Yersinia pestis Interacts With SIGNR1 (CD209b) for Promoting Host Dissemination and Infection

Kun Yang; Yingxia He; Chae Gyu Park; Young Sun Kang; Pei Zhang; Yanping Han; Yujun Cui; Silvia Bulgheresi; Andrey P Anisimov; Svetlana V Dentovskaya; Xiaoling Ying; Lingyu Jiang; Honghui Ding; Olivia Adhiambo Njiri; Shusheng Zhang; Guoxing Zheng; Lianxu Xia; Biao Kan; Xin Wang; Huaiqi Jing; Meiying Yan; Wei Li; Yuanzhi Wang; Xiding Xiamu; Gang Chen; Ding Ma; Sara Schesser Bartra; Gregory V Plano; John D Klena; Ruifu Yang; Mikael Skurnik; Tie Chen

doi:10.3389/fimmu.2019.00096

Yersinia pestis Interacts With SIGNR1 (CD209b) for Promoting Host Dissemination and Infection

Kun Yang, Yingxia He, Chae Gyu Park, Young Sun Kang, Pei Zhang, Yanping Han, Yujun Cui, Silvia Bulgheresi, Andrey P Anisimov, Svetlana V Dentovskaya, Xiaoling Ying, Lingyu Jiang, Honghui Ding, Olivia Adhiambo Njiri, Shusheng Zhang, Guoxing Zheng, Lianxu Xia, Biao Kan, Xin Wang, Huaiqi JingMeiying Yan, Wei Li, Yuanzhi Wang, Xiding Xiamu, Gang Chen, Ding Ma, Sara Schesser Bartra, Gregory V Plano, John D Klena, Ruifu Yang, Mikael Skurnik, Tie Chen

Publications: Contribution to journal › Article › Peer Reviewed

Abstract

Yersinia pestis, a Gram-negative bacterium and the etiologic agent of plague, has evolved from Yersinia pseudotuberculosis, a cause of a mild enteric disease. However, the molecular and biological mechanisms of how Y. pseudotuberculosis evolved to such a remarkably virulent pathogen, Y. pestis, are not clear. The ability to initiate a rapid bacterial dissemination is a characteristic hallmark of Y. pestis infection. A distinguishing characteristic between the two Yersinia species is that Y. pseudotuberculosis strains possess an O-antigen of lipopolysaccharide (LPS) while Y. pestis has lost the O-antigen during evolution and therefore exposes its core LPS. In this study, we showed that Y. pestis utilizes its core LPS to interact with SIGNR1 (CD209b), a C-type lectin receptor on antigen presenting cells (APCs), leading to bacterial dissemination to lymph nodes, spleen and liver, and the initiation of a systemic infection. We therefore propose that the loss of O-antigen represents a critical step in the evolution of Y. pseudotuberculosis into Y. pestis in terms of hijacking APCs, promoting bacterial dissemination and causing the plague.

Original language	English
Article number	96
Number of pages	15
Journal	Frontiers in Immunology
Volume	10
DOIs	https://doi.org/10.3389/fimmu.2019.00096
Publication status	Published - 2019

Austrian Fields of Science 2012

106023 Molecular biology

Keywords

CAPSULAR POLYSACCHARIDE
CORE LIPOPOLYSACCHARIDE
DC-SIGN
DENDRITIC CELLS
ESCHERICHIA-COLI
LIPOPOLYSACCHARIDE O-ANTIGEN
MEDIATES UPTAKE
NEISSERIA-GONORRHOEAE
NONINTEGRIN CD209
RFB GENE-CLUSTER
SIGNR1 (CD209b)
Yersinia pestis
antigen presenting cells (APCs)
bacterial dissemination
core lipopolysaccharide/lipooligosaccharides (core LPS/LOS)
dendritic cells (DCs)
host-pathogen interactions
macrophages
Dendritic cells (DCs)
Bacterial dissemination
Macrophages
Host-pathogen interactions
Antigen presenting cells (APCs)
Core lipopolysaccharide/lipooligosaccharides (core LPS/LOS)

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https://phaidra.univie.ac.at/o:1144838Licence: CC BY 4.0

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Yang, K., He, Y., Park, C. G., Kang, Y. S., Zhang, P., Han, Y., Cui, Y., Bulgheresi, S., Anisimov, A. P., Dentovskaya, S. V., Ying, X., Jiang, L., Ding, H., Njiri, O. A., Zhang, S., Zheng, G., Xia, L., Kan, B., Wang, X., ... Chen, T. (2019). Yersinia pestis Interacts With SIGNR1 (CD209b) for Promoting Host Dissemination and Infection. Frontiers in Immunology, 10, Article 96. https://doi.org/10.3389/fimmu.2019.00096

@article{2c3adf8199864437b3bcf05f56861e0b,

title = "Yersinia pestis Interacts With SIGNR1 (CD209b) for Promoting Host Dissemination and Infection",

abstract = "Yersinia pestis, a Gram-negative bacterium and the etiologic agent of plague, has evolved from Yersinia pseudotuberculosis, a cause of a mild enteric disease. However, the molecular and biological mechanisms of how Y. pseudotuberculosis evolved to such a remarkably virulent pathogen, Y. pestis, are not clear. The ability to initiate a rapid bacterial dissemination is a characteristic hallmark of Y. pestis infection. A distinguishing characteristic between the two Yersinia species is that Y. pseudotuberculosis strains possess an O-antigen of lipopolysaccharide (LPS) while Y. pestis has lost the O-antigen during evolution and therefore exposes its core LPS. In this study, we showed that Y. pestis utilizes its core LPS to interact with SIGNR1 (CD209b), a C-type lectin receptor on antigen presenting cells (APCs), leading to bacterial dissemination to lymph nodes, spleen and liver, and the initiation of a systemic infection. We therefore propose that the loss of O-antigen represents a critical step in the evolution of Y. pseudotuberculosis into Y. pestis in terms of hijacking APCs, promoting bacterial dissemination and causing the plague.",

keywords = "CAPSULAR POLYSACCHARIDE, CORE LIPOPOLYSACCHARIDE, DC-SIGN, DENDRITIC CELLS, ESCHERICHIA-COLI, LIPOPOLYSACCHARIDE O-ANTIGEN, MEDIATES UPTAKE, NEISSERIA-GONORRHOEAE, NONINTEGRIN CD209, RFB GENE-CLUSTER, SIGNR1 (CD209b), Yersinia pestis, antigen presenting cells (APCs), bacterial dissemination, core lipopolysaccharide/lipooligosaccharides (core LPS/LOS), dendritic cells (DCs), host-pathogen interactions, macrophages, Dendritic cells (DCs), Bacterial dissemination, Macrophages, Host-pathogen interactions, Antigen presenting cells (APCs), Core lipopolysaccharide/lipooligosaccharides (core LPS/LOS)",

author = "Kun Yang and Yingxia He and Park, {Chae Gyu} and Kang, {Young Sun} and Pei Zhang and Yanping Han and Yujun Cui and Silvia Bulgheresi and Anisimov, {Andrey P} and Dentovskaya, {Svetlana V} and Xiaoling Ying and Lingyu Jiang and Honghui Ding and Njiri, {Olivia Adhiambo} and Shusheng Zhang and Guoxing Zheng and Lianxu Xia and Biao Kan and Xin Wang and Huaiqi Jing and Meiying Yan and Wei Li and Yuanzhi Wang and Xiding Xiamu and Gang Chen and Ding Ma and Bartra, {Sara Schesser} and Plano, {Gregory V} and Klena, {John D} and Ruifu Yang and Mikael Skurnik and Tie Chen",

note = "Publisher Copyright: Copyright {\textcopyright} 2019 Yang, He, Park, Kang, Zhang, Han, Cui, Bulgheresi, Anisimov, Dentovskaya, Ying, Jiang, Ding, Njiri, Zhang, Zheng, Xia, Kan, Wang, Jing, Yan, Li, Wang, Xiamu, Chen, Ma, Bartra, Plano, Klena, Yang, Skurnik and Chen.",

year = "2019",

doi = "10.3389/fimmu.2019.00096",

language = "English",

volume = "10",

journal = "Frontiers in Immunology",

issn = "1664-3224",

publisher = "FRONTIERS MEDIA SA",

}

Yang, K, He, Y, Park, CG, Kang, YS, Zhang, P, Han, Y, Cui, Y, Bulgheresi, S, Anisimov, AP, Dentovskaya, SV, Ying, X, Jiang, L, Ding, H, Njiri, OA, Zhang, S, Zheng, G, Xia, L, Kan, B, Wang, X, Jing, H, Yan, M, Li, W, Wang, Y, Xiamu, X, Chen, G, Ma, D, Bartra, SS, Plano, GV, Klena, JD, Yang, R, Skurnik, M & Chen, T 2019, 'Yersinia pestis Interacts With SIGNR1 (CD209b) for Promoting Host Dissemination and Infection', Frontiers in Immunology, vol. 10, 96. https://doi.org/10.3389/fimmu.2019.00096

TY - JOUR

T1 - Yersinia pestis Interacts With SIGNR1 (CD209b) for Promoting Host Dissemination and Infection

AU - Yang, Kun

AU - He, Yingxia

AU - Park, Chae Gyu

AU - Kang, Young Sun

AU - Zhang, Pei

AU - Han, Yanping

AU - Cui, Yujun

AU - Bulgheresi, Silvia

AU - Anisimov, Andrey P

AU - Dentovskaya, Svetlana V

AU - Ying, Xiaoling

AU - Jiang, Lingyu

AU - Ding, Honghui

AU - Njiri, Olivia Adhiambo

AU - Zhang, Shusheng

AU - Zheng, Guoxing

AU - Xia, Lianxu

AU - Kan, Biao

AU - Wang, Xin

AU - Jing, Huaiqi

AU - Yan, Meiying

AU - Li, Wei

AU - Wang, Yuanzhi

AU - Xiamu, Xiding

AU - Chen, Gang

AU - Ma, Ding

AU - Bartra, Sara Schesser

AU - Plano, Gregory V

AU - Klena, John D

AU - Yang, Ruifu

AU - Skurnik, Mikael

AU - Chen, Tie

N1 - Publisher Copyright: Copyright © 2019 Yang, He, Park, Kang, Zhang, Han, Cui, Bulgheresi, Anisimov, Dentovskaya, Ying, Jiang, Ding, Njiri, Zhang, Zheng, Xia, Kan, Wang, Jing, Yan, Li, Wang, Xiamu, Chen, Ma, Bartra, Plano, Klena, Yang, Skurnik and Chen.

PY - 2019

Y1 - 2019

N2 - Yersinia pestis, a Gram-negative bacterium and the etiologic agent of plague, has evolved from Yersinia pseudotuberculosis, a cause of a mild enteric disease. However, the molecular and biological mechanisms of how Y. pseudotuberculosis evolved to such a remarkably virulent pathogen, Y. pestis, are not clear. The ability to initiate a rapid bacterial dissemination is a characteristic hallmark of Y. pestis infection. A distinguishing characteristic between the two Yersinia species is that Y. pseudotuberculosis strains possess an O-antigen of lipopolysaccharide (LPS) while Y. pestis has lost the O-antigen during evolution and therefore exposes its core LPS. In this study, we showed that Y. pestis utilizes its core LPS to interact with SIGNR1 (CD209b), a C-type lectin receptor on antigen presenting cells (APCs), leading to bacterial dissemination to lymph nodes, spleen and liver, and the initiation of a systemic infection. We therefore propose that the loss of O-antigen represents a critical step in the evolution of Y. pseudotuberculosis into Y. pestis in terms of hijacking APCs, promoting bacterial dissemination and causing the plague.

AB - Yersinia pestis, a Gram-negative bacterium and the etiologic agent of plague, has evolved from Yersinia pseudotuberculosis, a cause of a mild enteric disease. However, the molecular and biological mechanisms of how Y. pseudotuberculosis evolved to such a remarkably virulent pathogen, Y. pestis, are not clear. The ability to initiate a rapid bacterial dissemination is a characteristic hallmark of Y. pestis infection. A distinguishing characteristic between the two Yersinia species is that Y. pseudotuberculosis strains possess an O-antigen of lipopolysaccharide (LPS) while Y. pestis has lost the O-antigen during evolution and therefore exposes its core LPS. In this study, we showed that Y. pestis utilizes its core LPS to interact with SIGNR1 (CD209b), a C-type lectin receptor on antigen presenting cells (APCs), leading to bacterial dissemination to lymph nodes, spleen and liver, and the initiation of a systemic infection. We therefore propose that the loss of O-antigen represents a critical step in the evolution of Y. pseudotuberculosis into Y. pestis in terms of hijacking APCs, promoting bacterial dissemination and causing the plague.

KW - CAPSULAR POLYSACCHARIDE

KW - CORE LIPOPOLYSACCHARIDE

KW - DC-SIGN

KW - DENDRITIC CELLS

KW - ESCHERICHIA-COLI

KW - LIPOPOLYSACCHARIDE O-ANTIGEN

KW - MEDIATES UPTAKE

KW - NEISSERIA-GONORRHOEAE

KW - NONINTEGRIN CD209

KW - RFB GENE-CLUSTER

KW - SIGNR1 (CD209b)

KW - Yersinia pestis

KW - antigen presenting cells (APCs)

KW - bacterial dissemination

KW - core lipopolysaccharide/lipooligosaccharides (core LPS/LOS)

KW - dendritic cells (DCs)

KW - host-pathogen interactions

KW - macrophages

KW - Dendritic cells (DCs)

KW - Bacterial dissemination

KW - Macrophages

KW - Host-pathogen interactions

KW - Antigen presenting cells (APCs)

KW - Core lipopolysaccharide/lipooligosaccharides (core LPS/LOS)

UR - http://www.scopus.com/inward/record.url?scp=85063935356&partnerID=8YFLogxK

U2 - 10.3389/fimmu.2019.00096

DO - 10.3389/fimmu.2019.00096

M3 - Article

C2 - 30915064

SN - 1664-3224

VL - 10

JO - Frontiers in Immunology

JF - Frontiers in Immunology

M1 - 96

ER -

Yersinia pestis Interacts With SIGNR1 (CD209b) for Promoting Host Dissemination and Infection

Abstract

Austrian Fields of Science 2012

Keywords

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