Optimal protection against Salmonella infection requires noncirculating memory

While CD4 Th1 cells are required for resistance to intramacrophage infections, adoptive transfer of Th1 cells is insufficient to protect against Salmonella infection. Using an epitope-tagged vaccine strain of Salmonella, we found that effective protection correlated with expanded Salmonella-specific...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 115; no. 41; pp. 10416 - 10421
Main Authors Benoun, Joseph M., Peres, Newton G., Wang, Nancy, Pham, Oanh H., Rudisill, Victoria L., Fogassy, Zachary N., Whitney, Paul G., Fernandez-Ruiz, Daniel, Gebhardt, Thomas, Pham, Quynh-Mai, Puddington, Lynn, Bedoui, Sammy, Strugnell, Richard A., McSorley, Stephen J.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 09.10.2018
Subjects
Adoptive transfer
Animal tissues
Animals
Bacteria
Biological Sciences
Blood circulation
CD4 antigen
Cells
Cells, Cultured
Computer memory
Epitopes
Female
Hepatocytes
Immunity
Immunization
Immunologic Memory - immunology
Immunological memory
Infections
LFA-1 antigen
Liver
Liver - immunology
Liver - microbiology
Lymphocytes
Lymphocytes T
Memory
Memory cells
Mice
Mice, Inbred C57BL
Salmonella
Salmonella Infections - immunology
Salmonella Infections - microbiology
Salmonella Infections - prevention & control
Salmonella typhimurium - immunology
Studies
T-Lymphocytes - immunology
T-Lymphocytes - microbiology
Th1 Cells - immunology
Th1 Cells - microbiology
Vaccines
γ-Interferon
Salmonella infection
CD4 T cell
vaccines
tissue-resident memory
protective immunity
Online AccessGet full text

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Abstract While CD4 Th1 cells are required for resistance to intramacrophage infections, adoptive transfer of Th1 cells is insufficient to protect against Salmonella infection. Using an epitope-tagged vaccine strain of Salmonella, we found that effective protection correlated with expanded Salmonella-specific memory CD4 T cells in circulation and nonlymphoid tissues. However, naive mice that previously shared a blood supply with vaccinated partners lacked T cell memory with characteristics of tissue residence and did not acquire robust protective immunity. Using a YFP–IFN-γ reporter system, we identified Th1 cells in the liver of immunized mice that displayed markers of tissue residence, including P2X7, ARTC2, LFA-1, and CD101. Adoptive transfer of liver memory cells after ARTC2 blockade increased protection against highly virulent bacteria. Taken together, these data demonstrate that noncirculating memory Th1 cells are a vital component of immunity to Salmonella infection and should be the focus of vaccine strategies.
AbstractList Effective vaccination against Salmonella infection requires the generation of memory T cells that can be reactivated upon exposure to bacteria in a natural setting. It is unclear whether immunity requires memory T cells that continuously patrol blood, lymphatics, and tissues, whether noncirculating T cells are important, or both. We demonstrate the generation of circulating and noncirculating memory pools after immunization. However, naive mice that previously shared a blood supply with vaccinated partners received recirculating memory T cells, but did not have T cell memory with characteristics of tissue residence, resulting in a failure to acquire robust protective immunity. Thus, noncirculating tissue-resident memory T cells are vital for effective protection against Salmonella . While CD4 Th1 cells are required for resistance to intramacrophage infections, adoptive transfer of Th1 cells is insufficient to protect against Salmonella infection. Using an epitope-tagged vaccine strain of Salmonella , we found that effective protection correlated with expanded Salmonella -specific memory CD4 T cells in circulation and nonlymphoid tissues. However, naive mice that previously shared a blood supply with vaccinated partners lacked T cell memory with characteristics of tissue residence and did not acquire robust protective immunity. Using a YFP–IFN-γ reporter system, we identified Th1 cells in the liver of immunized mice that displayed markers of tissue residence, including P2X7, ARTC2, LFA-1, and CD101. Adoptive transfer of liver memory cells after ARTC2 blockade increased protection against highly virulent bacteria. Taken together, these data demonstrate that noncirculating memory Th1 cells are a vital component of immunity to Salmonella infection and should be the focus of vaccine strategies.
While CD4 Th1 cells are required for resistance to intramacrophage infections, adoptive transfer of Th1 cells is insufficient to protect against Salmonella infection. Using an epitope-tagged vaccine strain of Salmonella, we found that effective protection correlated with expanded Salmonella-specific memory CD4 T cells in circulation and nonlymphoid tissues. However, naive mice that previously shared a blood supply with vaccinated partners lacked T cell memory with characteristics of tissue residence and did not acquire robust protective immunity. Using a YFP–IFN-γ reporter system, we identified Th1 cells in the liver of immunized mice that displayed markers of tissue residence, including P2X7, ARTC2, LFA-1, and CD101. Adoptive transfer of liver memory cells after ARTC2 blockade increased protection against highly virulent bacteria. Taken together, these data demonstrate that noncirculating memory Th1 cells are a vital component of immunity to Salmonella infection and should be the focus of vaccine strategies.
While CD4 Th1 cells are required for resistance to intramacrophage infections, adoptive transfer of Th1 cells is insufficient to protect against infection. Using an epitope-tagged vaccine strain of , we found that effective protection correlated with expanded -specific memory CD4 T cells in circulation and nonlymphoid tissues. However, naive mice that previously shared a blood supply with vaccinated partners lacked T cell memory with characteristics of tissue residence and did not acquire robust protective immunity. Using a YFP-IFN-γ reporter system, we identified Th1 cells in the liver of immunized mice that displayed markers of tissue residence, including P2X7, ARTC2, LFA-1, and CD101. Adoptive transfer of liver memory cells after ARTC2 blockade increased protection against highly virulent bacteria. Taken together, these data demonstrate that noncirculating memory Th1 cells are a vital component of immunity to infection and should be the focus of vaccine strategies.
Significance Effective vaccination against Salmonella infection requires the generation of memory T cells that can be reactivated upon exposure to bacteria in a natural setting. It is unclear whether immunity requires memory T cells that continuously patrol blood, lymphatics, and tissues, whether noncirculating T cells are important, or both. We demonstrate the generation of circulating and noncirculating memory pools after immunization. However, naive mice that previously shared a blood supply with vaccinated partners received recirculating memory T cells, but did not have T cell memory with characteristics of tissue residence, resulting in a failure to acquire robust protective immunity. Thus, noncirculating tissue-resident memory T cells are vital for effective protection against Salmonella . While CD4 Th1 cells are required for resistance to intramacrophage infections, adoptive transfer of Th1 cells is insufficient to protect against Salmonella infection. Using an epitope-tagged vaccine strain of Salmonella , we found that effective protection correlated with expanded Salmonella -specific memory CD4 T cells in circulation and nonlymphoid tissues. However, naive mice that previously shared a blood supply with vaccinated partners lacked T cell memory with characteristics of tissue residence and did not acquire robust protective immunity. Using a YFP–IFN-γ reporter system, we identified Th1 cells in the liver of immunized mice that displayed markers of tissue residence, including P2X7, ARTC2, LFA-1, and CD101. Adoptive transfer of liver memory cells after ARTC2 blockade increased protection against highly virulent bacteria. Taken together, these data demonstrate that noncirculating memory Th1 cells are a vital component of immunity to Salmonella infection and should be the focus of vaccine strategies.
Author Pham, Oanh H.
McSorley, Stephen J.
Pham, Quynh-Mai
Benoun, Joseph M.
Peres, Newton G.
Wang, Nancy
Rudisill, Victoria L.
Bedoui, Sammy
Whitney, Paul G.
Fernandez-Ruiz, Daniel
Strugnell, Richard A.
Fogassy, Zachary N.
Puddington, Lynn
Gebhardt, Thomas
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  givenname: Newton G.
  surname: Peres
  fullname: Peres, Newton G.
  organization: Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, The University of Melbourne, Melbourne, VIC 3000, Australia
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  surname: Wang
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  organization: Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, The University of Melbourne, Melbourne, VIC 3000, Australia
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Keywords Salmonella infection
CD4 T cell
vaccines
tissue-resident memory
protective immunity
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1J.M.B., N.G.P., N.W., S.B., R.A.S., and S.J.M. contributed equally to this work.
Edited by Harvey Cantor, Dana-Farber Cancer Institute, Boston, MA, and approved August 27, 2018 (received for review May 15, 2018)
Author contributions: J.M.B., N.G.P., N.W., T.G., L.P., S.B., R.A.S., and S.J.M. designed research; J.M.B., N.G.P., N.W., O.H.P., V.L.R., Z.N.F., P.G.W., D.F.-R., Q.-M.P., L.P., and S.J.M. performed research; J.M.B., N.G.P., N.W., O.H.P., V.L.R., Z.N.F., P.G.W., D.F.-R., T.G., Q.-M.P., L.P., S.B., R.A.S., and S.J.M. analyzed data; and J.M.B., N.G.P., N.W., S.B., R.A.S., and S.J.M. wrote the paper.
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Snippet While CD4 Th1 cells are required for resistance to intramacrophage infections, adoptive transfer of Th1 cells is insufficient to protect against Salmonella...
While CD4 Th1 cells are required for resistance to intramacrophage infections, adoptive transfer of Th1 cells is insufficient to protect against infection....
Significance Effective vaccination against Salmonella infection requires the generation of memory T cells that can be reactivated upon exposure to bacteria in...
Effective vaccination against Salmonella infection requires the generation of memory T cells that can be reactivated upon exposure to bacteria in a natural...
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StartPage 10416
SubjectTerms Adoptive transfer
Animal tissues
Animals
Bacteria
Biological Sciences
Blood circulation
CD4 antigen
Cells
Cells, Cultured
Computer memory
Epitopes
Female
Hepatocytes
Immunity
Immunization
Immunologic Memory - immunology
Immunological memory
Infections
LFA-1 antigen
Liver
Liver - immunology
Liver - microbiology
Lymphocytes
Lymphocytes T
Memory
Memory cells
Mice
Mice, Inbred C57BL
Salmonella
Salmonella Infections - immunology
Salmonella Infections - microbiology
Salmonella Infections - prevention & control
Salmonella typhimurium - immunology
Studies
T-Lymphocytes - immunology
T-Lymphocytes - microbiology
Th1 Cells - immunology
Th1 Cells - microbiology
Vaccines
γ-Interferon
Title Optimal protection against Salmonella infection requires noncirculating memory
URI https://www.jstor.org/stable/26532193
https://www.ncbi.nlm.nih.gov/pubmed/30254173
https://www.proquest.com/docview/2130279643
https://search.proquest.com/docview/2112611654
https://pubmed.ncbi.nlm.nih.gov/PMC6187142
Volume 115
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