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The effect of O-antigen length determinant wzz on the immunogenicity of Salmonella Typhimurium for Escherichia coli O2 O-polysaccharides delivery

Attenuated Salmonella Typhimurium is a promising antigen delivery system for live vaccines such as polysaccharides. The length of polysaccharides is a well-known key factor in modulating the immune response induced by glycoconjugates. However, the relationship between the length of Lipopolysaccharid...

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Autores principales: Han, Yue, Luo, Ping, Zeng, Huan, Wang, Pu, Xu, Jiali, Chen, Pengju, Chen, Xindan, Chen, Yuji, Cao, Qiyu, Zhai, Ruidong, Xia, Jing, Deng, Simin, Cheng, Anchun, Cheng, Changyong, Song, Houhui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9969949/
https://www.ncbi.nlm.nih.gov/pubmed/36849993
http://dx.doi.org/10.1186/s13567-023-01142-4
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author Han, Yue
Luo, Ping
Zeng, Huan
Wang, Pu
Xu, Jiali
Chen, Pengju
Chen, Xindan
Chen, Yuji
Cao, Qiyu
Zhai, Ruidong
Xia, Jing
Deng, Simin
Cheng, Anchun
Cheng, Changyong
Song, Houhui
author_facet Han, Yue
Luo, Ping
Zeng, Huan
Wang, Pu
Xu, Jiali
Chen, Pengju
Chen, Xindan
Chen, Yuji
Cao, Qiyu
Zhai, Ruidong
Xia, Jing
Deng, Simin
Cheng, Anchun
Cheng, Changyong
Song, Houhui
author_sort Han, Yue
collection PubMed
description Attenuated Salmonella Typhimurium is a promising antigen delivery system for live vaccines such as polysaccharides. The length of polysaccharides is a well-known key factor in modulating the immune response induced by glycoconjugates. However, the relationship between the length of Lipopolysaccharide (LPS) O-antigen (OAg) and the immunogenicity of S. Typhimurium remains unclear. In this study, we assessed the effect of OAg length determined by wzz(ST) on Salmonella colonization, cell membrane permeability, antimicrobial activity, and immunogenicity by comparing the S. Typhimurium wild-type ATCC14028 strain to those with various OAg lengths of the Δwzz(ST) mutant and Δwzz(ST)::wzz(ECO2). The analysis of the OAg length distribution revealed that, except for the very long OAg, the short OAg length of 2–7 repeat units (RUs) was obtained from the Δwzz(ST) mutant, the intermediate OAg length of 13–21 RUs was gained from Δwzz(ST)::wzz(ECO2), and the long OAg length of over 20 RUs was gained from the wild-type. In addition, we found that the OAg length affected Salmonella colonization, cell permeability, and antibiotic resistance. Immunization of mice revealed that shortening the OAg length by altering wzz(ST) had an effect on serum bactericidal ability, complement deposition, and humoral immune response. S. Typhimurium mutant strain Δwzz(ST)::wzz(ECO2) possessed good immunogenicity and was the optimum option for delivering E. coli O2 O-polysaccharides. Furthermore, the attenuated strain ATCC14028 ΔasdΔcrpΔcyaΔrfbPΔwzz(ST)::wzz(ECO2)-delivered E. coli O2 OAg gene cluster outperforms the ATCC14028 ΔasdΔcrpΔcyaΔrfbP in terms of IgG eliciting, cytokine expression, and immune protection in chickens. This study sheds light on the role of OAg length in Salmonella characteristics, which may have a potential application in optimizing the efficacy of delivered polysaccharide vaccines. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13567-023-01142-4.
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spelling pubmed-99699492023-02-28 The effect of O-antigen length determinant wzz on the immunogenicity of Salmonella Typhimurium for Escherichia coli O2 O-polysaccharides delivery Han, Yue Luo, Ping Zeng, Huan Wang, Pu Xu, Jiali Chen, Pengju Chen, Xindan Chen, Yuji Cao, Qiyu Zhai, Ruidong Xia, Jing Deng, Simin Cheng, Anchun Cheng, Changyong Song, Houhui Vet Res Research Article Attenuated Salmonella Typhimurium is a promising antigen delivery system for live vaccines such as polysaccharides. The length of polysaccharides is a well-known key factor in modulating the immune response induced by glycoconjugates. However, the relationship between the length of Lipopolysaccharide (LPS) O-antigen (OAg) and the immunogenicity of S. Typhimurium remains unclear. In this study, we assessed the effect of OAg length determined by wzz(ST) on Salmonella colonization, cell membrane permeability, antimicrobial activity, and immunogenicity by comparing the S. Typhimurium wild-type ATCC14028 strain to those with various OAg lengths of the Δwzz(ST) mutant and Δwzz(ST)::wzz(ECO2). The analysis of the OAg length distribution revealed that, except for the very long OAg, the short OAg length of 2–7 repeat units (RUs) was obtained from the Δwzz(ST) mutant, the intermediate OAg length of 13–21 RUs was gained from Δwzz(ST)::wzz(ECO2), and the long OAg length of over 20 RUs was gained from the wild-type. In addition, we found that the OAg length affected Salmonella colonization, cell permeability, and antibiotic resistance. Immunization of mice revealed that shortening the OAg length by altering wzz(ST) had an effect on serum bactericidal ability, complement deposition, and humoral immune response. S. Typhimurium mutant strain Δwzz(ST)::wzz(ECO2) possessed good immunogenicity and was the optimum option for delivering E. coli O2 O-polysaccharides. Furthermore, the attenuated strain ATCC14028 ΔasdΔcrpΔcyaΔrfbPΔwzz(ST)::wzz(ECO2)-delivered E. coli O2 OAg gene cluster outperforms the ATCC14028 ΔasdΔcrpΔcyaΔrfbP in terms of IgG eliciting, cytokine expression, and immune protection in chickens. This study sheds light on the role of OAg length in Salmonella characteristics, which may have a potential application in optimizing the efficacy of delivered polysaccharide vaccines. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13567-023-01142-4. BioMed Central 2023-02-27 2023 /pmc/articles/PMC9969949/ /pubmed/36849993 http://dx.doi.org/10.1186/s13567-023-01142-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Han, Yue
Luo, Ping
Zeng, Huan
Wang, Pu
Xu, Jiali
Chen, Pengju
Chen, Xindan
Chen, Yuji
Cao, Qiyu
Zhai, Ruidong
Xia, Jing
Deng, Simin
Cheng, Anchun
Cheng, Changyong
Song, Houhui
The effect of O-antigen length determinant wzz on the immunogenicity of Salmonella Typhimurium for Escherichia coli O2 O-polysaccharides delivery
title The effect of O-antigen length determinant wzz on the immunogenicity of Salmonella Typhimurium for Escherichia coli O2 O-polysaccharides delivery
title_full The effect of O-antigen length determinant wzz on the immunogenicity of Salmonella Typhimurium for Escherichia coli O2 O-polysaccharides delivery
title_fullStr The effect of O-antigen length determinant wzz on the immunogenicity of Salmonella Typhimurium for Escherichia coli O2 O-polysaccharides delivery
title_full_unstemmed The effect of O-antigen length determinant wzz on the immunogenicity of Salmonella Typhimurium for Escherichia coli O2 O-polysaccharides delivery
title_short The effect of O-antigen length determinant wzz on the immunogenicity of Salmonella Typhimurium for Escherichia coli O2 O-polysaccharides delivery
title_sort effect of o-antigen length determinant wzz on the immunogenicity of salmonella typhimurium for escherichia coli o2 o-polysaccharides delivery
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9969949/
https://www.ncbi.nlm.nih.gov/pubmed/36849993
http://dx.doi.org/10.1186/s13567-023-01142-4
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