A sensitive gel-based method combining distinct cyclophellitol-based probes for the identification of acid/base residues in human retaining β-glucosidases

J Biol Chem. 2014 Dec 19;289(51):35351-62. doi: 10.1074/jbc.M114.593376. Epub 2014 Oct 24.

Abstract

Retaining β-exoglucosidases operate by a mechanism in which the key amino acids driving the glycosidic bond hydrolysis act as catalytic acid/base and nucleophile. Recently we designed two distinct classes of fluorescent cyclophellitol-type activity-based probes (ABPs) that exploit this mechanism to covalently modify the nucleophile of retaining β-glucosidases. Whereas β-epoxide ABPs require a protonated acid/base for irreversible inhibition of retaining β-glucosidases, β-aziridine ABPs do not. Here we describe a novel sensitive method to identify both catalytic residues of retaining β-glucosidases by the combined use of cyclophellitol β-epoxide- and β-aziridine ABPs. In this approach putative catalytic residues are first substituted to noncarboxylic amino acids such as glycine or glutamine through site-directed mutagenesis. Next, the acid/base and nucleophile can be identified via classical sodium azide-mediated rescue of mutants thereof. Selective labeling with fluorescent β-aziridine but not β-epoxide ABPs identifies the acid/base residue in mutagenized enzyme, as only the β-aziridine ABP can bind in its absence. The Absence of the nucleophile abolishes any ABP labeling. We validated the method by using the retaining β-glucosidase GBA (CAZy glycosylhydrolase family GH30) and then applied it to non-homologous (putative) retaining β-glucosidases categorized in GH1 and GH116: GBA2, GBA3, and LPH. The described method is highly sensitive, requiring only femtomoles (nanograms) of ABP-labeled enzymes.

Keywords: Acid/Base; Activity-based Probe; Gaucher Disease; Glycobiology; Glycoconjugate; Glycolipid; Glycosidase; Labeling; Nucleophile.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • Amino Acids / chemistry
  • Amino Acids / genetics
  • Amino Acids / metabolism*
  • Animals
  • Aziridines / chemistry
  • Aziridines / metabolism
  • COS Cells
  • Catalytic Domain
  • Chlorocebus aethiops
  • Cyclohexanols / chemistry
  • Cyclohexanols / metabolism*
  • Epoxy Compounds / chemistry
  • Epoxy Compounds / metabolism
  • Humans
  • Hydrolysis
  • Immunoblotting / methods
  • Molecular Probes / chemistry
  • Molecular Probes / metabolism*
  • Mutagenesis, Site-Directed
  • Mutation, Missense
  • Reproducibility of Results
  • Sodium Azide / chemistry
  • Sodium Azide / metabolism
  • Substrate Specificity
  • beta-Glucosidase / chemistry
  • beta-Glucosidase / genetics
  • beta-Glucosidase / metabolism*

Substances

  • Amino Acids
  • Aziridines
  • Cyclohexanols
  • Epoxy Compounds
  • Molecular Probes
  • cyclophellitol
  • aziridine
  • Sodium Azide
  • beta-Glucosidase