using a mouse transgenic enhancer essay showed extended ectopic expression dispersed throughout the entire limb bud (E11.5).

Conclusion: Our work describes the first mutation in the pZRS to be associated with TPT-PS and provides functional evidence that this mutation leads to ectopic expression of this enhancer within the developing limb.

Keywords: congenital limb deformities; genetic enhancer elements; hedgehog protein; polydactyly; syndactyly.

MeSH terms

  • Animals
  • Chromosomes, Human, Pair 7 / genetics
  • Congenital Abnormalities / genetics*
  • Enhancer Elements, Genetic / genetics
  • Exome Sequencing
  • Female
  • Gene Expression Regulation / genetics
  • Genetic Linkage
  • Genetic Predisposition to Disease*
  • Hedgehog Proteins / genetics*
  • Humans
  • In Situ Hybridization, Fluorescence
  • Limb Buds / physiopathology
  • Male
  • Mandibulofacial Dysostosis / genetics*
  • Membrane Proteins / genetics*
  • Mice
  • Pedigree
  • Point Mutation / genetics
  • Polymorphism, Single Nucleotide

Substances

  • Hedgehog Proteins
  • LMBR1 protein, human
  • Membrane Proteins
  • SHH protein, human

Supplementary concepts

  • Patterson Stevenson syndrome