First Evidence for a Covalent Linkage between Enterobacterial Common Antigen and Lipopolysaccharide in Shigella sonnei Phase II ECALPS

Gozdziewicz, Tomasz K.; Ługowski, Czesław; Łukasiewicz, Jolanta

doi:10.1074/jbc.m113.512749

Cited by 27 publications

(34 citation statements)

References 46 publications

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“…Since repeating units of both polymers are assembled on the same lipid carrier—undecaprenyl pyrophosphate (Und-PP)—and undergone similar processing [ 25 ], key features of ECA LPS structures are predicted partially on the basis of biosynthesis pathway analyses: (i) ECA LPS can only be observed in strains incapable of producing the O-PS [ 3 , 25 ]; (ii) ECA is ligated to the core OS in the position used to be occupied by O-PS, and (iii) an inverted anomeric configuration of the D-Glc p NAc residue in the first ECA repeating unit linked to the core OS has to be observed, whereas an α-configuration is a characteristic for polymeric chain ( Figure 1 ) [ 3 ]. All these presumptions were positively verified by our single case study on S. sonnei phase II ECA LPS [ 7 , 8 ].…”

Section: Introductionmentioning

confidence: 52%

“…Even though the existence and immunogenicity of ECA LPS were suggested in the 1960s by Kunin et al [ 5 , 6 ], it was relatively recent studies that demonstrated the first example of the covalent linkage between ECA and LPS in rough Shigella sonnei phase II [ 7 , 8 ]. Rough form of S. sonnei LPS, lipooligosaccharide (LOS) devoid of the O-PS, was partially substituted by ECA at the position occupied by the O-PS in the case of smooth S. sonnei phase I.…”

Section: Introductionmentioning

confidence: 99%

“…Rough form of S. sonnei LPS, lipooligosaccharide (LOS) devoid of the O-PS, was partially substituted by ECA at the position occupied by the O-PS in the case of smooth S. sonnei phase I. Specifically, the distal β- d -Glc p residue in the outer core region of the chemotype R1 was substituted at position 3 by ECA [ 7 , 8 ] ( Figure 1 ).…”

Section: Introductionmentioning

confidence: 99%

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Lipopolysaccharide-Linked Enterobacterial Common Antigen (ECALPS) Occurs in Rough Strains of Escherichia coli R1, R2, and R4

Maciejewska

Kaszowska

Jachymek

et al. 2020

IJMS

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Enterobacterial common antigen (ECA) is a conserved surface antigen characteristic for Enterobacteriaceae. It is consisting of trisaccharide repeating unit, →3)-α-d-Fucp4NAc-(1→4)-β-d-ManpNAcA-(1→4)-α-d-GlcpNAc-(1→, where prevailing forms include ECA linked to phosphatidylglycerol (ECAPG) and cyclic ECA (ECACYC). Lipopolysaccharide (LPS)-associated form (ECALPS) has been proved to date only for rough Shigella sonnei phase II. Depending on the structure organization, ECA constitutes surface antigen (ECAPG and ECALPS) or maintains the outer membrane permeability barrier (ECACYC). The existence of LPS was hypothesized in the 1960–80s on the basis of serological observations. Only a few Escherichia coli strains (i.e., R1, R2, R3, R4, and K-12) have led to the generation of anti-ECA antibodies upon immunization, excluding ECAPG as an immunogen and conjecturing ECALPS as the only immunogenic form. Here, we presented a structural survey of ECALPS in E. coli R1, R2, R3, and R4 to correlate previous serological observations with the presence of ECALPS. The low yields of ECALPS were identified in the R1, R2, and R4 strains, where ECA occupied outer core residues of LPS that used to be substituted by O-specific polysaccharide in the case of smooth LPS. Previously published observations and hypotheses regarding the immunogenicity and biosynthesis of ECALPS were discussed and correlated with presented herein structural data.

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Section: Introductionmentioning

confidence: 52%

Section: Introductionmentioning

confidence: 99%

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Lipopolysaccharide-Linked Enterobacterial Common Antigen (ECALPS) Occurs in Rough Strains of Escherichia coli R1, R2, and R4

Maciejewska

Kaszowska

Jachymek

et al. 2020

IJMS

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“…Based on this finding, we presume that Wzz fepE has a novel role during L-OAg biosynthesis in the absence of VisP via cross-complementation. Recently, enterobacterial common antigen (ECA) was first characterized in Shigella sonnei as linked to LPS (more specifically, to lipid A) anchored to the OM (108). Therefore, the L-OAg modality observed here in the absence of Wzz ST in the ΔvisP wzz ST strain may be ECA LPS chains with similar lengths of L-OAg.…”

Section: Discussionmentioning

confidence: 79%

Novel Role of VisP and the Wzz System during O-Antigen Assembly in Salmonella enterica Serovar Typhimurium Pathogenesis

et al. 2018

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serovars are associated with diarrhea and gastroenteritis and are a helpful model for understanding host-pathogen mechanisms. serovar Typhimurium regulates the distribution of O antigen (OAg) and presents a trimodal distribution based on Wzy polymerase and the Wzz (long-chain-length OAg [L-OAg]) and Wzz (very-long-chain-length OAg [VL-OAg]) copolymerases; however, several mechanisms regulating this process remain unclear. Here, we report that LPS modifications modulate the infectious process and that OAg chain length determination plays an essential role during infection. An increase in VL-OAg is dependent on Wzy polymerase, which is promoted by a growth condition resembling the environment of -containing vacuoles (SCVs). The virulence- and stress-related periplasmic protein (VisP) participates in OAg synthesis, as a Δ mutant presents a semirough OAg phenotype. The Δ mutant has greatly decreased motility and J774 macrophage survival in a colitis model of infection. Interestingly, the phenotype is restored after mutation of the or gene in a Δ background. Loss of both the and genes promotes an imbalance in flagellin secretion. L-OAg may function as a shield against host immune systems in the beginning of an infectious process, and VL-OAg protects bacteria during SCV maturation and facilitates intramacrophage replication. Taken together, these data highlight the roles of OAg length in generating phenotypes during Typhimurium pathogenesis and show the periplasmic protein VisP as a novel protein in the OAg biosynthesis pathway.

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“…It consists of linear repetitive units of a trisaccharide composed of 4-acetamide-4,6-dideoxy-D-galactose (Fuc4NAc), N-acetyl-D-mannosaminuronic acid (ManNAcA), and N-acetyl-D-glucosamine (GlcNAc). It is considered the second dominant immunogen, ranked next to the lipopolysaccharide (LPS) O-antigen [3,5,6]. Three ECA variants, ECA PG , ECA LPS and ECA CYC , have been described since it was rst found in E. coli [3].…”

Section: Introductionmentioning

confidence: 99%

Effect of Deletion of Gene Cluster involved in Synthesis of Enterobacterial Common Antigen on Virulence and Immunogenicity of Live Attenuated Salmonella Vaccine when Delivering Heterologous Streptococcus pneumoniae Antigen PspA

Liu

Shen

Bian

et al. 2020

Preprint

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Background: Enterobacterial common antigen (ECA) is a family-specific surface antigen shared by all members of the Enterobacteriaceae family. Previous studies showed that the loss of ECA results in Salmonella attenuation, indicating its usefulness as a vaccine candidate for Salmonella infection, but no studies have shown whether the mutation resulting from the deletion of the ECA operon in conjunction with other mutations could be used as an antigen vehicle for heterologous protein antigen delivery.Results: In this study, we introduced a nonpolar, defined ECA operon deletion into wild-type S. Typhimurium χ3761 and an attenuated vaccine strain χ9241, obtaining two isogenic ECA operon mutants, namely, χ12357 and χ12358, respectively. A number of in vitro and in vivo properties of the mutants were analyzed. We found that the loss of ECA did not affect the growth, lipopolysaccharide (LPS) production and motility of S. Typhimurium wild type strain χ3761 and its attenuated vaccine strain χ9241 but significantly affected the virulence when administered orally to BALB/c mice. Furthermore, the effects of the ECA mutation on the immunogenicity of a recombinant S. Typhimurium vaccine strain χ9241 when delivering the pneumococcal antigen PspA were determined. The result showed that the total anti-PspA IgG level of χ12358 (pYA4088) was slightly lower than that of χ9241 (pYA4088), but the protection rate was not compromised.Conclusions: ECA affects virulence and benefits the Th2 immunity of Salmonella Typhimurium, therefore, it is feasible to use a reversible ECA mutant mode to design future Salmonella vaccine strains for heterologous protective antigens.

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First Evidence for a Covalent Linkage between Enterobacterial Common Antigen and Lipopolysaccharide in Shigella sonnei Phase II ECALPS

Cited by 27 publications

References 46 publications

Lipopolysaccharide-Linked Enterobacterial Common Antigen (ECALPS) Occurs in Rough Strains of Escherichia coli R1, R2, and R4

Lipopolysaccharide-Linked Enterobacterial Common Antigen (ECALPS) Occurs in Rough Strains of Escherichia coli R1, R2, and R4

Novel Role of VisP and the Wzz System during O-Antigen Assembly in Salmonella enterica Serovar Typhimurium Pathogenesis

Effect of Deletion of Gene Cluster involved in Synthesis of Enterobacterial Common Antigen on Virulence and Immunogenicity of Live Attenuated Salmonella Vaccine when Delivering Heterologous Streptococcus pneumoniae Antigen PspA

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