Defective initiation of glycosaminoglycan synthesis due to B3GALT6 mutations causes a pleiotropic Ehlers-Danlos-syndrome-like connective tissue disorder

Am J Hum Genet. 2013 Jun 6;92(6):935-45. doi: 10.1016/j.ajhg.2013.04.016. Epub 2013 May 9.

Abstract

Proteoglycans are important components of cell plasma membranes and extracellular matrices of connective tissues. They consist of glycosaminoglycan chains attached to a core protein via a tetrasaccharide linkage, whereby the addition of the third residue is catalyzed by galactosyltransferase II (β3GalT6), encoded by B3GALT6. Homozygosity mapping and candidate gene sequence analysis in three independent families, presenting a severe autosomal-recessive connective tissue disorder characterized by skin fragility, delayed wound healing, joint hyperlaxity and contractures, muscle hypotonia, intellectual disability, and a spondyloepimetaphyseal dysplasia with bone fragility and severe kyphoscoliosis, identified biallelic B3GALT6 mutations, including homozygous missense mutations in family 1 (c.619G>C [p.Asp207His]) and family 3 (c.649G>A [p.Gly217Ser]) and compound heterozygous mutations in family 2 (c.323_344del [p.Ala108Glyfs(∗)163], c.619G>C [p.Asp207His]). The phenotype overlaps with several recessive Ehlers-Danlos variants and spondyloepimetaphyseal dysplasia with joint hyperlaxity. Affected individuals' fibroblasts exhibited a large decrease in ability to prime glycosaminoglycan synthesis together with impaired glycanation of the small chondroitin/dermatan sulfate proteoglycan decorin, confirming β3GalT6 loss of function. Dermal electron microcopy disclosed abnormalities in collagen fibril organization, in line with the important regulatory role of decorin in this process. A strong reduction in heparan sulfate level was also observed, indicating that β3GalT6 deficiency alters synthesis of both main types of glycosaminoglycans. In vitro wound healing assay revealed a significant delay in fibroblasts from two index individuals, pointing to a role for glycosaminoglycan defect in impaired wound repair in vivo. Our study emphasizes a crucial role for β3GalT6 in multiple major developmental and pathophysiological processes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abnormalities, Multiple / diagnostic imaging
  • Abnormalities, Multiple / genetics*
  • Abnormalities, Multiple / metabolism
  • Adult
  • Amino Acid Sequence
  • Base Sequence
  • Child
  • Consanguinity
  • Ehlers-Danlos Syndrome / diagnostic imaging
  • Ehlers-Danlos Syndrome / genetics*
  • Ehlers-Danlos Syndrome / metabolism
  • Female
  • Galactosyltransferases / genetics*
  • Genetic Association Studies
  • Genetic Pleiotropy
  • Glycosaminoglycans / biosynthesis*
  • Humans
  • Infant
  • Male
  • Molecular Sequence Data
  • Mutation, Missense
  • Pedigree
  • Radiography
  • Sequence Analysis, DNA
  • Wound Healing / genetics

Substances

  • Glycosaminoglycans
  • B3GALT6 protein, human
  • Galactosyltransferases