Characterization of the specific interaction between sialoadhesin and sialylated Campylobacter jejuni lipooligosaccharides.

A.P. Heikema, M.P. Bergman, H. Richards, P.R. Crocker, M. Gilbert, J.N. Samsom, W.J. Wamel, H.Ph. Endtz, A. van Belkum

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

In Campylobacter jejuni-induced Guillain-Barré syndrome (GBS), molecular mimicry between C. jejuni lipooligosaccharide (LOS) and host gangliosides leads to the production of cross-reactive antibodies directed against the peripheral nerves of the host. Currently, the presence of surface exposed sialylated LOS in C. jejuni is the single known bacterial pathogenesis factor associated with the development of GBS. Using a unique, well-characterized strain collection, we demonstrate that GBS-associated C. jejuni strains bind preferentially to sialoadhesin (Sn, Siglec-1, or CD169), a sialic acid receptor found on a subset of macrophages. In addition, using a whole-cell enzyme-linked immunosorbent assay (ELISA), C. jejuni strains with sialylated LOS bound exclusively to soluble Sn. Mass spectrometry revealed that binding was sialic acid-linkage specific with a preference for α(2,3)-linked sialic acid attached to the terminal galactose of the LOS chain as seen in the gangliosides GD1a, GM1b, and GM3. This molecular interaction was also related to functional consequences as a GBS-associated C. jejuni strain that bound Sn in a whole-cell ELISA adhered to surface-expressed Sn of Sn-transfected CHO cells but was unable to adhere to wild-type CHO cells. Moreover, a sialic acid-negative mutant of the same C. jejuni strain was unable to bind Sn-transfected CHO cells. This is the first report of the preferential binding of GBS-associated C. jejuni strains to the Sn immune receptor (P = 0.014). Moreover, because this binding is dependent on sialylated LOS, the main pathogenic factor in GBS progression, the present findings bring us closer to unraveling the mechanisms that lead to formation of cross-reactive antibodies in GBS disease. Copyright © 2010, American Society for Microbiology. All Rights Reserved.
Original languageEnglish
Pages (from-to)3237-3246
Number of pages10
JournalInfection and Immunity
Volume78
Issue number7
DOIs
Publication statusPublished - 2010

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Sialic Acid Binding Ig-like Lectin 1
Campylobacter jejuni
CHO Cells
N-Acetylneuraminic Acid
Enzyme-Linked Immunosorbent Assay
G(M3) Ganglioside
Molecular Mimicry
lipid-linked oligosaccharides
Antibodies
Gangliosides
Microbiology
Galactose
Peripheral Nerves
Mass Spectrometry
Macrophages

Cite this

Heikema, A.P. ; Bergman, M.P. ; Richards, H. ; Crocker, P.R. ; Gilbert, M. ; Samsom, J.N. ; Wamel, W.J. ; Endtz, H.Ph. ; van Belkum, A. / Characterization of the specific interaction between sialoadhesin and sialylated Campylobacter jejuni lipooligosaccharides. In: Infection and Immunity. 2010 ; Vol. 78, No. 7. pp. 3237-3246.
@article{6071b5ec0d914b3a81cfd2ace440ef16,
title = "Characterization of the specific interaction between sialoadhesin and sialylated Campylobacter jejuni lipooligosaccharides.",
abstract = "In Campylobacter jejuni-induced Guillain-Barr{\'e} syndrome (GBS), molecular mimicry between C. jejuni lipooligosaccharide (LOS) and host gangliosides leads to the production of cross-reactive antibodies directed against the peripheral nerves of the host. Currently, the presence of surface exposed sialylated LOS in C. jejuni is the single known bacterial pathogenesis factor associated with the development of GBS. Using a unique, well-characterized strain collection, we demonstrate that GBS-associated C. jejuni strains bind preferentially to sialoadhesin (Sn, Siglec-1, or CD169), a sialic acid receptor found on a subset of macrophages. In addition, using a whole-cell enzyme-linked immunosorbent assay (ELISA), C. jejuni strains with sialylated LOS bound exclusively to soluble Sn. Mass spectrometry revealed that binding was sialic acid-linkage specific with a preference for α(2,3)-linked sialic acid attached to the terminal galactose of the LOS chain as seen in the gangliosides GD1a, GM1b, and GM3. This molecular interaction was also related to functional consequences as a GBS-associated C. jejuni strain that bound Sn in a whole-cell ELISA adhered to surface-expressed Sn of Sn-transfected CHO cells but was unable to adhere to wild-type CHO cells. Moreover, a sialic acid-negative mutant of the same C. jejuni strain was unable to bind Sn-transfected CHO cells. This is the first report of the preferential binding of GBS-associated C. jejuni strains to the Sn immune receptor (P = 0.014). Moreover, because this binding is dependent on sialylated LOS, the main pathogenic factor in GBS progression, the present findings bring us closer to unraveling the mechanisms that lead to formation of cross-reactive antibodies in GBS disease. Copyright {\circledC} 2010, American Society for Microbiology. All Rights Reserved.",
author = "A.P. Heikema and M.P. Bergman and H. Richards and P.R. Crocker and M. Gilbert and J.N. Samsom and W.J. Wamel and H.Ph. Endtz and {van Belkum}, A.",
year = "2010",
doi = "10.1128/IAI.01273-09",
language = "English",
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Heikema, AP, Bergman, MP, Richards, H, Crocker, PR, Gilbert, M, Samsom, JN, Wamel, WJ, Endtz, HP & van Belkum, A 2010, 'Characterization of the specific interaction between sialoadhesin and sialylated Campylobacter jejuni lipooligosaccharides.' Infection and Immunity, vol. 78, no. 7, pp. 3237-3246. https://doi.org/10.1128/IAI.01273-09

Characterization of the specific interaction between sialoadhesin and sialylated Campylobacter jejuni lipooligosaccharides. / Heikema, A.P.; Bergman, M.P.; Richards, H.; Crocker, P.R.; Gilbert, M.; Samsom, J.N.; Wamel, W.J.; Endtz, H.Ph.; van Belkum, A.

In: Infection and Immunity, Vol. 78, No. 7, 2010, p. 3237-3246.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - Characterization of the specific interaction between sialoadhesin and sialylated Campylobacter jejuni lipooligosaccharides.

AU - Heikema, A.P.

AU - Bergman, M.P.

AU - Richards, H.

AU - Crocker, P.R.

AU - Gilbert, M.

AU - Samsom, J.N.

AU - Wamel, W.J.

AU - Endtz, H.Ph.

AU - van Belkum, A.

PY - 2010

Y1 - 2010

N2 - In Campylobacter jejuni-induced Guillain-Barré syndrome (GBS), molecular mimicry between C. jejuni lipooligosaccharide (LOS) and host gangliosides leads to the production of cross-reactive antibodies directed against the peripheral nerves of the host. Currently, the presence of surface exposed sialylated LOS in C. jejuni is the single known bacterial pathogenesis factor associated with the development of GBS. Using a unique, well-characterized strain collection, we demonstrate that GBS-associated C. jejuni strains bind preferentially to sialoadhesin (Sn, Siglec-1, or CD169), a sialic acid receptor found on a subset of macrophages. In addition, using a whole-cell enzyme-linked immunosorbent assay (ELISA), C. jejuni strains with sialylated LOS bound exclusively to soluble Sn. Mass spectrometry revealed that binding was sialic acid-linkage specific with a preference for α(2,3)-linked sialic acid attached to the terminal galactose of the LOS chain as seen in the gangliosides GD1a, GM1b, and GM3. This molecular interaction was also related to functional consequences as a GBS-associated C. jejuni strain that bound Sn in a whole-cell ELISA adhered to surface-expressed Sn of Sn-transfected CHO cells but was unable to adhere to wild-type CHO cells. Moreover, a sialic acid-negative mutant of the same C. jejuni strain was unable to bind Sn-transfected CHO cells. This is the first report of the preferential binding of GBS-associated C. jejuni strains to the Sn immune receptor (P = 0.014). Moreover, because this binding is dependent on sialylated LOS, the main pathogenic factor in GBS progression, the present findings bring us closer to unraveling the mechanisms that lead to formation of cross-reactive antibodies in GBS disease. Copyright © 2010, American Society for Microbiology. All Rights Reserved.

AB - In Campylobacter jejuni-induced Guillain-Barré syndrome (GBS), molecular mimicry between C. jejuni lipooligosaccharide (LOS) and host gangliosides leads to the production of cross-reactive antibodies directed against the peripheral nerves of the host. Currently, the presence of surface exposed sialylated LOS in C. jejuni is the single known bacterial pathogenesis factor associated with the development of GBS. Using a unique, well-characterized strain collection, we demonstrate that GBS-associated C. jejuni strains bind preferentially to sialoadhesin (Sn, Siglec-1, or CD169), a sialic acid receptor found on a subset of macrophages. In addition, using a whole-cell enzyme-linked immunosorbent assay (ELISA), C. jejuni strains with sialylated LOS bound exclusively to soluble Sn. Mass spectrometry revealed that binding was sialic acid-linkage specific with a preference for α(2,3)-linked sialic acid attached to the terminal galactose of the LOS chain as seen in the gangliosides GD1a, GM1b, and GM3. This molecular interaction was also related to functional consequences as a GBS-associated C. jejuni strain that bound Sn in a whole-cell ELISA adhered to surface-expressed Sn of Sn-transfected CHO cells but was unable to adhere to wild-type CHO cells. Moreover, a sialic acid-negative mutant of the same C. jejuni strain was unable to bind Sn-transfected CHO cells. This is the first report of the preferential binding of GBS-associated C. jejuni strains to the Sn immune receptor (P = 0.014). Moreover, because this binding is dependent on sialylated LOS, the main pathogenic factor in GBS progression, the present findings bring us closer to unraveling the mechanisms that lead to formation of cross-reactive antibodies in GBS disease. Copyright © 2010, American Society for Microbiology. All Rights Reserved.

U2 - 10.1128/IAI.01273-09

DO - 10.1128/IAI.01273-09

M3 - Article

VL - 78

SP - 3237

EP - 3246

JO - Infection and Immunity

JF - Infection and Immunity

SN - 0019-9567

IS - 7

ER -