A human homeotic transformation resulting from mutations in PLCB4 and GNAI3 causes auriculocondylar syndrome

Am J Hum Genet. 2012 May 4;90(5):907-14. doi: 10.1016/j.ajhg.2012.04.002.

Abstract

Auriculocondylar syndrome (ACS) is a rare, autosomal-dominant craniofacial malformation syndrome characterized by variable micrognathia, temporomandibular joint ankylosis, cleft palate, and a characteristic "question-mark" ear malformation. Careful phenotypic characterization of severely affected probands in our cohort suggested the presence of a mandibular patterning defect resulting in a maxillary phenotype (i.e., homeotic transformation). We used exome sequencing of five probands and identified two novel (exclusive to the patient and/or family studied) missense mutations in PLCB4 and a shared mutation in GNAI3 in two unrelated probands. In confirmatory studies, three additional novel PLCB4 mutations were found in multigenerational ACS pedigrees. All mutations were confirmed by Sanger sequencing, were not present in more than 10,000 control chromosomes, and resulted in amino-acid substitutions located in highly conserved protein domains. Additionally, protein-structure modeling demonstrated that all ACS substitutions disrupt the catalytic sites of PLCB4 and GNAI3. We suggest that PLCB4 and GNAI3 are core signaling molecules of the endothelin-1-distal-less homeobox 5 and 6 (EDN1-DLX5/DLX6) pathway. Functional studies demonstrated a significant reduction in downstream DLX5 and DLX6 expression in ACS cases in assays using cultured osteoblasts from probands and controls. These results support the role of the previously implicated EDN1-DLX5/6 pathway in regulating mandibular specification in other species, which, when disrupted, results in a maxillary phenotype. This work defines the molecular basis of ACS as a homeotic transformation (mandible to maxilla) in humans.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Cohort Studies
  • Ear / abnormalities
  • Ear / physiopathology
  • Ear Diseases / genetics*
  • Ear Diseases / physiopathology
  • Endothelin-1 / genetics
  • Endothelin-1 / metabolism
  • Exome
  • Female
  • GTP-Binding Protein alpha Subunits, Gi-Go / genetics*
  • GTP-Binding Protein alpha Subunits, Gi-Go / metabolism
  • Gene Expression Regulation
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Humans
  • Male
  • Molecular Sequence Data
  • Mutation*
  • Pedigree
  • Phenotype
  • Phospholipase C beta / genetics*
  • Phospholipase C beta / metabolism
  • Protein Conformation
  • Sequence Analysis, RNA

Substances

  • Endothelin-1
  • Homeodomain Proteins
  • PLCB4 protein, human
  • Phospholipase C beta
  • GNAI3 protein, human
  • GTP-Binding Protein alpha Subunits, Gi-Go

Supplementary concepts

  • Auriculo-condylar syndrome