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Infection and Immunity, September 2002, p. 5299-5303, Vol. 70, No. 9
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.9.5299-5303.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Campylobacter jejuni from Patients with Guillain-Barré Syndrome Preferentially Expresses a GD1a-Like Epitope

Irving Nachamkin,1* Jirong Liu,1 Ming Li,1 Huong Ung,1 Anthony P. Moran,2 Martina M. Prendergast,2 and Kazim Sheikh3

Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-4283,1 Department of Microbiology, National University of Ireland, Galway, Ireland,2 Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, Maryland 212873

Received 12 March 2002/ Returned for modification 14 May 2002/ Accepted 14 June 2002


   ABSTRACT
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GM1- and GD1a-like ganglioside mimicry in Campylobacter jejuni lipooligosaccharide (LOS) is considered to be involved in the pathogenesis of Campylobacter-induced Guillain-Barré syndrome (GBS). Compared with gastroenteritis-related isolates, GBS-related C. jejuni isolates were strongly associated with the expression of GD1a-like mimicry. The presence of a few genes involved in LOS ganglioside mimicry, cst-II, cgtA, and cgtB, was also associated with GBS-related strains. GD1a-like epitope expression may be an important virulence phenotype associated with the risk of developing GBS following campylobacter infection.


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Guillain-Barré syndrome (GBS) is an acute, immune-mediated, postinfection disorder affecting the peripheral nervous system and is strongly associated with Campylobacter jejuni gastrointestinal (GI) infection (13). Expression of ganglioside-like mimicry in the outer core lipooligosaccharide (LOS) and development of an immune response in the host that cross-reacts with ganglioside-rich targets in the peripheral nerve are considered to be involved in the pathogenesis of Campylobacter-induced GBS (21). Anti-GD1a antibodies are associated with the axonal (acute motor axonal neuropathy [AMAN]) form of GBS, whereas anti-GM1 antibodies are seen in both AMAN and demyelinating (acute inflammatory demyelinating polyneuropathy [AIDP]) forms (12). Both AIDP and AMAN are associated with C. jejuni infection; however, patients with GBS following Campylobacter infection may be more likely to have axonal neuropathy (11, 12, 26, 28).

To determine whether GD1a-like mimicry is specifically expressed in C. jejuni from patients with GBS, we analyzed a collection of isolates from GBS and enteritis (GI infection) patients for expression of both GD1a- and GM1-like mimicry.

(This work was presented in part at the 11th International Workshop on Campylobacter, Helicobacter and Related Organisms, Freiburg, Germany, 1 to 5 September 2001.)

Isolates listed in Table 1 were collected from a variety of worldwide sources and were previously studied by multilocus enzyme electrophoresis and for GM1-like mimicry (5, 23). The isolates from GBS patients are likely to represent both AMAN and AIDP forms of GBS. However, information on the type of GBS was available from only a limited number of patients and is noted in Table 1.


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  		TABLE 1. Isolates studied for GM1- and GD1a-like expression

 
GM1-like and GD1a-like mimicries were determined using a dot blot assay that was validated for the detection of GM1-like mimicry, as described previously (24). GM1-like mimicry was detected using cholera toxin subunit B, which was labeled with horseradish peroxidase (Sigma, St. Louis, Mo.) and used at a concentration of 0.105 µg/ml. The GD1a-like epitope was detected using an anti-GD1a monoclonal antibody (clone, Gg101; isotype, immunoglobulin G1) produced in knockout mice defective in the production of endogenous complex gangliosides and characterized previously by Lunn et al. (17). Purified antibody was labeled with horseradish peroxidase as described by McIlhinney et al. (18) and used at a concentration of 0.035 µg/ml. The GD1a binding assay was validated using control strains of known ganglioside mimicry, and binding assays using 12 different blots of each reference strain were used to calculate confidence intervals (CI). There was clear separation of binding between C. jejuni HS:3 (ATCC 43431), which does not mimic gangliosides, and the serotype reference strain (serostrain) HS:19 (ATCC 43446), which exhibits both GM1- and GD1a-like mimicry (24). The range of binding for the HS:19 reference strain was 192 to 235 U, whereas HS:3 had an upper 99% CI of 71 U. Serostrains HS:36 (ATCC 43456) and HS:1 (ATCC 43429) express GM2 mimicry, with an upper 99% CI of 125 U. Escherichia coli (ATCC 35218) and Salmonella enterica serovar Typhimurium X4550 (provided by R. Curtiss, Washington University, St. Louis, Mo.) as negative controls showed a binding value of <20 U. Strains with binding values above 125 U were considered positive for the GD1a epitope. The antibody was also strongly reactive against serostrain HS:4, which contains a 9:1 ratio of molecules bearing GD1a to molecules bearing GM1 in thin-layer chromatography (1). Fisher's exact test or the chi-square test (Yates' correction) was used to compare the differences between proportions (EpiInfo 2000, verion 1.1.2; Centers for Disease Control and Prevention, Atlanta, Ga.).

When isolates were analyzed for the expression of GM1-like mimicry, there was no difference between GI and GBS isolates or between HS:19 and non-HS:19 serotypes (P = 0.85) (Table 2). Compared to GI isolates, GBS-associated isolates were significantly more likely to express a GD1a-like epitope (78.6 versus 19.8%; P < 0.0000001; OR, 14.90; CI, 4.69 to 49.71). When isolates were analyzed according to serotype, HS:19 isolates from GBS patients (n = 17) were associated with GD1a expression significantly more often than GI infection-associated HS:19 isolates (88.2 versus 30.6%; P = 0.0003; OR, 17.05; CI, 2.89 to 130.72). For isolates of serotypes other than HS:19, GBS-associated isolates (n = 11) were also associated with GD1a expression significantly more often than GI serotypes (63.6 versus 11.1%; P = 0.0008; OR, 14.00; CI, 2.44 to 91.03).


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  		TABLE 2. Distribution of GD1a- and GM1-like mimicry in GBS- and GI-related isolates of C. jejuni

 
Also, we examined whether GD1a-like expression was independent of GM1-like mimicry. Eight of 28 GBS (28.6%) isolates and 11 of 81 GI (13.6%) isolates expressed both GM1- and GD1a-like structures, results that are not statistically different (P = 0.130; OR, 2.55; CI, 0.8 to 8.07). Expression of only GM1-like mimicry was not associated with either GBS (14.3%) or GI isolates (29.6%) (P = 0.176; OR, 0.40; CI, 0.1 to 1.39). However, expression of only GD1a was strongly associated with GBS-related isolates (50.0% for GBS isolates versus 6.2% for GI isolates; P = 0.00001; OR, 15.2; CI, 4.2 to 58.57). Expression of only GD1a was independent of serotype and was significantly associated with GBS-related HS:19 isolates (52.9% for GBS isolates versus 11.1% for GI isolates; P = 0.0018; OR, 9.00; CI, 1.85 to 47.95) and non-HS:19 serotypes (45.4% for GBS isolates versus 2.2% for GI isolates; P = 0.0006; OR, 36.67; CI, 3.1 to 996.5).

Using PCR, we examined the presence of core LOS genes, cgtA, cgtB, and cst-II, associated with ganglioside mimicry in GBS- and GI infection-related C. jejuni isolates. Primer sets for each of the genes were developed based on previously published sequences (6, 15). The primers for cgtA were CgtAUp (5'ATA CGG GAG GGG CAT AAA G3') and CgtADn (5'ATA AGC AAG CAA TCT CCT GGT T3') (527 bp). The cgtB primers were CgtBUp (5'AGA GCA AGA TAT GAA GGT GTG AA3') and CgtBDn (5'AAA CCA ACT GCA ACT CTT GAA T3') (502 bp). Two primer sets were used to detect cstII based on the HS:2 (NCTC11168) and HS:19 (OH4384) sequences reported by Gilbert et al. (6). The primers used for cstII from HS:19 were Cst-IIUp (5'GTT ATT ATT GCT GGA AAT GGA CCA AGT 3') and Cst-IIDn (5' ACA TAT AGA CCC CTG AGG TAA TTC TTT GAT3') (400 bp), and the primers used for HS:2 were Cst-IIUp (5'TTG GTA TGC GGT AAT GGA CCT A3') and Cst-IIDn (5'CAG AGC CAC AGC TGT AGC ACA 3') (417 bp). Amplification using either cstII primer was indicative of the presence of the cstII gene. As a control for each bacterial DNA preparation, waaC, a conserved heptosyltransferase gene involved in LOS biosynthesis, was also amplified.

The presence of the three genes cst-II, cgtA, and cgtB was strongly associated with GBS-related isolates, unlike with GI isolates (82.1 versus 45.7%; P = 0.001; OR, 5.47; CI, 1.74 to 18.34). There was no difference between GBS- and GI infection-related HS:19 isolates, as 98.1% of all HS:19 isolates contained these genes. However, GBS-related non-HS:19 isolates were more likely to contain these genes (54.5%) than were GI infection-related non-HS:19 isolates (2.2%) (P = 0.001).

The role of ganglioside-like mimicry in eliciting pathogenic host immune responses is not fully understood, but patients with GBS are more likely to mount a host response to these mimics than are patients with GI disease only (29, 33). C. jejuni strains have been shown to exhibit various types of ganglioside mimicry, including expression of GM1-, GM2-, GM3-, GD1a-, GD1b, GD2-, GD3-, and GT1a-like structures (20). In the present study, we examined both GM1- and GD1a-like expression in GBS- and GI infection-associated C. jejuni isolates that were collected from all over the world. GM1-like mimicry was found not to be specific to isolates from either group of patients, which is consistent with our previous findings on the distribution of GM1 mimicry in U.S. diarrheal isolates (24). Likewise, a detailed structural analysis of C. jejuni HS:19 isolates associated with GBS or GI infection showed that both could express GM1 mimicry (19). Other studies have examined small numbers of isolates for the presence of ganglioside-type mimicry (25, 27, 31, 32, 36, 37); however, none have adequately assessed differences among GBS- and diarrhea-related strains.

Anti-GD1a antibodies are highly associated with the AMAN form of GBS and are usually not generally produced in patients with AIDP (2, 12, 39). Other antibodies, including anti-GalNAc-GD1a and anti-GD1b antibodies, have also been found to be associated with AMAN development (26). Using a specific monoclonal antibody directed against GD1a, we showed that expression of GD1a-like mimicry was strongly associated with GBS-related isolates. Moreover, GBS-related isolates of the HS:19 serotype and non-HS:19 serotypes were significantly more likely to express the GD1a-like epitope than were GI infection-related isolates. The association of GD1a expression with GBS-related isolates was independent of GM1-type mimicry. Various C. jejuni HS serotypes have been isolated from patients with GBS, and some studies suggest that serotype HS:19 is overrepresented among patients with GBS in certain geographic locations but not in others (22). These findings suggest that expression of GD1a may be a serotype-independent property linked to the ability of C. jejuni to induce pathogenic antibodies in susceptible hosts.

There may also be quantitative differences in the amounts of GD1a expressed, as suggested by the observation that the HS:4 serotype expresses a 9:1 ratio of GD1a moieties to GM1 moieties, compared to a 1:1 ratio for the HS:19 serostrain (1). The expression of GD1a-like mimicry in GBS-related isolates does not rule out the possibility that other types of mimicry may be involved in the pathogenesis of Campylobacter-induced GBS. In preliminary studies using previously described techniques (27), thin-layer chromatography immunostaining of several isolates with anti-GD1a binding in the intermediate range suggest that GD1b-like mimicry may also be present (data not shown and reference 24).

While a GD1a-like epitope was preferentially expressed in GBS-related isolates, some GI infection-related isolates expressed this epitope as well. The presence of this epitope, therefore, is not alone responsible for causing GBS. Host genetic susceptibility to developing GBS following exposure to a strain with this virulence phenotype is likely to be a critical factor (30, 35).

The genetic basis for ganglioside-type mimicry has been studied only recently, and it is clear that the mechanisms for producing ganglioside-like structures in LOS are complex and undergo phase variation (7, 9, 10, 15, 16). We did not study the degree of phase-variable GD1a expression in this study. Nevertheless, it is possible that phase-variable rates of GD1a expression differ between GBS- and GI infection-related isolates. A few genes, cst-II, cgtA, and cgtB, appear to be critical in C. jejuni ganglioside mimicry expression (7, 9,10, 15, 16). In particular, cst-II ({alpha}-2,3 and/or {alpha}-2,3/{alpha}-2,8 sialyltransferase) has been shown to be involved in the addition of a terminal sialic acid residue that forms the GD1a epitope (6). The cgtA gene product, ß1,4-N-acetylgalactosyltransferase, and the cgtB gene product, ß1,3-galactosyltransferase, add the substrates for sialylation to the LOS backbone.

We compared GBS- and GI infection-related isolates for the presence of these three genes and found that they were more strongly associated with GBS-related isolates than with uncomplicated GI isolates and that they were highly associated with the HS:19 serotype. The uniform presence of these genes in HS:19 isolates is not totally surprising since this serotype is highly clonal and infection with HS:19 is associated with an increased risk of GBS (22, 23). Of particular interest is the observation by Gilbert et al. (8) that a GBS-related HS:2 isolate was shown to possess the HS:19 LOS gene cluster, suggesting that this gene cluster may confer unique, still to be completely defined, virulence properties involved in GBS pathogenesis.

Molecular analysis of C. jejuni isolates from GBS and GI patients has been unable to differentiate between GI infection-related and GBS-related isolates (3-5, 23). The cst-II gene was found previously to be associated with a small number of GBS-related strains by van Belkum et al. (34). In contrast, the present study clearly identified a phenotype strongly associated with GBS-related isolates. The lack of relevant animal models has hampered studies of the role of ganglioside-like mimicry in inducing GBS; however, the recent description of the development of nerve pathology in rabbits immunized with gangliosides may be applicable to studies of Campylobacter in the near future (14, 38).


   ACKNOWLEDGMENTS
 
This study was supported in part by grants from the National Institutes of Health (grant NS31528 to I.N.) and from the Irish Health Research Board (to A.P.M. and M.M.P.).

We especially thank Jorgen Engberg and Eva Moller Nielsen, Danish Veterinary Laboratory, for contributing many of the strains used in the study, as well as other investigators who provided isolates.


   FOOTNOTES
 
* Corresponding author. Mailing address: Department of Pathology & Laboratory Medicine, University of Pennsylvania School of Medicine, 4th Floor, Gates Building, 3400 Spruce St., Philadelphia, PA 19104-4283. Phone: (215) 662-6651. Fax: (215) 662-6655. E-mail: nachamki{at}mail.med.upenn.edu. Back

Editor: J. D. Clements


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Infection and Immunity, September 2002, p. 5299-5303, Vol. 70, No. 9
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.9.5299-5303.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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J. Bacteriol. J. Virol. Eukaryot. Cell
Microbiol. Mol. Biol. Rev. Clin. Vaccine Immunol. All ASM Journals