Absent expression of the osteoblast-specific maternally imprinted genes, DLX5 and DLX6, causes split hand/split foot malformation type I

J Med Genet. 2014 Dec;51(12):817-23. doi: 10.1136/jmedgenet-2014-102576. Epub 2014 Oct 20.

Abstract

Background: Split hand/split foot malformation (SHFM) type 1 is characterised by missing central digital rays with clefts of the hands and/or feet, which was linked to chromosome 7q21.3. While double knockout of Dlx5 and Dlx6 resulted in limb defects in mice, the majority of patients with SHFM1 had only heterozygous chromosomal abnormalities.

Objective: To investigate the clinical and molecular features of a large family with SHFM1.

Methods: Blood samples of family members were investigated by linkage analysis, array comparative genomic hybridisation, exome sequencing and PCR-Sanger sequencing. Cultures from bone specimens obtained from the proband and an unrelated unaffected individual were established and subjected to quantitative real-time PCR, reverse-transcribed PCR, Western blot and imprinting analysis.

Results: We report a large pedigree of SHFM1 with 10 members having a heterozygous 103 kb deletion, the smallest one ever reported to be associated with SHFM1. Of these 10, two had no limb anomalies, making a penetrance of 80%. The deletion encompassed exons 15 and 17 of DYNC1I1, which are known enhancers of two downstream genes, DLX5 and DLX6. Surprisingly, DLX5 and DLX6 RNA and proteins in our proband's cultured osteoblasts, instead of 50% decrease, were absent. Allelic expression studies in cultured osteoblasts of the unaffected individual showed that DSS1, DLX6 and DLX5 expressed only paternal alleles. These lines of evidence indicate that DSS1, DLX6 and DLX5 were maternally imprinted in osteoblasts.

Conclusions: SHFM1 in our family is caused by a heterozygous paternal deletion of enhancers of the osteoblast-specific maternally imprinted DLX6 and DLX5 genes, leading to the absence of their proteins.

Keywords: Developmental; Imprinting; Molecular genetics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chromosome Breakpoints
  • Comparative Genomic Hybridization
  • DNA Copy Number Variations
  • Female
  • Foot Deformities, Congenital / diagnostic imaging
  • Foot Deformities, Congenital / pathology
  • Gene Expression
  • Genetic Linkage
  • Genomic Imprinting*
  • Hand Deformities, Congenital / diagnostic imaging
  • Hand Deformities, Congenital / pathology
  • Heterozygote
  • Homeodomain Proteins / genetics*
  • Humans
  • Limb Deformities, Congenital / diagnosis
  • Limb Deformities, Congenital / metabolism*
  • Male
  • Organ Specificity / genetics
  • Osteoblasts / metabolism
  • Pedigree
  • Phenotype
  • Point Mutation
  • Radiography
  • Sequence Deletion
  • Transcription Factors / genetics*

Substances

  • DLX5 protein, human
  • DLX6 protein, human
  • Homeodomain Proteins
  • Transcription Factors

Supplementary concepts

  • Ectrodactyly