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

Research output: Contribution to journalArticle

1 Citation (Scopus)

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 languageEnglish (US)
Number of pages1
JournalFrontiers in immunology
Volume10
DOIs
StatePublished - Jan 1 2019

Fingerprint

Yersinia pestis
Yersinia pseudotuberculosis
O Antigens
Infection
Lipopolysaccharides
Plague
Antigen-Presenting Cells
Yersinia Infections
C-Type Lectins
Yersinia
Gram-Negative Bacteria
Spleen
Lymph Nodes
Liver

Keywords

  • antigen presenting cells (APCs)
  • bacterial dissemination
  • core lipopolysaccharide/lipooligosaccharides (core LPS/LOS)
  • dendritic cells (DCs)
  • host-pathogen interactions
  • macrophages
  • SIGNR1 (CD209b)
  • Yersinia pestis

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology

Cite this

Yersinia pestis Interacts With SIGNR1 (CD209b) for Promoting Host Dissemination and Infection. / Yang, Kun; He, Yingxia; Park, Chae Gyu; Kang, Young Sun; Zhang, Pei; Han, Yanping; Cui, Yujun; Bulgheresi, Silvia; Anisimov, Andrey P.; Dentovskaya, Svetlana V.; Ying, Xiaoling; Jiang, Lingyu; Ding, Honghui; Njiri, Olivia Adhiambo; Zhang, Shusheng; Zheng, Guoxing; Xia, Lianxu; Kan, Biao; Wang, Xin; Jing, Huaiqi; Yan, Meiying; Li, Wei; Wang, Yuanzhi; Xiamu, Xiding; Chen, Gang; Ma, Ding; Bartra, Sara Schesser; Plano, Gregory V; Klena, John D.; Yang, Ruifu; Skurnik, Mikael; Chen, Tie.

In: Frontiers in immunology, Vol. 10, 01.01.2019.

Research output: Contribution to journalArticle

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. https://doi.org/10.3389/fimmu.2019.00096
Yang, Kun ; He, Yingxia ; Park, Chae Gyu ; Kang, Young Sun ; Zhang, Pei ; Han, Yanping ; Cui, Yujun ; Bulgheresi, Silvia ; Anisimov, Andrey P. ; Dentovskaya, Svetlana V. ; Ying, Xiaoling ; Jiang, Lingyu ; Ding, Honghui ; Njiri, Olivia Adhiambo ; Zhang, Shusheng ; Zheng, Guoxing ; Xia, Lianxu ; Kan, Biao ; Wang, Xin ; Jing, Huaiqi ; Yan, Meiying ; Li, Wei ; Wang, Yuanzhi ; Xiamu, Xiding ; Chen, Gang ; Ma, Ding ; Bartra, Sara Schesser ; Plano, Gregory V ; Klena, John D. ; Yang, Ruifu ; Skurnik, Mikael ; Chen, Tie. / Yersinia pestis Interacts With SIGNR1 (CD209b) for Promoting Host Dissemination and Infection. In: Frontiers in immunology. 2019 ; Vol. 10.
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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.",
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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

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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.

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KW - host-pathogen interactions

KW - macrophages

KW - SIGNR1 (CD209b)

KW - Yersinia pestis

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