S115
Structure and Conserved Characteristics of Campylobacter jejuni
Lipopolysaccharides
Anthony P. Moran
Department of Microbiology, National University of Ireland, Galway,
Galway, Ireland
The lipid A component of Campylobacter jejuni lipopolysaccharides (LPSs) contains the same
architectural principle as that found in other bacterial species; however, unlike the case with other
bacterial species, the lipid A backbone of C. jejuni strains is composed of a phosphorylated b(1*6) – linked disaccharide containing 2,3-diamino-2,3-dideoxy-D-glucose and D-glucosamine as the
major molecular species. Despite a backbone that differs structurally from that of classic enterobacterial lipid A, C. jejuni lipid A is antigenically similar to enterobacterial lipid A, and the respective LPSs
have comparable endotoxic activities. Structural variability is greater in the core oligosaccharide than
in lipid A of C. jejuni LPS. Nevertheless, the inner core oligosaccharides of C. jejuni strains share
a common unique tetrasaccharide and also possess a trisaccharide that occurs in the inner core of
other bacterial species. Ganglioside mimicry in the outer core is a common feature shared by a
number of C. jejuni serotypes, but this mimicry is not conserved in all serotypes.
Lipopolysaccharides (LPSs), also termed endotoxins, are
constituents of the outer membrane of most gram-negative bacteria, including Campylobacter jejuni [1]. In general, LPSs are
a family of toxic phosphorylated glycolipids that are the main
surface antigens (O-antigens) of gram-negative bacteria and
are essential for the physical integrity and functioning of the
outer membrane [2].
As surface structures, these glycolipids play an important
role in the interaction of gram-negative bacteria with their
environment and with higher organisms. LPS molecules possess binding sites for antibodies and serum factors and, hence,
are involved in recognition and elimination of bacteria by the
host’s defense system [1, 3]. They are potent immunostimulators and strongly activate B lymphocytes, granulocytes, and
mononuclear cells [1, 4, 5]. Low doses of LPS are considered
to be beneficial to the host by causing immunostimulation and
enhanced resistance to infections and malignancy. However,
LPSs possess a broad spectrum of endotoxic activities (e.g.,
pyrogenicity and lethal toxicity), which contribute to the pathogenic potential of gram-negative bacteria [1, 4]. Furthermore,
variations in the saccharide moiety of LPS may prevent efficient complement activation and phagocytosis, thereby contributing to the virulence of bacterial infections [6].
Herein, the structure of C. jejuni LPSs is reviewed, the common
structural characteristics shared by LPSs of different C. jejuni
Presented: Workshop on the Development of Guillain-Barré Syndrome following Campylobacter Infection, National Institute of Allergy and Infectious
Diseases, National Institutes of Health, Bethesda, Maryland, 26 – 27 August
1996.
Grant support: Irish Health Research Board (HRB 86-95).
Reprints or correspondence: Dr. Anthony P. Moran, Dept. of Microbiology,
National University of Ireland, Galway, University Rd., Galway, Ireland.
The Journal of Infectious Diseases 1997;176(Suppl 2):S115–21
q 1997 by The University of Chicago. All rights reserved.
0022–1899/97/76S2–0006$02.00
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strains are defined, and the contribution of these characteristics
to the pathogenic potential of the bacterium is addressed.
General Structure of LPS
Structurally, LPSs of various bacterial species share a common architecture of a polysaccharide or oligosaccharide (OS)
covalently bound to a lipid component, lipid A. High – relative
molecular – mass (high-Mr), smooth-form LPS, as characterized
by enterobacterial LPS (figure 1), consists of three principal
domains [1, 3, 5], and each of these domains has different
structural and functional properties.
The O-specific chain, the outer polysaccharide moiety, contributes to the antigenicity and serospecificity of the native
molecule and is a polymer of identical repeating units that may
contain up to seven different sugars [1]. The nature, ring form,
anomeric configuration, and type of substitution of the individual monosaccharide residues and their sequence within a repeating unit is characteristic for a given LPS and the parental
bacterial strain. The second domain, the core OS, is composed
of a short series of sugars (10 – 15), mediates binding of activated T lymphocytes, is involved in immunomodulation, and
is essential for the permeation properties of the bacterial outer
membrane [1 – 3]. The innermost component, lipid A, anchors
LPS in the outer membrane and endows the molecule with its
immunologic and endotoxic properties [1, 3 – 5]. The degree
of bioactivity of lipid A may be modulated by the saccharide
region of LPS, particularly the core OS [5]. Generally, for a
given bacterial species, the structure of lipid A is highly conserved, whereas that of the core OS is more variable, and that
of the O-specific chain is highly variable.
A second type of LPS, low – relative molecular – weight (lowMr), rough-form LPS without an O-specific chain is produced
by enterobacterial mutants because of genetic defects in the
biosynthesis of LPS [2]. Also, wild-type isolates of Neisseria
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Figure 1. Schematic architecture
of enterobacterial LPS.
and Haemophilus species produce low-Mr LPS without an Ochain, sometimes termed lipooligosaccharide, which has properties distinct from those of enterobacterial rough-form LPS,
particularly antigenic diversity [7].
Architecture of C. jejuni LPS
Like wild-type isolates of the Enterobacteriaceae, one-third
of C. jejuni serostrains (serotype reference strains) have been
shown to produce high-Mr LPS [8]. In contrast to enterobacterial LPS, which can be visualized in electrophoretic gels by
silver staining, C. jejuni high-Mr LPS from phenol-water extracts can only be visualized with the more sensitive technique
of immunostaining. However, ladder-like patterns characteristic of high-Mr LPS were observed in silver-stained electrophoretic gels of C. jejuni LPS extracted by a different technique
[9]. The basis for the lack of reactivity of the high-Mr molecules
from phenol-water extracts with the silver stain has not been
resolved but may be due to low concentrations of molecules
containing O-specific chains in these preparations. Nevertheless, the structures of a number of C. jejuni O-chains have been
established by chemical analysis of LPS from phenol-water
extracts [10, 11].
The remaining two-thirds of C. jejuni serostrains produce
low-Mr LPS [8]. Preliminary electrophoretic investigations suggested this LPS resembled enterobacterial rough-form LPS
lacking the O-specific chain [12 – 14]. However, structural studies have shown that they more closely resemble the low-Mr
LPS of Neisseria and Haemophilus species [15 – 18] and have
properties distinct from those of enterobacterial rough-form
LPS, particularly antigenic diversity [8, 19].
Lipid A
General structure. Comparison of lipid As of different
gram-negative genera and families reveals that they possess a
similar architectural principle [1, 3 – 5, 20]. Variations in structure result from the type of hexosamine present, the degree of
phosphorylation, the presence of phosphate substituents, and
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most notably, the nature, chain length, number, and location
of fatty acyl chains [4, 20]. Despite these variations, lipid A,
compared with the other LPS regions, exhibits a rather low
structural variability.
Endotoxically active lipid A, exemplified by the lipid As of
Escherichia coli (figure 2A) and of Salmonella minnesota (figure 2B), contains a hydrophilic backbone of a b(1*-6)-linked
D-glucosamine (GlcN) disaccharide carrying phosphate groups
at positions 1 and 4* and substituted by hydrophobic fatty acids
[1, 4, 20]. Six fatty acids, 12 – 14 carbons in length, are esteror amide-linked on the backbone in an asymmetric distribution;
(R)-3-hydroxy fatty acids occur at positions 2 and 3, whereas
(R)-3-acyloxyacyl residues occur at positions 2* and 3*. In S.
minnesota lipid A, however, a second molecular species occurs
due to nonstoichiometric substitution with an extra acyl residue,
hexadecanoic acid (16:0), on the (R)-3-hydroxytetradecanoic
(3-OH-14:0) acid at position 2. Further heterogeneity arises
due to the nonstoichiometric substitution of phosphoryl headgroups at position 1 with phosphate (E. coli) or ethanolaminephosphate (S. minnesota) and at position 4* with 4-amino-4deoxy-L-arabinose (S. minnesota).
Deviating backbone structures have been described and are
composed of a GlcN3N monosaccharide, a phosphorylated 2,3diamino-2,3-dideoxy-D-glucose (GlcN3N) disaccharide, or a glucosaminuronic acid monosaccharide, which possess different
biologic activities [4, 20–23]. In addition to lipid A structures
containing either GlcN (e.g., in Enterobacteriaceae) or GlcN3N
(e.g., in Rhodopseudomonas viridis and Pseudomonas diminuta),
mixed lipid A containing both GlcN and GlcN3N have been
reported (e.g., in some Brucella and Thiobacillus species and in
species of the Chromatiaceae and Rhizobiaceae) [21].
Mixed lipid A of C. jejuni. Although initial studies reported
the presence of GlcN in C. jejuni LPS and lipid A [24 – 27],
more detailed investigations by my colleagues and I showed
that both GlcN and GlcN3N occurred in LPSs and lipid A of
a number of C. jejuni strains [28, 29]. Structural analysis of
this mixed lipid A from C. jejuni O:2 showed that the major
molecular species (figure 3) is a hybrid backbone of a b(1*6)-linked GlcN3N-GlcN disaccharide carrying phosphate
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Structure of C. jejuni LPS
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Figure 2. Chemical structure of lipid A of Escherichia coli (A) and Salmonella minnesota (B) [1, 4, 20]. Hydroxyl group at position 6* (on
GlcN II) constitutes attachment site of core oligosaccharide. Nos. in circles indicate no. of carbon atoms in fatty acyl chains; 14:0(3-OH)
residues possess (R) configuration. Dotted line indicates nonstoichiometric substitution. Note presence of 6 fatty acids attached to D-glucosamine
disaccharide backbone with 2 phosphate groups at position 1 (GlcN I) and position 4* (GlcN II).
Figure 3. Chemical structure of major component of lipid A of
Campylobacter jejuni O:2 [30]. Compared with enterobacterial lipid
A (figure 1), note presence of GlcN3N-GlcN backbone disaccharide
with amide group at position 3* (arrow). As occurs in Salmonella
minnesota lipid A, heterogeneity in substitution of lipid A backbone
is present in C. jejuni. At position 2*, 16:0 on 14:0(3-OH) is partially
(20%) replaced by 14:0, and nonstoichiometric substitution of phosphate groups occurs (position 1: ethanolamine or ethanolamine-phosphate; position 4*: ethanolamine-phosphate).
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groups at positions 1 and 4* and substituted with six fatty acids
[30], in an architecture similar to that seen in enterobacterial
lipid A [1, 4, 20]. Two other lipid A backbone species are
present: one with a b(1*-6)-linked GlcN-GlcN disaccharide
(12%), and the other with a GlcN3N-GlcN3N disaccharide
(15%), both of which are phosphorylated and acylated in a
manner similar to that for the major backbone species [30].
The presence of both GlcN and GlcN3N in lipid A is a
common property of all C. jejuni serostrains examined [28,
29]. Nevertheless, interstrain variation in the molar ratios of
GlcN and GlcN3N in C. jejuni lipid A may occur. Structural
analysis of lipid A from different C. jejuni serostrains confirmed the presence of the same type of backbone structures
with substitution patterns identical to those encountered in C.
jejuni O:2 lipid A, but the relative proportions of the various
backbones differed [31].
Apart from the occurrence of GlcN3N in two of the lipid A
backbone disaccharides (GlcN3N-GlcN and GlcN3N-GlcN3N),
including the major backbone species, the architecture of the C.
jejuni lipid A component conforms with the structural principle
encountered in many lipid As, especially enterobacterial lipid
A [1, 4, 20]. Although GlcN3N is present in the backbone of
C. jejuni lipid A, antigenically, the latter resembled classic
enterobacterial lipid A when tested with anti-lipid A antibodies
[29]. Since both GlcN and GlcN3N possess the gluco-configuration, the only structural influence exerted by the occurrence
of GlcN3N in the backbone disaccharides is the presence of a
higher proportion of amide-bound 3-OH-14:0 (75% of the total
for GlcN3N-GlcN, compared with 50% for a GlcN-GlcN disaccharide backbone).
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Despite the presence of a high proportion of a longer fatty
acid (16:0) in C. jejuni lipid A than in enterobacterial lipid A
and the production of a lipid A backbone containing a hybrid
disaccharide as its main molecular species, C. jejuni LPS, compared with enterobacterial preparations, expresses slightly
lower, yet comparable, endotoxic activity in biologic test systems [25, 29, 32]. C. jejuni LPS and lipid A exhibit higher
phase-transition temperatures than those of Salmonella preparations, and thus the former have lower fluidity at 377C [29].
This lower fluidity of acyl chains may influence the biologic
activities of C. jejuni LPS, but the acyl chain characteristics
and the replacement of GlcN by GlcN3N may also influence the
supramolecular structure of C. jejuni lipid A, thereby affecting
biologic activities.
Emphasizing the specificity of lipid A structure to each bacterial species (and in contrast to C. jejuni), Campylobacter fetus
LPS contains GlcN but not GlcN3N and has a different fatty
acid composition [33].
Core OS
General structure. The core OS of enterobacterial LPS
consists of a hetero-OS that can be formally subdivided into
the outer core region proximal to the O-specific chain and the
lipid A proximal inner core region [1, 3, 5] (figure 1). This
subdivision was originally devised because of the different
composition of both regions (i.e., hexoses and hexosamines in
the outer core and the unusual sugars, heptose and, notably, 3deoxy-D-manno-2-octulosonic acid [Kdo], in the inner core).
Within a bacterial species, chemical variation in the structures
of the core OS is greater than that in lipid A but is more limited
than in the structures of the O-chain [34]. Thus, in E. coli five
core types (R1 – R4 and K12) have been described for ú100
serotypes [1, 34]. Structural differences between these core
types are mainly recognized in the outer core region.
LPSs of the Enterobacteriaceae and most other bacteria studied (including those that lack the O-specific chain) contain
heptose, mainly in the L-glycero-D-manno- (L,D-Hep) but occasionally in the D-glycero-D-manno- (D,D-Hep) configuration
[34]. Despite these variations, all LPSs, independent of bacterial origin, contain at least one Kdo residue (or derivative
thereof) that serves as a link between the core OS and the lipid
A component [1, 3, 5]. A typical structural element of the core
region of enterobacterial LPS is the tetrasaccharide Glc-a(1,3)L,D-Hep-a(1,3)-L,D-Hep-a(1,5)-Kdo, whereas the smaller trisaccharide L,D-Hep-a(1,3)-L,D-Hep-a(1,5)-Kdo is present in
LPS of various bacteria [34].
Shared structures in the inner core. Compositional analyses of LPSs from a variety of C. jejuni strains revealed the
presence of D-glucose, D-galactose, N-acetyl-D-galactosamine,
N-acetyl-D-glucosamine, L,D-Hep, and Kdo, which are sugar
constituents commonly encountered in the core regions of LPSs
[24 – 27]. More detailed analyses also showed that D-glucuronic
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Figure 4. Molecular mimicry of saccharide moieties of gangliosides by core oligosaccharides of Campylobacter jejuni serostrains
O:1 (A), O:4 (B), O:19 (C), and O:23 and O:36 (D) [15, 36]. PEA,
O-phosphoethanolamine; Kdo, 3-deoxy-D-manno-2-octulosonic acid;
LDHep, L-glycero-D-manno-heptose; Glc, D-glucose; Gal, D-galactose; GalNAc, N-acetyl-D-galactosamine; Neu5Ac, N-acetylneuraminic acid.
acid and N-acetylneuraminic (sialic) acid (Neu5Ac), an acidic
sugar related to Kdo, had been overlooked as constituents in
the earlier studies and were associated with the core region of
C. jejuni LPS [28, 29, 32].
The structure of the core OSs of LPS belonging to 8 C.
jejuni serotypes (O:1, O:2, O:3, O:4, O:10, O:19, O:23, and
O:36) have been examined [15 – 18, 35 – 38] (figures 4, 5). Although discrepancies existed in the reported structures of the
heptose region of O:19 core OS [35, 36], these were resolved
in a later study [37]. All of the core OSs contain the trisaccharide L,D-Hep-a(1,3)-L,D-Hep-a(1,5)-Kdo (see above) in their
inner core. A further common feature of these core OSs is that
the heptose adjacent to Kdo is substituted by D-glucose in b(1 –
4) linkage, hence producing a common tetrasaccharide in C.
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Structure of C. jejuni LPS
Figure 5. Structures of core oligosaccharides of Campylobacter jejuni serostrains O:2 (A) and O:3 (B) [16, 17]. P, O-phosphoryl group;
PEA, O-phosphoethanolamine; Kdo, 3-deoxy-D-manno-2-octulosonic
acid; LDHep, L-glycero-D-manno-heptose; Glc, D-glucose; Gal, Dgalactose; GalNAc, N-acetyl-D-galactosamine; GlcNAc, N-acetyl-Dglucosamine; QuiNAc, N-acetyl-D-quniovosamine; Neu5Ac, N-acetylneuraminic acid.
jejuni LPS. Two core OSs (O:23 and O:36) contain the tetrasaccharide Glc-a(1,2)-L,D-Hep-a(1,3)-L,D-Hep-a(1,5)-Kdo (figure 4D), which resembles the tetrasaccharide in enterobacterial
LPS, Glc-a(1,3)-L,D-Hep-a(1,3)-L,D-Hep-a(1,5)-Kdo; the remaining serostrains contain the tetrasaccharide Gal-a(1,3)-L,DHep-a(1,3)-L,D-Hep-a(1,5)-Kdo, in which D-galactose replaces D-glucose (figures 4A – C, 5A – B).
Detailed structural studies based on chemical methods have
been unable to assign glucuronic acid as a constituent of the
core OS of C. jejuni serostrains [15 – 18, 36]. However, this
sugar is liberated with Kdo upon mild acidic hydrolysis of C.
jejuni LPS [29], and similar conditions are used to liberate OSs
from LPS for structural studies, thereby possibly explaining
the difficulties encountered in assigning this sugar as a constituent of C. jejuni core OS.
Mimicry of gangliosides by C. jejuni. Neu5Ac is present
in the outer core region of C. jejuni LPS [7, 18], as it is in the
core OSs of low-Mr LPS of gonococci and meningococci. Some
of the core OSs of low-Mr LPS of gonococci and meningococci
have been shown to mimic glycosphingolipids on human cells
[7]. Likewise, antibody cross-reactions between sialylated GM1
ganglioside and LPS of C. jejuni O:19, commonly associated
with antecedent infection in Guillain-Barré syndrome (GBS)
patients [18], suggested the presence of molecular mimicry in
this LPS [39]. Structural analyses showed that the outer core
of C. jejuni O:19 LPSs, including those from GBS-associated
isolates, contain terminal tetra- and pentasaccharide moieties
identical to those of GM1 and GD1a gangliosides, respectively
(figure 4C) [35 – 37].
In addition to molecular mimicry of GM1 , mimicry of GT1a
and GD3 gangliosides by the terminal hexasaccharides and tri-
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saccharides, respectively, of LPS of some GBS-associated C.
jejuni O:19 isolates was observed [36]. Mimicry of GD3 ganglioside was demonstrated also in the outer core of a C. jejuni
O:10 isolate from a patient with Miller Fisher syndrome [38].
The presence of GT1a- and GD3-like epitopes in the latter O:19
LPS has been confirmed serologically [40]. The terminal pentasaccharide of the outer core of C. jejuni serostrain O:4, another
serotype associated with the development of GBS [18], also
mimics that of GD1a ganglioside [15]. As would be expected,
both GM1- and GD1a-like epitopes are present in this LPS [41].
In addition, other types of ganglioside mimicry occur in C.
jejuni serostrains. The outer core of C. jejuni serostrains O:1,
O:23, and O:36 exhibit mimicry of GM2 ganglioside [15]. The
terminii of the core OSs of C. jejuni O:23 and O:36 LPSs are
composed of the same tetrasaccharide as that present in GM2
ganglioside (figure 4D). However, mimicry of GM2 ganglioside
is limited to a terminal trisaccharide in the core OS of C. jejuni
O:1 (figure 4A).
Although C. jejuni serotype O:2 strains are associated with
the development of GBS [18], mimicry of gangliosides is limited to that of a terminal disaccharide (Neu5Aca2-3Gal) in the
core OS of the serostrain [16] (figure 5A). Nevertheless, this
disaccharide is present as the OS moiety in GM4 ganglioside,
and it is also present as the terminal disaccharide in other
gangliosides (e.g., GD1a , GT1b , and GM3). Moreover, antiasialo GM1 antibody can bind both O:2 and O:19 LPSs, indicating a shared epitope not dependent on ganglioside mimicry
[42] but which may be implicated in the induction of GBS by
these strains [18].
Despite this phenomenon of mimicry of gangliosides by the
outer core of some C. jejuni strains, LPSs of all C. jejuni strains
are not sialylated. The LPS of C. jejuni O:3 is not sialylated
[28, 29], the core OS does not exhibit any mimicry of gangliosides [17], and of interest, this serotype has not been associated
with antecedent infection in GBS patients. Moreover, O:3 LPS
has been used as a negative control in experiments with antiganglioside antibodies [42]. Thus, although ganglioside mimicry is a common feature shared by a number of C. jejuni
serotypes, this mimicry is not conserved in all serotypes.
Conclusions
C. jejuni strains possess a lipid A moiety that contains a
hybrid backbone of a phosphorylated b(1*-6)-linked GlcN3NGlcN disaccharide as the major molecular species. Despite
this backbone, which differs structurally from that of classic
enterobacterial lipid A, C. jejuni lipid A is antigenically similar
to enterobacterial lipid As, and the endotoxic activities of its
LPS are comparable with those of enterobacterial LPSs. Furthermore, the inner core OSs of C. jejuni strains share a common unique tetrasaccharide but also possess a trisaccharide
present in the inner core of other bacterial species. Thus, depending on epitope recognition, it may prove possible to obtain
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antibodies reacting with C. jejuni LPS alone, which would be
of potential use in diagnosis, or cross-reacting with LPSs of
C. jejuni and other bacteria, which would be of potential therapeutic use in endotoxemia. Finally, the outer core of some C.
jejuni strains mimics gangliosides in structure, and this may
play an important role in the induction of autoantibodies in
GBS following C. jejuni infection.
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