O-Linked Flagellar Glycosylation in Campylobacter

Susan M. Logan; Ian C. Schoenhofen; Patricia Guerry

doi:10.1128/9781555815554.ch26

Chapter 26 : O-Linked Flagellar Glycosylation in Campylobacter

Authors: Susan M. Logan¹, Ian C. Schoenhofen², Patricia Guerry³

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Affiliations: 1: Institute for Biological Sciences, National Research Council of Canada, Ottawa, Canada ON K1A OR6; 2: Institute for Biological Sciences, National Research Council of Canada, Ottawa, Canada ON K1A OR6; 3: Naval Medical Research Center, Silver Spring, MD 20910

Content Type: Monograph

Publication Year: 2008

Category: Bacterial Pathogenesis

Book DOI: 10.1128/9781555815554

Chapter DOI: 10.1128/9781555815554.ch26

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Abstract:

Protein glycosylation has long been recognized as an important posttranslational modification in eukaryotic systems and one that imparts unique and diverse biological functions to the respective proteins. Although there is a considerable gap in our knowledge on the process of O-linked glycosylation in prokaryotes as a result of the significant glycan diversity among prokaryotes, the O-linked flagellar glycosylation system of Campylobacter has received considerable attention and is one of the more detailed prokaryotic systems studied to date. The first evidence for posttranslational modification of Campylobacter flagellin came from Campylobacter coli VC167 flagellin by direct chemical analysis of purified flagellar peptides. Mapping of glycosylation sites of C. coli VC167 flagellin also confirmed a conservation in localization to the central region of the monomer. Comparative genomic analyses of Campylobacter isolates has revealed that the flagellar locus displays considerable genetic variability. The glycans on flagellin appear to play complex roles in the biology of Campylobacter. The role of glycan composition on flagellar filaments was examined in vivo. Flagellins from the Epsilonproteobacteria, including both Campylobacter and Helicobacter spp., are not recognized by TLR5 receptors. Significant progress has been made in defining at the molecular level the structural nature of the novel sialic acid-like nonulosonate sugars found to be decorating the flagellar filaments of Campylobacter, and it is clear that these types of studies will be integral to future work exploring the role of novel glycan moieties in biological interactions.

Citation: Logan S, Schoenhofen I, Guerry P. 2008. O-Linked Flagellar Glycosylation in Campylobacter, p 471-481. In Nachamkin I, Szymanski C, Blaser M (ed), Campylobacter, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch26

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O-Linked Flagellar Glycosylation in Campylobacter

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Figure 1.

Localization of flagellar glycosylation sites to surface-exposed regions of each monomer within the assembled filament. (A) Structure of FliC from S. enterica serovar Typhimurium with major domains labeled as previously described ( Samatey et al., 2000 ; Yonekura et al., 2003 , 2005 ). The Protein Data Bank accession code is 1UCU and is displayed in Protein Explorer. (B) Assignment map of C. jejuni flagellin 81-176. The primary amino acid sequence of FlaA is shown, and modified residues are highlighted. The sequences corresponding to ND0, ND1, D2, D3, CD1, and CD0 domains from the FliC structure are indicated for FlaA on the left side.

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Figure 1.

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Figure 2.

Structures of glycans found on Campylobacter flagellins compared with that of sialic acid. (A) Sialic acid or 5-acetamido-3,5-dideoxy-d–glycero-β-d–galacto-nonulosonic acid (Neu5Ac). (B) Pseudaminic acid or 5,7-diacetamido-3,5,7,9-tetradeoxy-l–glycero-α-l–manno-nonulosonic acid and derivatives. (C) Legionaminic acid or 5,7-diacetamido-3,5,7,9-tetradeoxy-d–glycero-β-d–galacto-nonulosonic acid and derivatives. Known R groups are shown for both (B) and (C), illustrating the diversity of functional groups observed for each. Sialic acid and legionaminic acid exhibit the same d–glycero- d–galacto absolute configuration. Confirmation of α or β linkage of B and C to flagellin has yet to be determined.

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Figure 2.

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Figure 3.

CMP-Pse pathway of Campylobacter jejuni. The enzymes and biosynthetic intermediates of the CMP–pseudaminic acid pathway, in order, are PseB, NAD(P)-dependent dehydratase/epimerase; PseC, PLP-dependent aminotransferase; PseH, N-acetyltransferase; PseG, UDP-sugar hydrolase; PseI, pseudaminic acid synthase; PseF, CMP-pseudaminic acid synthetase; and (I) UDP-GlcNAc; (II) UDP-2-acetamido-2,6-dideoxy-β-l–arabino-hexos-4-ulose; (III) UDP-4-amino-4,6-dideoxy-β-l-AltNAc; (IV) UDP-2,4-diacetamido-2,4,6-trideoxy-β-l-altropyranose; (V) 2,4-diacetamido-2,4,6-trideoxy-l-altropyranose; (VI) pseudaminic acid; (VII) CMP–pseudaminic acid. Pyranose rings are shown as their predominant chair conformation in solution determined from nuclear Overhauser effects (NOEs) and J H,H coupling constants. Schematic representations of PseB and PseC structures from H. pylori are shown ( Ishiyama et al., 2006 ; Schoenhofen et al., 2006a ).

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Figure 3.

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Figure 4.

Adherence pattern of green fluorescent protein (GPF)-tagged C. jejuni 81-176 cells to INT407 cells. A microcolony of C. jejuni 81-176 tagged with GFP on INT407 cells in culture after 18-h incubation ( Guerry et al., 2006 ). The image shows complex interactions of bacteria on the intestinal epithelial cells, and some of the bacteria are visible as apparent chains. Phase microscopy of the same field confirmed that the monolayer remained intact.

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Figure 4.

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Figure 5.

Molecular models of Pse5Ac7Ac, Leg5Am7Ac, and Leg5AmNMe7Ac. The exocyclic chain (C7 to C9) and pendant groups at C5 and C7 are displayed as reduced van der Waals spheres to show the extent of their structural diversities. Coordinates are available at http://ibs-isb.nrc-cnrc.gc.ca/facilities/NMR/molecularmodeling-e.html. From McNally et al. (2007) .

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Figure 5.

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Tables

O-Linked Flagellar Glycosylation in Campylobacter

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Table 1.

Campylobacter O-linked flagellar glycans

Table 1.

Campylobacter O-linked flagellar glycans