Authors

Xiaoying Wang

Type

Text

Type

Dissertation

Advisor

Bliska, James B | Karzai, Wali | Velden, Adrianus | Konopka, James | Viboud, Gloria.

Date

2015-12-01

Keywords

GAP activity, Yersinia, YopE | Biology

Department

Department of Molecular and Cellular Biology.

Language

en_US

Source

This work is sponsored by the Stony Brook University Graduate School in compliance with the requirements for completion of degree.

Identifier

http://hdl.handle.net/11401/76501

Publisher

The Graduate School, Stony Brook University: Stony Brook, NY.

Format

application/pdf

Abstract

The mammalian immune system has the ability to discriminate between pathogens and innocuous microbes by detecting conserved molecular patterns. In addition to conserved microbial patterns, the mammalian immune system may recognize distinct pathogen-induced processes, the mechanism of which is poorly understood. Pathogenic Yersinia species utilize a type III secretion system (T3SS) to translocate various bacterial effectors into target cells, which aim to modify multiple host signaling pathways. Interestingly, previous studies have shown that the T3SS in Yersinia pseudotuberculosis leads to decreased survival of this bacterium in primary murine macrophages, the mechanism of which is unknown. Here, we use colony forming unit assays and fluorescence microscopy to investigate how the T3SS triggers killing of Yersinia in naïve murine macrophages. To identify specific effectors that limit Yersinia intracellular survival, the intra-macrophage survival of wild-type strain and several Yersinia outer protein (yop) deletion mutants was compared. Additionally, intra-macrophage survival of Yersinia producing YopE or YopE variants was tested to further investigate the role of YopE GAP activity in this process. Furthermore, experiments were performed to better characterize the mechanism of YopE-induced killing of Yersinia inside macrophages. Our results show that YopE and YopH limit survival of Yersinia inside macrophages, while YopT counteracts the YopE-triggered killing effect. YopE-induced killing of Yersinia is an independent pathway from Synaptotagmin VII (SytVII) -mediated phagolysosome fusion. Importantly, data presented here suggest that the GAP activity of YopE towards Rho GTPases is essential for restricting Yersinia survival inside macrophages. Clostridium difficile Toxin B is able to mimic the effect of YopE and decrease Yersinia survival inside macrophages. Interestingly, macrophages limit Yersinia survival in response to Rac1 inhibition, but not Rho inhibition. In addition, our work indicates that LPS-TLR signaling is dispensable for YopE-stimulated intracellular killing. Remarkably, translocated YopE stimulates higher levels of nitric oxide (NO) from infected macrophages. However, NO production does not seem to mediate YopE-triggered killing. Moreover, signaling pathways that require capase-1/11, NOD1 or autophagy are not involved in the YopE-elicited killing response. In summary, I have shown that primary macrophages sense manipulation of Rho GTPases by Yersinia YopE and actively counteract pathogenic infection by restricting intracellular bacterial survival. Our results uncover a new mode of innate immune recognition in response to pathogenic infection. | The mammalian immune system has the ability to discriminate between pathogens and innocuous microbes by detecting conserved molecular patterns. In addition to conserved microbial patterns, the mammalian immune system may recognize distinct pathogen-induced processes, the mechanism of which is poorly understood. Pathogenic Yersinia species utilize a type III secretion system (T3SS) to translocate various bacterial effectors into target cells, which aim to modify multiple host signaling pathways. Interestingly, previous studies have shown that the T3SS in Yersinia pseudotuberculosis leads to decreased survival of this bacterium in primary murine macrophages, the mechanism of which is unknown. Here, we use colony forming unit assays and fluorescence microscopy to investigate how the T3SS triggers killing of Yersinia in naïve murine macrophages. To identify specific effectors that limit Yersinia intracellular survival, the intra-macrophage survival of wild-type strain and several Yersinia outer protein (yop) deletion mutants was compared. Additionally, intra-macrophage survival of Yersinia producing YopE or YopE variants was tested to further investigate the role of YopE GAP activity in this process. Furthermore, experiments were performed to better characterize the mechanism of YopE-induced killing of Yersinia inside macrophages. Our results show that YopE and YopH limit survival of Yersinia inside macrophages, while YopT counteracts the YopE-triggered killing effect. YopE-induced killing of Yersinia is an independent pathway from Synaptotagmin VII (SytVII) -mediated phagolysosome fusion. Importantly, data presented here suggest that the GAP activity of YopE towards Rho GTPases is essential for restricting Yersinia survival inside macrophages. Clostridium difficile Toxin B is able to mimic the effect of YopE and decrease Yersinia survival inside macrophages. Interestingly, macrophages limit Yersinia survival in response to Rac1 inhibition, but not Rho inhibition. In addition, our work indicates that LPS-TLR signaling is dispensable for YopE-stimulated intracellular killing. Remarkably, translocated YopE stimulates higher levels of nitric oxide (NO) from infected macrophages. However, NO production does not seem to mediate YopE-triggered killing. Moreover, signaling pathways that require capase-1/11, NOD1 or autophagy are not involved in the YopE-elicited killing response. In summary, I have shown that primary macrophages sense manipulation of Rho GTPases by Yersinia YopE and actively counteract pathogenic infection by restricting intracellular bacterial survival. Our results uncover a new mode of innate immune recognition in response to pathogenic infection. | 129 pages

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