A Protective Epitope in Type III Effector YopE Is a Major CD8 T Cell Antigen during Primary Infection with Yersinia pseudotuberculosis

Zhang, Yue; Mena, Patricio; Romanov, Galina; Lin, Jr-Shiuan; Smiley, Stephen T.; Bliska, James B.

doi:10.1128/iai.05971-11

Cited by 25 publications

(38 citation statements)

References 68 publications

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“…This H-2K b -restricted epitope, SVIGFIQRM, corresponds to amino acid residues 69 to 77 of YopE (YopE 69 -77 ) in Y. pestis and Y. pseudotuberculosis. Importantly, Y. pseudotuberculosis serogroup O1 strain 32777 induces an unusually large CD8 ϩ T cell response to YopE during primary infection of C57BL/6 mice; at the peak of the response, at day 14 postinfection, an average of 30% and as many as 50% of splenic CD8 ϩ T cells recognize YopE 69 -77 (17). This high level of response is unprecedented.…”

Section: Recent Studies Have Demonstrated a Dominant Cd8mentioning

confidence: 93%

“…In the initial stage of infection of C57BL/6 mice with Y. pseudotuberculosis strain 32777 through the intragastric route, a large number of CD11b ϩ cells were recruited to the spleens, such that they become the major component of the splenocytes (17,41). CD11b is found on the surfaces of phagocytes such as neutrophils, macrophages, monocytes, and some dendritic cells.…”

Section: Analysis Of the Svigfiqrm Epitope And Generation Of Y Pseudmentioning

confidence: 99%

“…During the primary response to Listeria monocytogenes infection in mice, approximately 2 to 3% of splenic CD8 ϩ T cells are specific for listeriolysin O amino acid residues 91 to 99 (LLO [91][92][93][94][95][96][97][98][99] ) at the peak of response (19); even at the peak of a recall response, about 17% of all CD8 ϩ T cells in the spleen recognize LLO [91][92][93][94][95][96][97][98][99] (20). Not only is the YopE 69 -77 response large in terms of the number of CD8 ϩ T cells recognizing the epitope, but these YopE-specific CD8 ϩ T cells potentially exhibit effector functions, since C57BL/6 mice vaccinated with the YopE 69 -77 peptide are protected from lethal challenge with Y. pestis (16) or Y. pseudotuberculosis (17). Moreover, the CD8 ϩ T cells from Y. pestis-immunized mice can, after secondary challenge with virulent Y. pestis, be induced to produce tumor necrosis factor alpha (TNF-␣) and gamma interferon (IFN-␥) upon ex vivo stimulation with YopE 69 -77 (16).…”

Section: Recent Studies Have Demonstrated a Dominant Cd8mentioning

confidence: 99%

“…It is therefore of interest to determine the characteristics of the YopE-specific CD8 ϩ T cell response during primary infection and to identify features of this protein that lead to its efficient recognition by the adaptive immune system. We demonstrated previously that GAP activity in YopE is not required for the dominant CD8 ϩ T cell response to the SVIGFIQRM epitope in C57BL/6 mice infected with Y. pseudotuberculosis (17). In this study, C57BL/6 mice were infected with a Y. pseudotuberculosis yopE R144A mutant lacking GAP activity, and the production of effector CD8 ϩ T cells was measured using flow cytometry in conjunction with staining for surface markers or intracellular cytokines and an H-2K b MHC class I YopE 69 -77 tetramer.…”

Section: Recent Studies Have Demonstrated a Dominant Cd8mentioning

confidence: 99%

“…ϩ T cell response to the T3SS effector YopE in C57BL/6 mice infected with attenuated Yersinia pestis (16) or Yersinia pseudotuberculosis (17). This H-2K b -restricted epitope, SVIGFIQRM, corresponds to amino acid residues 69 to 77 of YopE (YopE 69 -77 ) in Y. pestis and Y. pseudotuberculosis.…”

Section: Recent Studies Have Demonstrated a Dominant Cd8mentioning

confidence: 99%

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Effector CD8⁺T Cells Are Generated in Response to an Immunodominant Epitope in Type III Effector YopE during Primary Yersinia pseudotuberculosis Infection

et al. 2014

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YopE is a virulence factor that is secreted into host cells infected by Yersinia species. The YopE C-terminal domain has GTPaseactivating protein (GAP) activity. The YopE N-terminal domain contains an epitope that is an immunodominant CD8 ؉ T cell antigen during primary infection of C57BL/6 mice with Yersinia pseudotuberculosis. The characteristics of the CD8 ؉ T cells generated in response to the epitope, which comprises YopE amino acid residues 69 to 77 (YopE 69 -77 ), and the features of YopE that are important for antigenicity during primary infection, are unknown. Following intravenous infection of naïve C57BL/6 mice with a yopE GAP mutant (the R144A mutant), flow cytometry analysis of splenocytes by tetramer and intracellular cytokine staining over a time course showed that YopE 69 -77 -specific CD8 ؉ T cells producing gamma interferon (IFN-␥) and tumor necrosis factor alpha (TNF-␣) were generated by day 7, with a peak at day 14. In addition, ϳ80% of YopE 69 -77 -specific CD8 ؉ T cells were positive for KLRG1, a memory phenotype marker, at day 21. To determine if residues that regulate YopE activity by ubiquitination or membrane localization affect the antigenicity of YopE 69 -77 , mice were infected with a yopE ubiquitination or membrane localization mutant (the R62K or L55N I59N L63N

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Section: Recent Studies Have Demonstrated a Dominant Cd8mentioning

confidence: 93%

Section: Analysis Of the Svigfiqrm Epitope And Generation Of Y Pseudmentioning

confidence: 99%

Section: Recent Studies Have Demonstrated a Dominant Cd8mentioning

confidence: 99%

Section: Recent Studies Have Demonstrated a Dominant Cd8mentioning

confidence: 99%

Section: Recent Studies Have Demonstrated a Dominant Cd8mentioning

confidence: 99%

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Effector CD8⁺T Cells Are Generated in Response to an Immunodominant Epitope in Type III Effector YopE during Primary Yersinia pseudotuberculosis Infection

et al. 2014

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Microbiota-Dependent Sequelae of Acute Infection Compromise Tissue-Specific Immunity

Fonseca

Hand

Han

et al. 2015

Cell

237

209

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Summary Infections have been proposed as initiating factors for inflammatory disorders, however, identifying associations between defined infectious agents and the initiation of chronic disease has remained elusive. Here, we report that a single acute infection can have dramatic and long-term consequences for tissue-specific immunity. Following clearance of Yersinia pseudotuberculosis, sustained inflammation and associated lymphatic leakage in the mesenteric adipose tissue deviates migratory dendritic cells to the adipose compartment, thereby preventing their accumulation in the mesenteric lymph node. As a consequence, canonical mucosal immune functions, including tolerance and protective immunity, are persistently compromised. Post-resolution of infection, signals derived from the microbiota maintain inflammatory mesentery remodeling and consequently, transient ablation of the microbiota restores mucosal immunity. Our results indicate that persistent disruption of communication between tissues and the immune system following clearance of an acute infection represents an inflection point beyond which tissue homeostasis and immunity is compromised for the long-term.

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Transcriptomic Response to Yersinia pestis: RIG-I Like Receptor Signaling Response Is Detrimental to the Host against Plague

Yang

Tan

et al. 2014

Journal of Genetics and Genomics

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A Protective Epitope in Type III Effector YopE Is a Major CD8 T Cell Antigen during Primary Infection with Yersinia pseudotuberculosis

Cited by 25 publications

References 68 publications

Effector CD8⁺T Cells Are Generated in Response to an Immunodominant Epitope in Type III Effector YopE during Primary Yersinia pseudotuberculosis Infection

Effector CD8⁺T Cells Are Generated in Response to an Immunodominant Epitope in Type III Effector YopE during Primary Yersinia pseudotuberculosis Infection

Microbiota-Dependent Sequelae of Acute Infection Compromise Tissue-Specific Immunity

Transcriptomic Response to Yersinia pestis: RIG-I Like Receptor Signaling Response Is Detrimental to the Host against Plague

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A Protective Epitope in Type III Effector YopE Is a Major CD8 T Cell Antigen during Primary Infection with Yersinia pseudotuberculosis

Cited by 25 publications

References 68 publications

Effector CD8+T Cells Are Generated in Response to an Immunodominant Epitope in Type III Effector YopE during Primary Yersinia pseudotuberculosis Infection

Effector CD8+T Cells Are Generated in Response to an Immunodominant Epitope in Type III Effector YopE during Primary Yersinia pseudotuberculosis Infection

Microbiota-Dependent Sequelae of Acute Infection Compromise Tissue-Specific Immunity

Transcriptomic Response to Yersinia pestis: RIG-I Like Receptor Signaling Response Is Detrimental to the Host against Plague

Contact Info

Product

Resources

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Effector CD8⁺T Cells Are Generated in Response to an Immunodominant Epitope in Type III Effector YopE during Primary Yersinia pseudotuberculosis Infection

Effector CD8⁺T Cells Are Generated in Response to an Immunodominant Epitope in Type III Effector YopE during Primary Yersinia pseudotuberculosis Infection