Engineering Orthogonal Polypeptide GalNAc-Transferase and UDP-Sugar Pairs

J Am Chem Soc. 2019 Aug 28;141(34):13442-13453. doi: 10.1021/jacs.9b04695. Epub 2019 Aug 16.

Abstract

O-Linked α-N-acetylgalactosamine (O-GalNAc) glycans constitute a major part of the human glycome. They are difficult to study because of the complex interplay of 20 distinct glycosyltransferase isoenzymes that initiate this form of glycosylation, the polypeptide N-acetylgalactosaminyltransferases (GalNAc-Ts). Despite proven disease relevance, correlating the activity of individual GalNAc-Ts with biological function remains challenging due to a lack of tools to probe their substrate specificity in a complex biological environment. Here, we develop a "bump-hole" chemical reporter system for studying GalNAc-T activity in vitro. Individual GalNAc-Ts were rationally engineered to contain an enlarged active site (hole) and probed with a newly synthesized collection of 20 (bumped) uridine diphosphate N-acetylgalactosamine (UDP-GalNAc) analogs to identify enzyme-substrate pairs that retain peptide specificities but are otherwise completely orthogonal to native enzyme-substrate pairs. The approach was applicable to multiple GalNAc-T isoenzymes, including GalNAc-T1 and -T2 that prefer nonglycosylated peptide substrates and GalNAcT-10 that prefers a preglycosylated peptide substrate. A detailed investigation of enzyme kinetics and specificities revealed the robustness of the approach to faithfully report on GalNAc-T activity and paves the way for studying substrate specificities in living systems.

Publication types

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

MeSH terms

  • Acetylgalactosamine / chemistry
  • Acetylgalactosamine / metabolism*
  • Amino Acid Sequence
  • Catalytic Domain
  • Humans
  • Isoenzymes / chemistry
  • Isoenzymes / genetics
  • Isoenzymes / metabolism
  • Kinetics
  • Models, Molecular
  • Mutagenesis
  • N-Acetylgalactosaminyltransferases / chemistry
  • N-Acetylgalactosaminyltransferases / genetics
  • N-Acetylgalactosaminyltransferases / metabolism*
  • Polypeptide N-acetylgalactosaminyltransferase
  • Protein Engineering*
  • Substrate Specificity
  • Uridine Diphosphate / chemistry
  • Uridine Diphosphate / metabolism*

Substances

  • Isoenzymes
  • Uridine Diphosphate
  • N-Acetylgalactosaminyltransferases
  • Acetylgalactosamine