The PD-1 Pathway Regulates Development and Function of Memory CD8+ T Cells following Respiratory Viral Infection

The PD-1 pathway regulates dysfunctional T cells in chronic infection and cancer, but the role of this pathway during acute infection remains less clear. Here, we demonstrate that PD-1 signals are needed for optimal memory. Mice deficient in the PD-1 pathway exhibit impaired CD8+ T cell memory follo...

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Vydané v:	Cell reports (Cambridge) Ročník 31; číslo 13; s. 107827
Hlavní autori:	Pauken, Kristen E., Godec, Jernej, Odorizzi, Pamela M., Brown, Keturah E., Yates, Kathleen B., Ngiow, Shin Foong, Burke, Kelly P., Maleri, Seth, Grande, Shannon M., Francisco, Loise M., Ali, Mohammed-Alkhatim, Imam, Sabrina, Freeman, Gordon J., Haining, W. Nicholas, Wherry, E. John, Sharpe, Arlene H.
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	United States Elsevier Inc 30.06.2020 Elsevier
Predmet:	acute infection Administration, Intranasal Animals CD8+ T cell CD8-Positive T-Lymphocytes - immunology Cell Death - immunology Cell Differentiation - immunology Cell Proliferation checkpoint blockade effector Immunologic Memory influenza Influenza A Virus, H3N2 Subtype - physiology memory Mice, Inbred C57BL Orthomyxoviridae Infections - immunology Orthomyxoviridae Infections - pathology Orthomyxoviridae Infections - virology PD-1 PD-L1 PD-L2 Programmed Cell Death 1 Receptor - metabolism Signal Transduction Species Specificity influenza checkpoint blockade memory acute infection PD-L1 PD-L2 effector PD-1 CD8+ T cell CD8(+) T cell
ISSN:	2211-1247, 2211-1247
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Abstract	The PD-1 pathway regulates dysfunctional T cells in chronic infection and cancer, but the role of this pathway during acute infection remains less clear. Here, we demonstrate that PD-1 signals are needed for optimal memory. Mice deficient in the PD-1 pathway exhibit impaired CD8+ T cell memory following acute influenza infection, including reduced virus-specific CD8+ T cell numbers and compromised recall responses. PD-1 blockade during priming leads to similar differences early post-infection but without the defect in memory formation, suggesting that timing and/or duration of PD-1 blockade could be tailored to modulate host responses. Our studies reveal a role for PD-1 as an integrator of CD8+ T cell signals that promotes CD8+ T cell memory formation and suggest PD-1 continues to fine-tune CD8+ T cells after they migrate into non-lymphoid tissues. These findings have important implications for PD-1-based immunotherapy, in which PD-1 inhibition may influence memory responses in patients. [Display omitted] •Early loss of PD-1 leads to overactivation of CD8+ T cells during acute infection•Mice constitutively lacking PD-1 or PD-L develop impaired CD8+ T cell memory•Cell-intrinsic PD-1 signals suppress effector cell expansion and promote memory•Timing of PD-1 blockade determines impact on memory generation The role of PD-1 in memory development is poorly understood. Here, Pauken et al. show that constitutive loss of PD-1 during acute infection causes overactivation of CD8+ T cells during the effector phase and impairs memory and recall responses. These data indicate PD-1 is required for optimal memory.
AbstractList	The PD-1 pathway regulates dysfunctional T cells in chronic infection and cancer, but the role of this pathway during acute infection remains less clear. Here, we demonstrate that PD-1 signals are needed for optimal memory. Mice deficient in the PD-1 pathway exhibit impaired CD8+ T cell memory following acute influenza infection, including reduced virus-specific CD8+ T cell numbers and compromised recall responses. PD-1 blockade during priming leads to similar differences early post-infection but without the defect in memory formation, suggesting that timing and/or duration of PD-1 blockade could be tailored to modulate host responses. Our studies reveal a role for PD-1 as an integrator of CD8+ T cell signals that promotes CD8+ T cell memory formation and suggest PD-1 continues to fine-tune CD8+ T cells after they migrate into non-lymphoid tissues. These findings have important implications for PD-1-based immunotherapy, in which PD-1 inhibition may influence memory responses in patients. The PD-1 pathway regulates dysfunctional T cells in chronic infection and cancer, but the role of this pathway during acute infection remains less clear. Here, we demonstrate that PD-1 signals are needed for optimal memory. Mice deficient in the PD-1 pathway exhibit impaired CD8+ T cell memory following acute influenza infection, including reduced virus-specific CD8+ T cell numbers and compromised recall responses. PD-1 blockade during priming leads to similar differences early post-infection but without the defect in memory formation, suggesting that timing and/or duration of PD-1 blockade could be tailored to modulate host responses. Our studies reveal a role for PD-1 as an integrator of CD8+ T cell signals that promotes CD8+ T cell memory formation and suggest PD-1 continues to fine-tune CD8+ T cells after they migrate into non-lymphoid tissues. These findings have important implications for PD-1-based immunotherapy, in which PD-1 inhibition may influence memory responses in patients.The PD-1 pathway regulates dysfunctional T cells in chronic infection and cancer, but the role of this pathway during acute infection remains less clear. Here, we demonstrate that PD-1 signals are needed for optimal memory. Mice deficient in the PD-1 pathway exhibit impaired CD8+ T cell memory following acute influenza infection, including reduced virus-specific CD8+ T cell numbers and compromised recall responses. PD-1 blockade during priming leads to similar differences early post-infection but without the defect in memory formation, suggesting that timing and/or duration of PD-1 blockade could be tailored to modulate host responses. Our studies reveal a role for PD-1 as an integrator of CD8+ T cell signals that promotes CD8+ T cell memory formation and suggest PD-1 continues to fine-tune CD8+ T cells after they migrate into non-lymphoid tissues. These findings have important implications for PD-1-based immunotherapy, in which PD-1 inhibition may influence memory responses in patients. The PD-1 pathway regulates dysfunctional T cells in chronic infection and cancer, but the role of this pathway during acute infection remains less clear. Here, we demonstrate that PD-1 signals are needed for optimal memory. Mice deficient in the PD-1 pathway exhibit impaired CD8+ T cell memory following acute influenza infection, including reduced virus-specific CD8+ T cell numbers and compromised recall responses. PD-1 blockade during priming leads to similar differences early post-infection but without the defect in memory formation, suggesting that timing and/or duration of PD-1 blockade could be tailored to modulate host responses. Our studies reveal a role for PD-1 as an integrator of CD8+ T cell signals that promotes CD8+ T cell memory formation and suggest PD-1 continues to fine-tune CD8+ T cells after they migrate into nonlymphoid tissues. These findings have important implications for PD-1-based immunotherapy, in which PD-1 inhibition may influence memory responses in patients. The role of PD-1 in memory development is poorly understood. Here, Pauken et al. show that constitutive loss of PD-1 during acute infection causes overactivation of CD8+ T cells during the effector phase and impairs memory and recall responses. These data indicate PD-1 is required for optimal memory. The PD-1 pathway regulates dysfunctional T cells in chronic infection and cancer, but the role of this pathway during acute infection remains less clear. Here, we demonstrate that PD-1 signals are needed for optimal memory. Mice deficient in the PD-1 pathway exhibit impaired CD8+ T cell memory following acute influenza infection, including reduced virus-specific CD8+ T cell numbers and compromised recall responses. PD-1 blockade during priming leads to similar differences early post-infection but without the defect in memory formation, suggesting that timing and/or duration of PD-1 blockade could be tailored to modulate host responses. Our studies reveal a role for PD-1 as an integrator of CD8+ T cell signals that promotes CD8+ T cell memory formation and suggest PD-1 continues to fine-tune CD8+ T cells after they migrate into non-lymphoid tissues. These findings have important implications for PD-1-based immunotherapy, in which PD-1 inhibition may influence memory responses in patients. [Display omitted] •Early loss of PD-1 leads to overactivation of CD8+ T cells during acute infection•Mice constitutively lacking PD-1 or PD-L develop impaired CD8+ T cell memory•Cell-intrinsic PD-1 signals suppress effector cell expansion and promote memory•Timing of PD-1 blockade determines impact on memory generation The role of PD-1 in memory development is poorly understood. Here, Pauken et al. show that constitutive loss of PD-1 during acute infection causes overactivation of CD8+ T cells during the effector phase and impairs memory and recall responses. These data indicate PD-1 is required for optimal memory. The PD-1 pathway regulates dysfunctional T cells in chronic infection and cancer, but the role of this pathway during acute infection remains less clear. Here, we demonstrate that PD-1 signals are needed for optimal memory. Mice deficient in the PD-1 pathway exhibit impaired CD8 T cell memory following acute influenza infection, including reduced virus-specific CD8 T cell numbers and compromised recall responses. PD-1 blockade during priming leads to similar differences early post-infection but without the defect in memory formation, suggesting that timing and/or duration of PD-1 blockade could be tailored to modulate host responses. Our studies reveal a role for PD-1 as an integrator of CD8 T cell signals that promotes CD8 T cell memory formation and suggest PD-1 continues to fine-tune CD8 T cells after they migrate into non-lymphoid tissues. These findings have important implications for PD-1-based immunotherapy, in which PD-1 inhibition may influence memory responses in patients.
ArticleNumber	107827
Author	Godec, Jernej Imam, Sabrina Sharpe, Arlene H. Freeman, Gordon J. Wherry, E. John Odorizzi, Pamela M. Brown, Keturah E. Ali, Mohammed-Alkhatim Francisco, Loise M. Yates, Kathleen B. Ngiow, Shin Foong Pauken, Kristen E. Haining, W. Nicholas Grande, Shannon M. Maleri, Seth Burke, Kelly P.
AuthorAffiliation	6 Division of Hematology/Oncology, Children’s Hospital, Harvard Medical School, Boston, MA 02115, USA 7 Department of Pathology, Brigham and Women’s Hospital, Boston, MA 02115, USA 9 These authors contributed equally 3 Institute for Immunology and Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA 2 Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA 02115, USA 5 Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA 1 Department of Immunology, Blavatnik Institute, Harvard Medical School, and Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA 02115, USA 4 Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02115, USA 8 These authors contributed equally 10 Lead Contact
AuthorAffiliation_xml	– name: 9 These authors contributed equally – name: 3 Institute for Immunology and Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA – name: 8 These authors contributed equally – name: 1 Department of Immunology, Blavatnik Institute, Harvard Medical School, and Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA 02115, USA – name: 7 Department of Pathology, Brigham and Women’s Hospital, Boston, MA 02115, USA – name: 4 Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02115, USA – name: 6 Division of Hematology/Oncology, Children’s Hospital, Harvard Medical School, Boston, MA 02115, USA – name: 10 Lead Contact – name: 2 Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA 02115, USA – name: 5 Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA
Author_xml	– sequence: 1 givenname: Kristen E. surname: Pauken fullname: Pauken, Kristen E. organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, and Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA 02115, USA – sequence: 2 givenname: Jernej surname: Godec fullname: Godec, Jernej organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, and Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA 02115, USA – sequence: 3 givenname: Pamela M. surname: Odorizzi fullname: Odorizzi, Pamela M. organization: Institute for Immunology and Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA – sequence: 4 givenname: Keturah E. surname: Brown fullname: Brown, Keturah E. organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, and Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA 02115, USA – sequence: 5 givenname: Kathleen B. surname: Yates fullname: Yates, Kathleen B. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA 02115, USA – sequence: 6 givenname: Shin Foong surname: Ngiow fullname: Ngiow, Shin Foong organization: Institute for Immunology and Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA – sequence: 7 givenname: Kelly P. surname: Burke fullname: Burke, Kelly P. organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, and Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA 02115, USA – sequence: 8 givenname: Seth surname: Maleri fullname: Maleri, Seth organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, and Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA 02115, USA – sequence: 9 givenname: Shannon M. surname: Grande fullname: Grande, Shannon M. organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, and Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA 02115, USA – sequence: 10 givenname: Loise M. surname: Francisco fullname: Francisco, Loise M. organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, and Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA 02115, USA – sequence: 11 givenname: Mohammed-Alkhatim surname: Ali fullname: Ali, Mohammed-Alkhatim organization: Institute for Immunology and Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA – sequence: 12 givenname: Sabrina surname: Imam fullname: Imam, Sabrina organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA 02115, USA – sequence: 13 givenname: Gordon J. surname: Freeman fullname: Freeman, Gordon J. organization: Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02115, USA – sequence: 14 givenname: W. Nicholas surname: Haining fullname: Haining, W. Nicholas organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA 02115, USA – sequence: 15 givenname: E. John surname: Wherry fullname: Wherry, E. John email: wherry@pennmedicine.upenn.edu organization: Institute for Immunology and Department of Systems Pharmacology and Translational Therapeutics, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA – sequence: 16 givenname: Arlene H. surname: Sharpe fullname: Sharpe, Arlene H. email: arlene_sharpe@hms.harvard.edu organization: Department of Immunology, Blavatnik Institute, Harvard Medical School, and Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA 02115, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/32610128$$D View this record in MEDLINE/PubMed
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Keywords	influenza checkpoint blockade memory acute infection PD-L1 PD-L2 effector PD-1 CD8+ T cell CD8(+) T cell
Language	English
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS K.E.P., J.G., P.M.O., K.E.B., E.J.W., and A.H.S. conceived the studies. K.E.P., J.G., P.M.O., K.E.B., M.-A.A., S.F.N., K.P.B., and S.M. performed experiments and generated primary data, including developing methodology, validation, and data curation. K.E.P., J.G., P.M.O., and K.E.B. performed formal analysis and visualization. S.M.G., L.M.F., and M.-A.A. assisted in animal colony maintenance and performing some mouse experiments. K.B.Y., S.I., and W.N.H. performed and analyzed transcriptional profiling data. K.E.P., J.G., P.M.O., K.E.B., G.J.F., E.J.W., and A.H.S. contributed to writing the manuscript. All authors contributed to reviewing and editing the final manuscript. E.J.W. and A.H.S. were responsible for project supervision, administration, and funding acquisition.
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Snippet	The PD-1 pathway regulates dysfunctional T cells in chronic infection and cancer, but the role of this pathway during acute infection remains less clear. Here,... The PD-1 pathway regulates dysfunctional T cells in chronic infection and cancer, but the role of this pathway during acute infection remains less clear. Here,...
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SubjectTerms	acute infection Administration, Intranasal Animals CD8+ T cell CD8-Positive T-Lymphocytes - immunology Cell Death - immunology Cell Differentiation - immunology Cell Proliferation checkpoint blockade effector Immunologic Memory influenza Influenza A Virus, H3N2 Subtype - physiology memory Mice, Inbred C57BL Orthomyxoviridae Infections - immunology Orthomyxoviridae Infections - pathology Orthomyxoviridae Infections - virology PD-1 PD-L1 PD-L2 Programmed Cell Death 1 Receptor - metabolism Signal Transduction Species Specificity
Title	The PD-1 Pathway Regulates Development and Function of Memory CD8+ T Cells following Respiratory Viral Infection
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