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Cited by 7Glycosylation and Glycoproteins ResearchCarbohydrate Chemistry and SynthesisEnzyme Production and Characterization

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A novel family of sugar-specific phosphodiesterases that remove zwitterionic modifications of GlcNAc

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Fossa, Samantha L., Anton, Brian P., Kneller, Daniel W., Petralia, Laudine M.C., Ganatra, Mehul B., Boisvert, Madison L., Vainauskas, Saulius, Chan, Siu-Hong, Hokke, Cornelis H., Foster, Jeremy M., Taron, Christopher H.·2023·Journal of Biological Chemistry
DOI 10.1016/j.jbc.2023.105437PMC PMC10704324

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Abstract

The zwitterions phosphorylcholine (PC) and phosphoethanolamine (PE) are often found esterified to certain sugars in polysaccharides and glycoconjugates in a wide range of biological species. One such modification involves PC attachment to the 6-carbon of N-acetylglucosamine (GlcNAc-6-PC) in N-glycans and glycosphingolipids (GSLs) of parasitic nematodes, a modification that helps the parasite evade host immunity. Knowledge of enzymes involved in the synthesis and degradation of PC and PE modifications is limited. More detailed studies on such enzymes would contribute to a better understanding of the function of PC modifications and have potential application in the structural analysis of zwitterion-modified glycans. In this study, we used functional metagenomic screening to identify phosphodiesterases encoded in a human fecal DNA fosmid library that remove PC from GlcNAc-6-PC. A novel bacterial phosphodiesterase was identified and biochemically characterized. This enzyme (termed GlcNAc-PDase) shows remarkable substrate preference for GlcNAc-6-PC and GlcNAc-6-PE, with little or no activity on other zwitterion-modified hexoses. The identified GlcNAc-PDase protein sequence is a member of the large endonuclease/exonuclease/phosphatase superfamily where it defines a distinct subfamily of related sequences of previously unknown function, mostly from Clostridium bacteria species. Finally, we demonstrate use of GlcNAc-PDase to confirm the presence of GlcNAc-6-PC in N-glycans and GSLs of the parasitic nematode Brugia malayi in a glycoanalytical workflow.

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Metadata

Authors
Fossa, S. L., Anton, B. P., Kneller, D. W., Petralia, L. M. C., Ganatra, M. B., Boisvert, M. L., Vainauskas, S., Chan, S.-H., Hokke, C. H., Foster, J. M., & Taron, C. H.
Affiliations
  • New England Biolabs (United States) (US)
  • Leiden University (NL)
Corresponding author
Taron, Christopher H.
ORCID
Venue
Journal of Biological Chemistry
Publisher
Elsevier BV
Published
2023-12
Volume
299
Issue
12
Pages
105437
ISSN
0021-9258 (ISSN-L)
DOI
10.1016/j.jbc.2023.105437
PMC
PMC10704324
OpenAlex
W4388451840
Cited by
7
References
2
Citations by year
2026: 3 · 2025: 2 · 2024: 2
FWCI
0.62
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Biological Chemistry (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
New England Biolabs
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
  • Physical Sciences › Chemistry › Organic Chemistry › Carbohydrate Chemistry and Synthesis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Enzyme Production and Characterization
Keywords
phosphodiesterase, phosphorylcholine, phosphoethanolamine, N-glycans, glycosphingolipids, Brugia malayi, parasitic nematodes, Clostridium, human gut bacteria, parasite immune evasion
MeSH terms
Sugars, Acetylglucosamine, Carbohydrates, Glycoconjugates, Humans, Phosphoric Diester Hydrolases, Polysaccharides

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