A versatile fluorescence-quenched substrate for quantitative measurement of glucocerebrosidase activity within live cells

Proc Natl Acad Sci U S A. 2022 Jul 19;119(29):e2200553119. doi: 10.1073/pnas.2200553119. Epub 2022 Jul 12.

Abstract

Loss of activity of the lysosomal glycosidase β-glucocerebrosidase (GCase) causes the lysosomal storage disease Gaucher disease (GD) and has emerged as the greatest genetic risk factor for the development of both Parkinson disease (PD) and dementia with Lewy bodies. There is significant interest into how GCase dysfunction contributes to these diseases, however, progress toward a full understanding is complicated by presence of endogenous cellular factors that influence lysosomal GCase activity. Indeed, such factors are thought to contribute to the high degree of variable penetrance of GBA mutations among patients. Robust methods to quantitatively measure GCase activity within lysosomes are therefore needed to advance research in this area, as well as to develop clinical assays to monitor disease progression and assess GCase-directed therapeutics. Here, we report a selective fluorescence-quenched substrate, LysoFQ-GBA, which enables measuring endogenous levels of lysosomal GCase activity within living cells. LysoFQ-GBA is a sensitive tool for studying chemical or genetic perturbations of GCase activity using either fluorescence microscopy or flow cytometry. We validate the quantitative nature of measurements made with LysoFQ-GBA using various cell types and demonstrate that it accurately reports on both target engagement by GCase inhibitors and the GBA allele status of cells. Furthermore, through comparisons of GD, PD, and control patient-derived tissues, we show there is a close correlation in the lysosomal GCase activity within monocytes, neuronal progenitor cells, and neurons. Accordingly, analysis of clinical blood samples using LysoFQ-GBA may provide a surrogate marker of lysosomal GCase activity in neuronal tissue.

Keywords: Parkinson disease; enzyme kinetics; flow cytometry; fluorescence-quenched substrate; glycoside hydrolase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Gaucher Disease* / enzymology
  • Gaucher Disease* / genetics
  • Glucosylceramidase* / analysis
  • Glucosylceramidase* / genetics
  • Humans
  • Lewy Bodies / enzymology
  • Lewy Body Disease / enzymology
  • Lysosomes / enzymology
  • Mutation
  • Parkinson Disease* / enzymology
  • Parkinson Disease* / genetics
  • Substrate Specificity
  • alpha-Synuclein / metabolism

Substances

  • alpha-Synuclein
  • Glucosylceramidase