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Variations in the Expression of Terminal Oligosaccharide Units and Glycosylation of Poly(N-acetyllactosamine) Chain in the Helicobacter pylori Lipopolysaccharide upon Colonization of Rhesus Macaques

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Abstract

Helicobacter pylori is an important human pathogen that causes gastritis, gastric and duodenal ulcers, and gastric cancer. O-polysaccharides of H. pylori lipopolysaccharide (LPS) are composed of (β1→3)-poly(N-acetyllactosamine) (polyLacNAc) decorated with multiple α-L-fucose residues. In many strains, their terminal LacNAc units are mono- or difucosylated to mimic Lewis X (Lex) and/or Lewis Y (Ley) oligosaccharides. The studies in rhesus macaques as a model of human infection by H. pylori showed that this bacterium adapts to the host during colonization by expressing host Lewis antigens. Here, we characterized LPS from H. pylori strains used in the previous study, including the parental J166 strain and the three derivatives (98-149, 98-169, and 98-181) isolated from rhesus macaques after long-term colonization. Chemical and NMR spectroscopic analyses of the LPS showed that the parent strain expressed Lex, Ley, and H type 1 terminal oligosaccharide units. The daughter strains were similar to the parental one in the presence of the same LPS core and fucosylated polyLacNAc chain of the same length but differed in the terminal oligosaccharide units. These were Lex in the isolates 98-149 and 98-169, which corresponded to the Lea phenotype of the host animals, and Ley was found in the 98-181 isolate from the macaque characterized by the Leb phenotype. As Lea and Leb are isomers of Lex and Ley, respectively, the observed correlation confirmed adaptation of the expression of terminal oligosaccharide units in H. pylori strains to the properties of the host gastric mucosa. The 98-181 strain also acquired glucosylation of the polyLacNAc chain and was distinguished by a lower expression of fucosylated internal LacNAc units (internal Lex) as a result of decoration of polyLacNAc with β-glucopyranose, which may also play a role in the bacterial adaptation.

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Abbreviations

COSY:

correlation spectroscopy

DD-Hep and LD-Hep:

D-glycero- and L-glycero-D-manno-heptose

ESI MS:

electrospray ionization mass spectrometry

GLC:

gas-liquid chromatography

Kdo:

3-deoxy-D-manno-oct-2-ulosonic acid

LacNAc:

N-acetyllactosamine

Lea:

Leb, Lex, Ley, and H-1, Lewis a, Lewis b, Lewis X, Lewis Y and H type 1 antigens, respectively

LPS:

lipopolysaccharide

PEtn:

2-aminoethyl phosphate

polyLacNAc:

(β1→3)-poly(N-acetyllactosamine)

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Acknowledgements

The authors thank Prof. P.-E. Jansson (Karolinska Institute, Clinical Research Center, Huddinge University Hospital, Huddinge, Sweden) for the access to laboratory equipment, including an NMR spectrometer and a GLC-mass spectrometer, M. J. Blaser (New York University, New York, USA) for providing H. pylori strains, and A. P. Moran (National University of Ireland, Galway, Ireland) for cultivation of bacteria and valuable discussion.

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  1. Zelinsky Institute of Organic Chemistry, Russian Academy of Sciences, 119991, Moscow, Russia

    A. V. Perepelov, S. N. Senchenkova & Y. A. Knirel

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  1. A. V. Perepelov
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  2. S. N. Senchenkova
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  3. Y. A. Knirel
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Correspondence to A. V. Perepelov.

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Conflict of interest. The authors declare no conflict of interest in financial or any other area.

Published in Russian in Biokhimiya, 2020, Vol. 85, No. 2, pp. 272-279.

Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM19-289, December 30, 2019.

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Perepelov, A.V., Senchenkova, S.N. & Knirel, Y.A. Variations in the Expression of Terminal Oligosaccharide Units and Glycosylation of Poly(N-acetyllactosamine) Chain in the Helicobacter pylori Lipopolysaccharide upon Colonization of Rhesus Macaques. Biochemistry Moscow 85, 234–240 (2020). https://doi.org/10.1134/S0006297920020108

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  • DOI: https://doi.org/10.1134/S0006297920020108

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