Unraveling the novel structure and biosynthetic pathway of O-linked glycans in the Golgi apparatus of the human pathogenic yeast Cryptococcus neoformans

J Biol Chem. 2015 Jan 16;290(3):1861-73. doi: 10.1074/jbc.M114.607705. Epub 2014 Dec 4.

Abstract

Cryptococcus neoformans is an encapsulated basidiomycete causing cryptococcosis in immunocompromised humans. The cell surface mannoproteins of C. neoformans were reported to stimulate the host T-cell response and to be involved in fungal pathogenicity; however, their O-glycan structure is uncharacterized. In this study, we performed a detailed structural analysis of the O-glycans attached to cryptococcal mannoproteins using HPLC combined with exoglycosidase treatment and showed that the major C. neoformans O-glycans were short manno-oligosaccharides that were connected mostly by α1,2-linkages but connected by an α1,6-linkage at the third mannose residue. Comparison of the O-glycan profiles from wild-type and uxs1Δ mutant strains strongly supports the presence of minor O-glycans carrying a xylose residue. Further analyses of C. neoformans mutant strains identified three mannosyltransferase genes involved in O-glycan extensions in the Golgi. C. neoformans KTR3, the only homolog of the Saccharomyces cerevisiae KRE2/MNT1 family genes, was shown to encode an α1,2-mannosyltransferase responsible for the addition of the second mannose residue via an α1,2-linkage to the major O-glycans. C. neoformans HOC1 and HOC3, homologs of the Saccharomyces cerevisiae OCH1 family genes, were shown to encode α1,6-mannosyltransferases that can transfer the third mannose residue, via an α1,6-linkage, to minor O-glycans containing xylose and to major O-glycans without xylose, respectively. Moreover, the C. neoformans ktr3Δ mutant strain, which displayed increased sensitivity to SDS, high salt, and high temperature, showed attenuated virulence in a mouse model of cryptococcosis, suggesting that the extended structure of O-glycans is required for cell integrity and full pathogenicity of C. neoformans.

Keywords: Cell Wall; Cryptococcus neoforman; Fungi; Glycan Analysis; Glycomics; Glycoprotein; Glycosyltransferase; Mannosyltransferases; O-Mannosylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Wall / metabolism
  • Chromatography, High Pressure Liquid
  • Cryptococcosis / metabolism
  • Cryptococcosis / microbiology*
  • Cryptococcus neoformans / metabolism*
  • Female
  • Fungal Proteins / metabolism
  • Genetic Complementation Test
  • Glycosylation
  • Glycosyltransferases / metabolism
  • Mannose / chemistry
  • Mannosyltransferases / genetics
  • Mannosyltransferases / metabolism*
  • Melanins / chemistry
  • Mice
  • Mutation
  • Phenotype
  • Phylogeny
  • Plasmids / metabolism
  • Polysaccharides / biosynthesis*
  • Protein Conformation
  • Xylose / chemistry

Substances

  • Fungal Proteins
  • Melanins
  • Polysaccharides
  • Xylose
  • Glycosyltransferases
  • Mannosyltransferases
  • Mannose