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Anomerisation of fluorinated sugars by mutarotase studied by 19F NMR two-dimensional exchange spectroscopy

Anomerisation of fluorinated sugars by mutarotase studied by 19F NMR two-dimensional exchange spectroscopy
Anomerisation of fluorinated sugars by mutarotase studied by 19F NMR two-dimensional exchange spectroscopy

Five 19F-substituted glucose analogues were used to probe the activity and mechanism of the enzyme mutarotase by using magnetisation-exchange NMR spectroscopy. The sugars (2-fluoro-2-deoxy-d-glucose, FDG2; 3-fluoro-3-deoxy-d-glucose, FDG3; 4-fluoro-4-deoxy-d-glucose, FDG4; 2,3-difluoro-2,3-dideoxy-d-glucose, FDG23; and 2,2,3,3-tetrafluoro-2,3-dideoxy-d-glucose (2,3-dideoxy-2,2,3,3-tetrafluoro-d-erythro-hexopyranose), FDG2233) showed separate 19F NMR spectroscopic resonances from their respective α- and β-anomers, thus allowing two-dimensional exchange spectroscopy measurements of the anomeric interconversion at equilibrium, on the time scale of a few seconds. Mutarotase catalysed the rapid exchange between the anomers of FDG4, but not the other four sugars. This finding, combined with previous work identifying the mechanism of the anomerisation by mutarotase, suggests that the rotation around the C1-C2 bond of the pyranose ring is the rate-limiting reaction step. In addition to d-glucose itself, it was shown that all other fluorinated sugars inhibited the FDG4 anomerisation, with the tetrafluorinated FDG2233 being the most potent inhibitor. Inhibition of mutarotase by F-sugars paves the way for the development of novel fluorinated compounds that are able to affect the activity of this enzyme in vitro and in vivo.

2D exchange spectroscopy, NMR, enzyme inhibition, enzyme mechanism, fluorinated glucose, mutarotase
0004-9425
117-128
Shishmarev, Dmitry
11bac3f9-42c3-42ba-b3d1-e5fc06365580
Quiquempoix, Lucas G
1664af14-ee65-4888-884b-5331983a25ba
Fontenelle, Clement Q.
c746c5ea-96bc-46c2-849d-47215ab58c03
Linclau, Bruno
19b9cacd-b8e8-4c65-af36-6352cade84ba
Kuchel, Philip W.
62f434b1-d370-4552-85f4-05b76c625945
Shishmarev, Dmitry
11bac3f9-42c3-42ba-b3d1-e5fc06365580
Quiquempoix, Lucas G
1664af14-ee65-4888-884b-5331983a25ba
Fontenelle, Clement Q.
c746c5ea-96bc-46c2-849d-47215ab58c03
Linclau, Bruno
19b9cacd-b8e8-4c65-af36-6352cade84ba
Kuchel, Philip W.
62f434b1-d370-4552-85f4-05b76c625945

Shishmarev, Dmitry, Quiquempoix, Lucas G, Fontenelle, Clement Q., Linclau, Bruno and Kuchel, Philip W. (2020) Anomerisation of fluorinated sugars by mutarotase studied by 19F NMR two-dimensional exchange spectroscopy. Australian Journal of Chemistry, 73 (3), 117-128. (doi:10.1071/CH19562).

Record type: Article

Abstract

Five 19F-substituted glucose analogues were used to probe the activity and mechanism of the enzyme mutarotase by using magnetisation-exchange NMR spectroscopy. The sugars (2-fluoro-2-deoxy-d-glucose, FDG2; 3-fluoro-3-deoxy-d-glucose, FDG3; 4-fluoro-4-deoxy-d-glucose, FDG4; 2,3-difluoro-2,3-dideoxy-d-glucose, FDG23; and 2,2,3,3-tetrafluoro-2,3-dideoxy-d-glucose (2,3-dideoxy-2,2,3,3-tetrafluoro-d-erythro-hexopyranose), FDG2233) showed separate 19F NMR spectroscopic resonances from their respective α- and β-anomers, thus allowing two-dimensional exchange spectroscopy measurements of the anomeric interconversion at equilibrium, on the time scale of a few seconds. Mutarotase catalysed the rapid exchange between the anomers of FDG4, but not the other four sugars. This finding, combined with previous work identifying the mechanism of the anomerisation by mutarotase, suggests that the rotation around the C1-C2 bond of the pyranose ring is the rate-limiting reaction step. In addition to d-glucose itself, it was shown that all other fluorinated sugars inhibited the FDG4 anomerisation, with the tetrafluorinated FDG2233 being the most potent inhibitor. Inhibition of mutarotase by F-sugars paves the way for the development of novel fluorinated compounds that are able to affect the activity of this enzyme in vitro and in vivo.

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Mutarotase paper 2 FINAL_PWK - Accepted Manuscript
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Accepted/In Press date: 18 November 2019
e-pub ahead of print date: 29 January 2020
Published date: March 2020
Additional Information: Funding Information: The work was funded by a grant from the Leverhulme Trust (RPG-2015-211) and from the Australian Research Council (DP140102596). Dr Seung Seo Lee, University of Southampton, is thanked for critical and insightful comments on the manuscript; and the authors thank the University’s instrumentation umbrella organisation Sydney Analytical, and Dr Ann Kwan in particular, for the maintenance and supervision of the NMR spectrometers at the University of Sydney. Publisher Copyright: © 2020 CSIRO.
Keywords: 2D exchange spectroscopy, NMR, enzyme inhibition, enzyme mechanism, fluorinated glucose, mutarotase

Identifiers

Local EPrints ID: 436314
URI: http://eprints.soton.ac.uk/id/eprint/436314
ISSN: 0004-9425
PURE UUID: f2148d6a-5789-492f-aac0-33d41fd7f16c
ORCID for Clement Q. Fontenelle: ORCID iD orcid.org/0000-0002-1630-3407
ORCID for Bruno Linclau: ORCID iD orcid.org/0000-0001-8762-0170

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Date deposited: 06 Dec 2019 17:30
Last modified: 17 Mar 2024 05:06

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Contributors

Author: Dmitry Shishmarev
Author: Lucas G Quiquempoix
Author: Clement Q. Fontenelle ORCID iD
Author: Bruno Linclau ORCID iD
Author: Philip W. Kuchel

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