Spectroscopic and protein chemical analyses demonstrate the presence of C-mannosylated tryptophan in intact human RNase 2 and its isoforms

Biochemistry. 1996 Sep 17;35(37):12005-14. doi: 10.1021/bi9610515.

Abstract

Recently, the C-mannosylation of a specific tryptophan residue in RNase 2 from human urine has been reported [Hofsteenge, J., et al. (1994) Biochemistry 33, 13524-13530; de Beer, T., et al. (1995) Biochemistry 34, 11785-11789]. In those studies, identification of this unusual modification was accomplished by mass spectrometric and NMR spectroscopic analysis of peptide fragments. The evidence for the occurrence of C2-alpha-mannosyltryptophan [(C2-Man-)Trp] in the intact protein relied exclusively on the detection of the same phenylthiohydantoin derivatives during Edman degradation. In this paper, we have (1) excluded the possibility that (C2-Man-)Trp arose artificially under the acidic conditions previously employed for protein and peptide isolation and analysis, by maintaining the pH > 5 throughout these procedures, (2) demonstrated the occurrence of (C2-Man-)Trp in the intact protein, by NMR spectroscopy, (3) showed that (C2-Man-)Trp is not unique for RNase 2 from urine but that it is also present in the enzyme isolated from erythrocytes, and (4) found also that high-molecular mass isoforms of urinary RNase 2 are C-mannosylated. These observations firmly establish C-mannosylation as a novel way of post-translationally attaching carbohydrate to protein, in addition to the well-known N- and O-glycosylations. Furthermore, the NMR data, in combination with molecular dynamics calculations, indicate that in the native protein the mannopyranosyl residue is in a different conformation than in the glycopeptide or denatured protein, due to protein-carbohydrate interactions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Blotting, Western
  • Endoribonucleases / chemistry*
  • Endoribonucleases / isolation & purification
  • Endoribonucleases / urine
  • Female
  • Glycosylation
  • Humans
  • Isoenzymes / chemistry*
  • Isoenzymes / isolation & purification
  • Isoenzymes / urine
  • Magnetic Resonance Spectroscopy
  • Mannose / analysis*
  • Mass Spectrometry
  • Menopause
  • Models, Molecular
  • Molecular Sequence Data
  • Molecular Weight
  • Peptide Fragments / chemistry
  • Peptide Fragments / isolation & purification
  • Pregnancy
  • Protein Conformation
  • Tryptophan* / analogs & derivatives*
  • Tryptophan* / analysis

Substances

  • C(2)-mannosyltryptophan
  • Isoenzymes
  • Peptide Fragments
  • Tryptophan
  • Endoribonucleases
  • ribonuclease U
  • Mannose