The Caenorhabditis elegans genes sqv-2 and sqv-6, which are required for vulval morphogenesis, encode glycosaminoglycan galactosyltransferase II and xylosyltransferase

J Biol Chem. 2003 Apr 4;278(14):11735-8. doi: 10.1074/jbc.C200518200. Epub 2003 Feb 12.

Abstract

In mutants defective in any of eight Caenorhabditis elegans sqv (squashed vulva) genes, the vulval extracellular space fails to expand during vulval morphogenesis. Strong sqv mutations result in maternal-effect lethality, caused in part by the failure of the progeny of homozygous mutants to initiate cytokinesis and associated with the failure to form an extracellular space between the egg and the eggshell. Recent studies have implicated glycosaminoglycans in these processes. Here we report the cloning and characterization of sqv-2 and sqv-6. sqv-6 encodes a protein similar to human xylosyltransferases. Transfection of sqv-6 restored xylosyltransferase activity to and rescued the glycosaminoglycan biosynthesis defect of a xylosyltransferase mutant hamster cell line. sqv-2 encodes a protein similar to human galactosyltransferase II. A recombinant SQV-2 fusion protein had galactosyltransferase II activity with substrate specificity similar to that of human galactosyltransferase II. We conclude that C. elegans SQV-6 and SQV-2 likely act in concert with other SQV proteins to catalyze the stepwise formation of the proteoglycan core protein linkage tetrasaccharide GlcAbeta1,3Galbeta1, 3Galbeta1,4Xylbeta-O-(Ser), which is common to the two major types of glycosaminoglycans in vertebrates, chondroitin and heparan sulfate. Our results strongly support a model in which C. elegans vulval morphogenesis and zygotic cytokinesis depend on the expression of glycosaminoglycans.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • CHO Cells
  • Caenorhabditis elegans / embryology*
  • Caenorhabditis elegans Proteins / genetics*
  • Caenorhabditis elegans Proteins / metabolism
  • Chondroitin Sulfates / biosynthesis
  • Cloning, Molecular
  • Cricetinae
  • Female
  • Galactosyltransferases / genetics*
  • Galactosyltransferases / metabolism
  • Gene Expression Regulation, Developmental
  • Gene Expression Regulation, Enzymologic
  • Glycosaminoglycans / metabolism
  • Heparitin Sulfate / biosynthesis
  • Molecular Sequence Data
  • Pentosyltransferases / genetics*
  • Pentosyltransferases / metabolism
  • UDP Xylose-Protein Xylosyltransferase
  • Vulva / embryology*

Substances

  • Caenorhabditis elegans Proteins
  • Glycosaminoglycans
  • Chondroitin Sulfates
  • Heparitin Sulfate
  • Galactosyltransferases
  • Sqv-2 protein, C elegans
  • galactosylxylosylprotein 3-beta-galactosyltransferase
  • Pentosyltransferases
  • Sqv-6 protein, C elegans

Associated data

  • GENBANK/AY241927
  • GENBANK/AY241928